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IJA E
Italian Journal of Anatomy and Embryology
Official Organ of the Italian Society
of Anatomy and Histology
Vol. 121
N. 2
2016
FIRENZE ISSN 1122-6714
UNIVERSITY
PRESS
IJA E
It a l i a n J o u r n a l o f A n a t o m y a n d E m b r y o l o g y
O f f i c i a l O r g a n of t h e It a l i a n S o c i e t y of A n a t omy a n d H i s t o l o g y
Founded by Giulio Chiarugi in 1901
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Pepa Atanassova (Plovdiv, Bulgaria)
Daniele Bani (University of Florence, Italy)
Raffaele De Caro (University of Padua, Italy)
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Antonio Filippini (University of Rome “La Sapienza”, Italy)
Eugenio Gaudio (University of Rome “La Sapienza”, Italy)
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Menachem Hanani (Hebrew University of Jerusalem)
Nadir M. Maraldi (University of Bologna, Italy)
Hanne B. Mikkelsen (University of Copenhagen)
Giovanni Orlandini (University of Florence, Italy)
Maria Simonetta Pellegrini Faussone (University of Florence, Italy)
Alessandro Riva (University of Cagliari, Italy)
Ajai K. Srivastav (Gorakhpur, India)
Gabriella B. Vannelli (University of Florence, Italy)
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IJA E
Vo l . 121, n . 2: 12 3 -132, 2016
I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Basic and applied anatomy
Retrotransverse foramen in atlas vertebrae of the late
17th and 18th centuries
Laura Quiles-Guiñau1,*, Azucena Gómez-Cabrero2, Marcos Miquel-Feucht1, Luís Aparicio-Bellver1
1
2
Department of Anatomy and Human Embryology. School of Medicine. University of Valencia, Spain
Department of Hematology and Oncology. Children’s Hospital Los Angeles. Los Angeles, USA
Abstract
Anatomical variations of the atlas vertebra are of particular importance because of their possible repercussions on the vertebral vessels. In view of the extensive articular mobility of the
atlas, any anomaly where the vertebral artery and veins run through the transverse foramen
could impair blood flow. However, in spite of the possible effect of this anomaly on the vertebral artery and veins, there are few data on the presence of an abnormal accessory transverse
foramen, termed retrotransverse foramen, which is smaller and located behind the transverse
foramen of the atlas. The aim of this research was to analyse the prevalence of retrotransverse
foramen in a sample of 88 dry C1 vertebrae from a Spanish rural population of the late 17th and
the early 18th centuries, as well as to study the possible repercussions of the presence of this
anatomical variant on the size of the transverse foramen. The anteroposterior diameter and the
lateral diameter of the transverse foramen of all the atlas vertebrae and retrotransverse foramina were measured using digital calibres. Two atlases with retrotransverse foramina (2.27%)
were found in which the presence of the anatomical variant caused a larger anteroposterior
diameter and a smaller lateral diameter than those of the transverse foramina of the normal 86
C1 vertebrae that were analysed. Our results show that a thorough study should be performed
on the prevalence of this anatomical variant in the current population, as well as its possible
clinical repercussion on the vertebral artery.
Key words
Cervical atlas, anatomical variation, transverse foramen, Spain
Introduction
The unique morphology of the first cervical vertebra makes it clearly different
from the rest of the cervical vertebrae. The key role the atlas plays in the biomechanics of the craniovertebral junction induces its characteristic ring shape. This vertebra is also particularly important in the way it affects the last section of the vertebral artery and vertebral veins. In the same way as occurs in the rest of the cervical
vertebrae, the atlas presents a transverse foramen (TF) in both transverse processes,
which the vertebral artery and vertebral veins run through. Once the vertebral artery
emerges from the TF of C1, it continues on with the dorsal ramus of the first cervical spinal nerve and venous plexus along a groove, which varies in size and depth,
in the posterior arch of the atlas and eventually enters the cranial cavity through the
foramen magnum.
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18485
124
Laura Quiles-Guiñau et alii
Given the extensive articular mobility the cervical spine presents, particularly the
atlas, any anomaly where the vertebral vessels run through the TF of the atlas could
impair the blood flow. Added to this critical situation is the high anatomical variability of the atlas (Wysocki et al., 2003). One of the morphological variants that could
affect the vertebral vessels is the presence of an abnormal accessory foramen on the
posterior root of the transverse process, called retrotransverse foramen (RF), which
is smaller and located behind the TF of the atlas and is formed by a bony bridge
extending from the posterior root of the transverse process to the root of the posterior
arch of the atlas. Since the existing studies on this variant were carried out on dry
vertebral samples (Veleanu et al., 1977; Gupta et al., 1979; De Boeck et al., 1984; De
Sousa et al., 1989; Le Minor, 1997; Jaffar et al., 2004; Bilodi and Gupta, 2005; Paraskevas et al., 2005; Chinnappan and Manjunath, 2008; Nayak, 2008; Karau et al., 2010;
Agrawal et al., 2012; Gupta et al., 2013; Karau and Odula, 2013; Rekha and Neginhal, 2014), there are few studies that give information about the structures that run
through it or describe their possible clinical implications (Dubreuil-Chambardel, 1921;
Veleanu et al., 1977), such as headache, migraine and loss of consciousness relating
to certain neck movements (Nayak, 2008). Furthermore, the key position of the RF
with regard to the passage and calibre of the vertebral vessels should be taken into
account in surgical procedures that involve the atlas.
The aim of this work is to determine the prevalence of the presence of RF in a
sample of atlas vertebrae in a Spanish rural population from the late 17th to the early
18th centuries, as well as to analyse the possible repercussion of the presence of this
anatomical variant on the size of the TF by means of measuring the anteroposterior
diameter and the lateral diameter of the TF of normal C1 vertebrae compared with
those with RF.
Material and methods
Atlas vertebrae samples used in this study were discovered between 1999 and
2005 during restoration works at the fortress-church “Nuestra Señora de los Ángeles”, in Castielfabib (Rincón de Ademuz, Valencia, Spain). The buried osseous
remains found under its floors and within its walls date from the late 17th to the early
18th centuries, as has been revealed by the objects found in the tombs as well as by
the historical context.
Skeletal samples were labelled according to their stratigraphic unit and analysed
at the Anthropometry and Paleopathology Laboratory, Department of Anatomy and
Human Embryology, University of Valencia, as recommended by the Spanish forensic anthropology and odontology association known as “Asociación Española de
Antropología y Odontología Forense” (Serrulla, 2013).
Bone samples were initially cleaned with a soft-bristle brush under a constant
low-pressure water jet and then dried under mechanical ventilation at room temperature (Serrulla, 2013). After drying no consolidation procedures were necessary. The
species and anthropological identification was based on a morphological and morphometric analysis (Reverte-Coma, 1991). An estimated minimum number of individuals was used whenever osseous remains were collected from common graves,
in which bone samples from two or more individuals are mixed. In the case of sin-
Retrotransverse foramen in atlas vertebrae
125
gle graves we took care to confirm that all the osseous remains belonged to the same
individual (Puchalt-Fortea and Villalaín-Blanco, 2000). Then, bones samples were separated as adult or child bones. Gender of adult skeletons was determined by bone
length of humerus, radius, femur and tibia, and by morphological traits of pelvis and
skull (Reverte-Coma, 1991).
Due to the lack of availability of old registers on age at death from each individual in the study, their age was estimated from sternal extremities and ribs traits (Burns,
2008), thyroid cartilage ossification (Loth and Iscan, 1989), cranial bone synostoses
and pubic symphysis morphology (Reverte-Coma, 1991). Adult individuals were classified by age in either 25-40 year-old or 41-65 year-old.
Only atlas vertebrae from adult skeletons with a clear-cut age and gender classification and complete cervical spine were used to measure vertebral TF anteroposterior
and lateral diameters, as well as those of the RF if it was present. Measurements were
done with a digital calibre Powerfix 0-150 mm, in triplicates, and their average was
used for further analysis.
We analysed if RF was present in each atlas. This variation could be present bilaterally or only on the left or the right side. In order to compare our results with previous published studies, we considered that a RF was present only if it was complete;
partial forms or transition types were not considered for analysis.
SPSS 15.0 software was used for statistical analysis. Levene test was used to confirm homogeneous variance between groups, and t-test was used to analyse statistical
significance. When the number of cases was low, a non-parametric Wilcoxon test was
used instead.
This study was approved by the Ethical Committee for Research on Humans
from the University of Valencia; furthermore, the corresponding authorisation was
obtained from the local authorities at “Consellería de Cultura de la Comunidad
Valenciana”.
Results
Among the 17th century osseous remains found in the fortress-church “Nuestra
Señora de la Ángeles” a total of 331 specimens were identified as humans, of whom
177 (53.47%) were adults.
As our study only focused on C1 vertebrae from skeletons with a complete cervical
spine whose gender and age were identifiable, we finally selected 88 adults, 36 (40.90%)
of whom were classified as male and 52 (59.09%) as female. The majority of these specimens were from individuals who had died between 25 and 40 years of age (64.09%).
There were two vertebrae that presented RF (2.27%) in the sample of 88 C1 vertebrae. One belonged to a woman, with left unilateral RF (Figures 1a,b) and the other
belonged to a man, with bilateral RF (Figures 1c,d) which also presented incomplete
closure of the right TF. In both cases the RF was smaller than the TF and located
on the posterior root of the transverse process. Table 1 shows the dimensions of the
anteroposterior diameter and lateral diameter of the TF of these two vertebrae, and
Table 2 shows the RF diameters.
When the TF diameters of the two atlases with RF were compared with those of
the remaining 86 normal C1 vertebrae, it could be seen that the TF in the two ver-
126
Laura Quiles-Guiñau et alii
Figure 1 - Two atlas vertebrae with retrotransverse foramen (RF). a: Upper view of a female atlas with RF in
the left side. b: Lower view of the same atlas as (a). c: Upper view of a male atlas with bilateral RF. d: Lower
view of the same atlas as (c).
tebrae that presented RF had a greater anteroposterior diameter and a smaller lateral diameter than those of the TF of the 86 normal C1 vertebrae that were analysed.
Nonetheless, these results were not statistically significant (Table 3).
Discussion
The morphological variant detailed in this study, which analyses two C1 vertebrae
with RF, has already been described in the literature as a smaller-sized foramen than
the TF located on the posterior root of the transverse process, as we also found (Sylla
et al., 1976; Veleanu et al., 1977; Gupta et al., 1979; De Boeck et al., 1984; Le Minor,
1997; Jaffar et al., 2004; Bilodi and Gupta, 2005; Paraskevas et al., 2005; Chinnappan
and Manjunath, 2008; Nayak, 2008; Karau et al., 2010; Agrawal et al., 2012; Gupta et
al., 2013; Karau and Odula, 2013; Rekha and Neginhal, 2014). However, the diversity of the nomenclature in these publications is striking. Numerous synonyms have
been used, leading to confusion: “secondary hole” (Sylla et al., 1976), “retrotransverse
canal” (Veleanu et al., 1977; Gupta et al., 1979; Bilodi and Gupta, 2005), “retrotransverse foramen” (De Sousa et al., 1989; Le Minor, 1997; Paraskevas et al., 2005; Karau
et al., 2010), “retroarticular canal” (Gupta et al., 2013), “abnormal foramen on the posterior arch of atlas” (Nayak, 2008; Agrawal et al., 2012; Gupta et al., 2013), “accessory
costotransverse foramen” (De Boeck et al., 1984), “accessory foramen transversarium”
(Jaffar et al., 2004; Chinnappan and Manjunath, 2008; Rajani, 2014), “double foramina” (Karau and Odula, 2013; Rekha and Neginhal, 2014) and “double transverse
127
Retrotransverse foramen in atlas vertebrae
Table 1 – Measurement of the transverse foramen of both C1 vertebrae with retrotransverse foramen (RF).
Lat Ø †
Right
AP Ø *
Left
-
-
7.0
5.5
7.1
5.7
7.0
5.4
AP Ø *
Right
Female C1 with left RF
Male C1 with bilateral RF
Lat Ø
Left
†
RF: retrotransverse foramen; * anteroposterior diameter of the transverse foramen (mm); † lateral diameter
of the transverse foramen (mm).
Table 2 – Measurement of the retrotransverse foramen (RF) of both C1 vertebrae with this anatomical variant.
AP Ø *
Right
Female C1 with left RF
Male C1 with bilateral RF
Lat Ø † Right
AP Ø *
Left
Lat Ø † Left
-
-
2.3
1.8
3.9
2.8
3.6
2.9
RF: retrotransverse foramen; * anteroposterior diameter of the retrotransverse foramen (mm); † lateral diameter of the retrotransverse foramen (mm).
Table 3 – Comparison between transverse foramen of C1 vertebrae with and without retrotransverse foramen (RF).
Presence of RF
C1
2 with RF
86 without RF
Ø AP *
Ø lat
†
Mean±SD
Range
p‡
0.337
Yes
7.0±0.1
7.0-7.1
No
6.9±0.8
5.0-8.3
Yes
5.5±0.1
5.4-5.7
No
5.8±0.9
4.1-8.3
0.593
RF: retrotransverse foramen; SD: standard deviation; * anteroposterior diameter of the transverse foramen
(mm); † lateral diameter of the transverse foramen (mm); ‡ p-value (Student’s t-test)
foramina” (Karau and Odula, 2013). Among the variety of nomenclatures used to
describe this anatomical variant, “retroarticular canal” (Gupta et al., 2013) particularly
causes confusion as it has also been used for another anatomical variant of the atlas,
the posterior bony ponticle or ponticulus posticus (Mitchell, 1998; Karau et al., 2010).
In our study we chose the term “retrotransverse foramen” since it was the most frequently used in previous studies.
Our population sample showed a lower prevalence of vertebrae with RF (2.27%)
than those of other authors (Table 4). Those studies were mostly based on dry vertebrae samples. The frequencies observed by previous authors vary between 3.57%
and 25.49%. In any case, the discrepancy between RF prevalence from different
studies could be due to the diverse ethnic origin of the population samples that
were studied.
The possible clinical repercussions of RF could depend on the contents of the RF
itself, although they could also depend on how the presence of this anatomical variant influences the size of the TF.
128
Laura Quiles-Guiñau et alii
Table 4 – Summary of retrotransverse foramen (RF) prevalence described in the literature.
Author and year
Origin
Total C1 C1 with RF Right RF
vertebrae
n (%)
n (%)
Left RF
n (%)
Bilateral
RF
n (%)
50 (dry
vertebrae)
32
(16.0%)
unilateral:
16
(8.0%)
16
(8.0%)
Velanu C et al (1977) Romania
71 (dry
vertebrae)
9
(12.6%)
2
(2.8%)
6
(8.4%)
1
(1.4%)
Gupta SC et al (1979) India
123 (dry
vertebrae)
23
(18.6%)
10
(8.1%)
8
(6.5%)
5
(4.0%)
55 (dry
vertebrae)
7
(12.7%)
n.d.
n.d.
n.d.
14 (CT
images)
1
(7.1%)
n.d.
n.d.
0
(0.0%)
Sylla S et al (1976)
Senegal
De Boeck M et al
(1984)
Belgium
De Sousa CA et al
(1989)
Portugal
200 (dry
vertebrae)
18
(9.0%)
n.d.
n.d.
n.d.
Le Minor JM (1997)
France
Austria
500 (dry
vertebrae)
71
(14.2%)
27
(5.4%)
23
(4.6%)
21
(4.2%)
Jaffar AA et al (2004) Caucasoid
29 (dry
vertebrae)
n.d.
(approx.
10%)
n.d.
n.d.
n.d.
Bilodi AK and Gupta
India
SC (2005)
34 (dry
vertebrae)
3
(8.8%)
2
(5.8%)
1
(2.9%)
0
(0.0%)
Chinnappan M and
India
Manjunath KY (2008)
102 (dry
vertebrae)
9
(8.8%)
5
(4.9%)
3
(2.9%)
1
(0.9%)
Nayak B et al (2008) India
1 (dry
vertebrae)
1
(-)
0
(-)
0
(-)
1
(-)
Karau PB et al (2010) Kenya
102 (dry
vertebrae)
26
(25.4%)
16
(15.6%)
10
(9.8%)
0
(0.0%)
Agrawal R et al
(2012)
India
28 (dry
vertebrae)
1
( 3.5%)
0
(0.0%)
0
(0.0%)
1
(3.5%)
Gupta C et al (2013)
India
35 (dry
vertebrae)
2
(5.7%)
n.d.
n.d.
n.d.
Karau PB et al (2014) Kenya
102 (dry
vertebrae)
4
(3.9%)
3
(2.9%)
1
(0.9%)
0
(0.0%)
Rekha BS et al (2014) India
153 (dry
vertebrae)
10
(6.5%)
4
(2.6%)
3
(1.9%)
3
(1.9%)
Present study
88 (dry
vertebrae)
2
(2.2%)
1
(1.1%)
0
(0.0%)
1
(1.1%)
Spain
RF: retrotransverse foramen; n: number of vertebrae analyzed; CT: computed tomography; n.d.: non disclosed.
Retrotransverse foramen in atlas vertebrae
129
There are few studies that describe the contents of the RF. Veleanu et al. (1977),
when analysing twelve cadavers, observed that the RF contained an anastomotic vein
connecting atlanto-occipital and atlanto-axodian venous sinuses. Dubreuil-Chambardel (1921) observed in some cases also a thin artery accompanying these venous
elements. Sylla et al. (1976) postulated that a dorsal branch of the first cervical spinal
nerve runs through the RF. Other authors hypothesised that the RF could separate
the passage of the vertebral artery and vein, or change the course of the vertebral
artery and lead to its compression (Nayak, 2008; Rajani, 2014), or that it could also
be related to the presence of a duplication of the vertebral artery (Kaya et al., 2011).
Whatever the case, according to the observations of Le Minor (1997), the RF appears
to be a variant that is absent in all nonhuman primates, which would support an evolutionary origin regarding the acquisition of bipedalism associated with adaptations
in the vascular system in response to hydrostatic pressure and gravity, draining the
blood from the cranium into the vertebral venous plexus. In favour of this hypothesis, Paraskevas et al. (2005) observed a high incidence of coexistence of the posterior
bridge of the atlas and the RF (72.22%), which they attributed to the blood flow being
directed into the small vein of the RF, possibly due to compression of the vertebral
veins in the posterior bridge.
With regard to the possible repercussion of the RF on the size of the TF, although
in our study the results were not statistically significant (perhaps due to the scarcity
of atlases with RF in our study sample), we observed that the presence of RF could
condition a small-sized TF when compared with normal C1 vertebrae. This is why
it is striking that among the authors who investigated this anatomical variant none
commented on this possible influence, which could affect the flow of blood in the
vertebral artery. Only the study by Agrawal et al. (2012) contributed data about the
dimensions of the anteroposterior diameter and the lateral diameter of the two RF
they analysed in an atlas, whose dimensions were 3 x 2 mm which is similar to what
observed in the three RF found in our study.
On the other hand, there are indeed studies that have measured the anteroposterior diameter and the lateral diameter of the TF of the atlas, but none of them
says whether the measurements were of C1 vertebrae with RF or not (Rocha et al.,
2007; Evangelopoulos et al., 2012; Gupta et al., 2013; Karau and Odula, 2013; Rekha
and Neginhal, 2014), except Taitz et al. (1978) who stated that in their sample of 33
atlas vertebrae none presented RF. Moreover, it is worth mentioning that the values for the anteroposterior diameter and the lateral diameter of the TF studied by
these authors are very similar to those observed in our study, as shown in Table
5. Regarding the methodology used in these studies, all of them based their calculations on samples of dry vertebrae (Taitz et al., 1978; Rocha et al., 2007; Gupta et
al., 2013; Karau and Odula, 2013; Rekha and Neginhal, 2014), with the exception of
Evangelopoulos et al. (2012) who analysed computed tomography (CT) images of the
atlas. Other authors have turned their attention to measuring the area of the TF of the
C1 using the formula to calculate the area of an ellipse (Jaffar et al., 2004; Karau and
Odula, 2013), but their results should be considered merely as approximate as the
shape of the TF is not an even oval. Therefore, in order to obtain more precise results
that could help to elucidate the possible effect of RF on the size of the TF of C1, it
would be necessary to perform a study on the area of TF and RF using CT images of
the atlas.
130
Laura Quiles-Guiñau et alii
Table 5 – Measurements of anteroposterior and lateral diameters of the transverse foramen of C1 previously
published in the literature.
Author and year
Taitz C et al (1978)
Rocha R et al (2007)
Origin of
the sample
n
India and
Israel
33
Brazil
20
AP Ø *
Mean±SD
Greece
Gupta C et al (2013)
n.d.
35
Karau PB et al (2013)
Kenia
102
Rekha BS et al (2014)
India
153
Present study
Spain
86
Lat Ø †
Mean±SD
Range
(mm)
Rigt
7.2±0.8
5.1-8.9 Rigt
5.5±0.9
3.8-7.6
Left
7.2±0.9
5.4-8.9 Left
5.7±0.7
4.0-7.4
Rigt
7.3±1.1
5.6-9.4 Rigt
6.6±0.9
5.3-8.1
Left
7.2±1.1
5.2-9.0 Left
6.5±0.9
5.2-8.0
♂ 7.0±0.9
Rigt
♀ 6.8±1.0
50 ♂
50 ♂
♂ 7.5±1.1
Left
♀ 7.4±0.8
Evangelopoulos DS et al
(2012)
Range
(mm)
n.d.
7.0±n.d.
n.d.
♂ 7.2±1.2
Rigt
♀ 6.8±1.2
n.d.
n.d.
Left
♂ 7.4±1.2
♀6.8±0.9
n.d.
n.d.
5.7±n.d.
n.d.
6.5±n.d.
5.2-6.7
n.d.
Rigt
7.9±1.0
5.0-11.9 Rigt
6.3±0.9
4.1-9.1
Left
7.7±0.9 4.6-10.0 Left
6.3±1.0
4.6-9.1
6.9±0.8
5.0-8.3
5.8±0.9
4.1-8.3
n: number of vertebrae analyzed; * anteroposterior diameter of the transverse foramen (mm); † lateral
diameter of the transverse foramen (mm); SD: standard deviation; n.d.: non disclosed.
The results contributed by this study on RF should encourage professionals to
perform a wider-ranging analysis of the prevalence of this anatomical variant in a
present-day population sample. Moreover, due to the possible influence the RF may
have on the size of the TF, and consequently on the flow of blood in the vertebral
artery, it would be interesting to base subsequent analyses on an extensive sample
of CT images of C1 which would permit an exact calculation of the area of the TF
on the basis of the presence or absence of RF. It would also be necessary to establish unequivocally what anatomical structures run through the RF, either by means of
imaging techniques in vivo or by dissecting large series of cadavers. In any case, the
analysis and understanding of the RF is of the utmost importance for medical professionals, especially orthopaedic surgeons, radiologists and neurosurgeons, for greater
precision and safety in surgical procedures of the cervical spine.
Conflict of interest
The authors have no conflict of interest to declare.
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IJA E
Vo l . 121, n . 2: 133 -137, 2016
I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Education in anatomy and embryology
Students’ opinion towards the Pernkopf atlas: are the
Italian students ready to know the history?
Daniele Gibelli*, Chiarella Sforza
Department of Biomedical Sciences for Health, University of Milan, Italy
Abstract
The debate around Pernkopf’s atlas, the origin of bodies used to create its plates and the person
of Eduard Pernkopf has involved with time academic authorities and university professors, and
has shaken the anatomical scenario. However, no study has been so far performed concerning
the opinion of students towards this sensitive and problematic issue. This article aims at exposing the results of an interview performed on 42 Italian medical students, after a self-chosen
course of history of human anatomy, in order to ascertain the students’ opinion towards this
important debate in the anatomic scenario. Results showed that 91% of students did not know
the existence of Pernkopf’s atlas: 51% stated they would not use it, whereas for 65% it should
be preserved for didactic purposes. Subjects who preferred the atlas to be banished justified
their position mainly on the base of ethical reasons (25%); however, in a third of cases students
were not able to give an answer. Twenty-two percent of students who agree with a preservation of the atlas would limit its use to historical studies. In 11% ethical issues were not considered important. In 52% of cases no opinion was given. Results show that the debate concerning
Pernkopf’s atlas, at least among students, is at the very beginning: more efforts need to be performed in order to let the medical students know the history of the atlas and its importance in
the scientific debate around the ethics in anatomy.
Key words
Anatomy, history of anatomy, ethics
Introduction
Pernkopf’s “Topographische Anatomie des Menschen” (Topographical Anatomy of Man) is one of the most acclaimed atlases of human anatomy, developed by
Prof. Eduard Pernkopf of the University of Vienna in the first half of the 20th century, currently at the centre of an intense scientific debate concerning the origin of the
work and the figure of the author (Israel and Seidelman, 1996). Eduard Pernkopf in
fact is known as a leading supporter of Hitler’s Nazi party, together with the artists
involved in the production of figures. This aspect is also proved by the first edition of
the atlas containing several swastikas and other signs of the Nazi regime, which were
removed in more recent editions (Hubbard, 2001). The debate begun in 1995 when
the Jewish Holocaust Remembrance Authority, Yad Vashem, requested the authorities
of the University of Vienna to conduct an inquiry on the Pernkopf atlas in order to
ascertain the possible use of bodies from victims of Nazi concentration camps (Israel
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18486
134
Daniele Gibelli, Chiarella Sforza
and Seidelma, 1996). After this event, the scientific community became aware of the
issue, which led to the publication of several articles and comments concerning this
sensitive topic, also within universities: several institutions in fact decided to remove
the Pernkopf atlas from their didactic programs (Panush, 1996). The inquiry ascertained that between 1938 and 1945 3,964 unclaimed or donated bodies and 1,377 bodies of executed persons (guillotined at the Vienna assize court or shot by the Gestapo
at a rifle range) were delivered to the Anatomical Institute of Vienna (Malina and
Span, 1999; Angetter, 2000). In addition, 41 plates on 791 illustrations of the original
atlas were signed with dates from the Nazi period and it is likely that at least some of
the models came from the group of executed victims (Hildebrandt, 2006).
Additional information was given by three Pernkopf’s collaborators (Prof. W.
Kraus; Prof. A. Gisel; Prof. W. Platz) who were interviewed in 2006 and confirmed
the arrival of bodies from executed victims at the University of Vienna, including also
Jewish victims (Aharinejad and Carmichael, 2013). The three witnesses in a similar
way disregarded the origin of bodies, as also highlighted by an answer provided by
Prof. Kraus (“nobody cared, and why should have we cared?”).
The scientific debate has led since the beginning to two opposite views concerning the future of Pernkopf atlas: on one side Panush and Briggs (1995) requested the
Pernkopf atlas to be removed from all the libraries, stating that nobody should take
advantages from the victims of Nazi regime and the use of the atlas could risk to
justify the committed atrocities. In addition, Pernkopf’s work can now be replaced
by other anatomical atlases, advanced by the modern means of medical imaging and
technology. On the other side, a group of authors suggests to continue to use the
atlas, preferably in its first edition with Nazi symbols as a historical documentation
with notes and comments concerning the origin, stating that the use of the atlas could
honour the victims of Nazi regime (Atlas, 2001).
As one can observe, the case of Pernkopf’s atlas involves academic authorities
and universities, but no specific articles have been so far published concerning the
opinion of students, and if they are aware of the history. Yet they are the first figures
involved in the use of the atlas and their opinion is important to correctly address
this sensitive issue.
This article aims at exposing the results of an interview performed on 42 Italian
medical students, after a self-chosen course of history of human anatomy: the results
may provide a general idea concerning the students’ opinion towards this important
debate in the anatomic scenario.
Materials and methods
Forty-two medical students (17 males and 25 females, mean age 22.1 years, SD 4.8
years) attended a self-chosen six-hour course of history of human anatomy in two
lectures. Some among the students were still attending the regular lectures of anatomy. Within the course the specific issue of Pernkopf atlas together with the historical
evolution of the debate and the different views concerning its use for didactic purposes were exposed. At the end of the course, the students were requested to compile
an anonymized questionnaire, containing the following questions:
1) Do you known Pernkopf’s atlas?
135
Italian students and the Pernkopf atlas
2) After having known its history, do you think you would use it?
3) Do you agree with the view of banishment or preservation of Pernkopf’s
atlas in the academic field (according to Panush and Briggs’ and Atlas’ views)? Why?
Answers were evaluated in order to highlight the public opinion among students
concerning the issue of Pernkopf atlas.
Results
Among forty-three students, only three admitted to know Pernkopf’s atlas (7%),
and one gave no answer; in 91% cases the atlas and its history were unknown.
The second question requested the students to specify if they would use the atlas,
once they have known the history: 51% provided a negative answer, whereas 35%
were likely to use Pernkopf’s atlas. In 12% of cases no answer was given. Results
vary according to the sex: males almost homogeneously divided within the categories of positive and negative opinion, whereas 64% of females would not use the atlas
after having known its history (Table 1).
For what concerns the third question, almost two thirds of cases agreed with
Atlas’ view (the atlas should be preserved), also in this case with differences between
males and females (respectively 72.2% versus 60%).
Interesting data came from the analysis of the reasons given by the students for
their answer: students agreeing with Panush and Gribbs’ view stated that the use of
the atlas does not actually honour the victims (25%) and it is unethical (25%), and
that other textbooks make it useless (17%). However, 33% did not provide an answer.
On the contrary, students on the Atlas’ side stated that the atlas is useful (7%) and
its use does honour the victims of Nazi regime (4%); however, 22% thought that the
atlas should be preserved only as a historical document and not for anatomic studies. In addition, 11% thought that the ethical debate is secondary in comparison with
scientific advantages deriving from the atlas; in 4% of cases the use of the atlas was
justified by the sentence “the evil has been done”. In 52% of cases students gave no
answer.
Discussion
Pernkopf’s atlas is at the centre of an intense debate concerning the ethical limits
of anatomical research and the question concerning the possible separation of a uni-
Table 1 – Answers to question “After having known its history, do you think you would use Pernkopf’s atlas”,
depending on gender. Data as percentage and number.
Males
Females
I would use the atlas
41% (7)
32% (8)
I would not use the atlas
35% (6)
64% (16)
No answer given
24% (4)
4% (1)
IJA E
Italian Journal of Anatomy and Embryology
Official Organ of the Italian Society
of Anatomy and Histology
Vol. 121
N. 2
2016
FIRENZE ISSN 1122-6714
UNIVERSITY
PRESS
IJA E
It a l i a n J o u r n a l o f A n a t o m y a n d E m b r y o l o g y
O f f i c i a l O r g a n of t h e It a l i a n S o c i e t y of A n a t omy a n d H i s t o l o g y
Founded by Giulio Chiarugi in 1901
Editor-in-Chief
Paolo Romagnoli
Assistant Editors
Maria Simonetta Pellegrini Faussone
Gabriella B. Vannelli
Past-Editors
I. Fazzari – E. Allara – G.C. Balboni – E. Brizzi – G. Gheri
Editorial Board
Giuseppe Anastasi (University of Messina, Italy)
Pepa Atanassova (Plovdiv, Bulgaria)
Daniele Bani (University of Florence, Italy)
Raffaele De Caro (University of Padua, Italy)
Mirella Falconi Mazzotti (University of Bologna, Italy)
Antonio Filippini (University of Rome “La Sapienza”, Italy)
Eugenio Gaudio (University of Rome “La Sapienza”, Italy)
Krzysztof Gil (Jagiellonian University of Krakow, Poland)
Menachem Hanani (Hebrew University of Jerusalem)
Nadir M. Maraldi (University of Bologna, Italy)
Hanne B. Mikkelsen (University of Copenhagen)
Giovanni Orlandini (University of Florence, Italy)
Maria Simonetta Pellegrini Faussone (University of Florence, Italy)
Alessandro Riva (University of Cagliari, Italy)
Ajai K. Srivastav (Gorakhpur, India)
Gabriella B. Vannelli (University of Florence, Italy)
Contact
Prof. Paolo Romagnoli
Department of Anatomy, Histology and Forensic Medicine
Section “Enrico Allara”, Viale Pieraccini 6, 50139 Firenze (Italy)
Phone: +39 055 4271389 - Fax: +39 055 4271385
E-mail: [email protected] - [email protected]
Journal e-mail: [email protected] – Web site: http://www.fupress.com/ijae
© 2016 Firenze University Press
Firenze University Press
via Cittadella, 7
I-50144 Firenze, Italy
E-mail: [email protected]
Available online at
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For Subscriptions
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E-mail: [email protected]
136
Daniele Gibelli, Chiarella Sforza
versally recognized masterpiece from the behaviour and personality of the authors.
Discussions concerning Pernkopf’s atlas involved university authorities, professors,
scientific articles, and remain still without a common solution, although its volumes
have no longer been published (Hubbard, 2001). However the medical students have
not yet been involved in the discussion, although they are the first persons who may
use the plates of the atlas. This study for the first time asked students to give an
opinion concerning this sensitive issue: results highlight interesting points of discussion and confirm once again that the debate is still open.
Interestingly, in 51% of cases Italian students stated that they would not use the
atlas, with different percentages between males and females: the refusal of the atlas is
more pronounced in females (64%), whereas males did not show a clear answer, with
almost a quarter of students without an opinion. This result may be due to the different “sensitivity” of male and female population towards tragic events: however the
high percentage of students who did not give an answer is the sign of an incomplete
elaboration of the issue, which prevents from forming a precise opinion.
The choice for one of the two opposite opinions, banishment or preservation, was
more clear, with almost two thirds who agreed with the use of the atlas; however,
adducted motivations still show that a precise motivation has not yet been created.
Among students who preferred the atlas to be banned, one third of persons were
not able to give a precise reason, and even more problematic was the situation of students who agreed with preserving Pernkopf’s plates. They agreed with the preservation of the atlas, but in 52% of cases they are not able to say why. On the other
side, among those who gave an answer, 11% found that “ethical issues are of limited
importance” in comparison with scientific and didactic improvement, and 4% stated
that “the evil was done” and therefore it is preferable to keep the atlas. Undoubtedly these answers reflect a limited elaboration of ethical issues and testify that these
topics need to be strengthened in Italian Medical Schools. In addition, 22% of people
who agree with the preservation of Pernkopf’s atlas state that its use should be limited to the historical context: this opinion provides a limitation in its use which seems
more close to the positions of those who prefer to banish it.
In conclusion, Italian medical students seem still to have a primitive opinion concerning Pernkopf’s atlas and its history: this is probably due also to the scarce information about the scientific debate (91% of subjects did not know its existence). The
motivations leading to one or another position are expected to be confused as well.
However, this is the sign that the diffusion of literature concerning this case among
students needs to be improved in order to give to everyone the tools for creating an
opinion. Pernkpof’s atlas is not only a thorny issue, but also an important point of
debate which deals with ethics in anatomy, and reminds us, as underlined by Hildebrandt (2013), “to care”, in contrast with a model of anatomists who in the past had
learnt not to care the origin of the bodies and, probably, the nature itself of their discipline.
References
Aharinejad S.H., Carmichael S.W. (2013). First hand accounts of events in the laboratory of Prof. Eduard Pernkopf. Clin. Anat. 26: 297-303.
Italian students and the Pernkopf atlas
137
Angetter D.C. (1999). Die wiener anatomische Schule. Wien. Klin. Wochenschr. 111:
764-774
Atlas M.C. (2001). Ethics and access to teaching materials in the medical library: the
case of the Pernkopf atlas. Bull. Med. Libr. Assoc. 89: 51-58.
Hildebrandt S. (2006). How the Pernkopf controversy facilitated a historical and ethical analysis of the anatomical sciences in Austria and Germany: a recommendation for the continued use of the Pernkopf atlas. Clin. Anat. 19: 91-100.
Israel H.A., Seidelman W.E. (1996). Nazi origins of an anatomy text: the Pernkopf
atlas. JAMA 276: 1633.
Malina P., Spann G. (1999). Das Senatsprojekt der Universitaet Wien “Untersuchungen zur Anatomischen Wissenschaft in Wien 1938-1945”. Wien. Klin. Wochenschr.
111: 743-753
Panush R. (1996). Nazi origin of an anatomy text: the Pernkopf atlas. JAMA 276:
1633-1634
Panush R.S., Briggs R.M. (1995). The exodus of a medical school. Ann. Intern. Med.
123: 963.
IJA E
Vo l . 121, n . 2: 138 -147, 2016
I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Basic and applied anatomy
Description of an optic spine on the sphenoid bone of
camels and dromedaries
Gabrielle A. Fornazari1, Fabiano Montiani-Ferreira1,*, Jeverson C. Silva2, Ivan R. Barros1, Marcello
Z. Machado3
1
Universidade Federal do Paraná, Comparative Ophthalmology Laboratory, Curitiba-PR; 2 Universidade do Contestado, Departamento de Medicina Veterinária, Curso de Medicina Veterinária, Canoinhas-SC; 3 Universidade
Federal do Paraná - Departamento de Anatomia, Setor de Ciências Biológicas, Centro Politécnico, Curitiba-PR.
Brazil
Abstract
Objective To describe the presence of an intraorbital cylindrical osseous structure (a spine) in
two animal species: camel (Camelus bactrianus) and dromedary (Camelus dromedaries). A homologous osseous structure was previously observed in the large fruit-eating bat (Artibeus lituratus).
Procedures The bony anatomy of the orbital cavity was studied and quantified on macerated
skulls of 3 camels and 2 dromedaries. Additionally, one macerated skull of a large fruit-eating
bat (Artibeus lituratus) was used for comparative purposes.
Results The anatomic description of these unique intraorbital spine was made while studying
the bony orbit of macerated skulls, and was considered homologous to that of the bat based on
the same anatomic position (at the bone bridge that separates the optic canal and the sphenorbital fissure) and similarities in shape. We suggest the name optic spine of the sphenoid bone.
Discussion The novel observation of an optic spine on the sphenoid bone in camels and
dromedaries (Artiodactyla), when combined with the previous finding of a similar anatomic
structure in a bat (Chiroptera) suborder Microchiroptera, may provide further support to the
close proximity of these two apparently very distinct animal orders in the phylogenetic tree,
and may contribute to the understanding of bat evolution and provide new directions for
future research. The function of this osseous spine remains to be investigated, although we
hypothesize that the optic spine of the camelids may serve as an attachment site for extraocular muscles.
Key words
Anatomy, bony orbit, Camelus bactrianus, Camelus dromedaries, optic spine, sphenoid bone, comparative studies, mammals
Introduction
Evolutionary relationships among several different orders of the animal tree of life
have proven difficult to determine or have received little support in the vast majority
of phylogenomic studies of mammalian systematics, and thus remain unresolved at
best. Among those mammals with significant knowledge gaps are the bats (Chiroptera), despite representing one of the largest and most diverse radiations of mammals,
and accounting for one-fifth of extant species. Found worldwide, bats are also the only
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18487
Optic spine of camels and dromedaries
139
mammals to have achieved true self-powered flight, and they play a major ecological
role as pollinators and insect predators (Patterson et al., 2003; Simmons et al., 2008).
Currently the position of bats in the evolutionary tree of life is considered conflicting or incomplete, thus the phylogenetic and geographic origin of bats (and the
entire order Chiroptera) remains unclear. A plausible reason for this fact is that bats
are not well represented in the fossil record (Altringham, 1996; Nowak, 1999; Patterson et al., 2003; Springer et al., 2001; Van Den Bussche and Hoofer, 2004; Eick et
al., 2005; Gunnell and Simmons, 2005; Simmons et al., 2008). There are some possible
reasons for the lack of fossil evidence. One is that bats have small, delicate skeletons
that do not fossilize very well. Another is that most species live in tropical forests,
where conditions are usually unfavorable for the formation of fossils (Carroll, 1988).
Despite a poorly represented fossil record, even the earliest fossil bats dating back 45
to 50 million years ago have an outstanding resemblance to modern microbats, and
intriguingly no fossil bats have yet been identified that are in any way intermediate
in form between modern microbats and early tree-living ancestors (Altringham, 1996;
Nowak, 1999; Simmons et al., 1998; Springer et al., 2001; Eick et al., 2005; Teeling et
al., 2005). Thus, according to Altringham (1996), modern microbats may have made
their appearance about 65–100 million years ago. If so, they amazingly shared the
world with the dinosaurs, and watched their extinction at the end of the Cretaceous
period. Historically, the most common assumption about the evolutionary history of
bats has been based on morphological evidence, grouping bats with primates, flying
lemurs, and tree shrews to form the Archonta (Szalay, 1977; Novacek, 1992; Gunnell
and Simmons, 2005).
New genomic evidence demonstrates an unexpected sister relationship between
Chiroptera and Cetartiodactyla (Hallström and Janke, 2008; Nery et al., 2012, Zhang
et al. 2013). The curious and unusual phylogenetic position and consequent evolutionary proximity between Chiroptera and Artiodactyla has received genomic but no
real morphological support until now.
The skull has been used as a major skeletal structure to determine taxonomic affiliations as it is subject to phenotypic changes because of selective breeding (Bruenner
et al., 2002).
The objective of this study is to report the presence of an intraorbital cylindrical osseous structure, a spine, in two animal species: camel (Camelus bactrianus) and
dromedary (Camelus dromedaries). A homologous osseous structure in the bony orbit
was previously only observed in a bat (the large fruit-eating bat Artibeus lituratus)
(Machado et al., 2007). The observation of the same anatomic feature in the bony
orbit of both Artiodactyla (Old World camelids) and Chiroptera (bats, specifically
of the suborder Microchiroptera) may provide further support towards the growing
body of evidence suggesting close proximity of these two apparently very distinct
animal orders within the evolutionary tree.
Materials and methods
A thorough examination of the bony orbit from 5 previously macerated skulls
of Old World camelids (3 adult camels and 2 adult dromedariess) was performed,
including anatomic description and gross specimen morphometry. From the three
140
Gabrielle A. Fornazari et alii
camel skulls studied, two (from one 35 year-old male and one 21 year-old female)
belonged to the collection of Capão da Imbuia – Museum of Natural History (MHNCI) and one from a 34 year-old male belonged to the collection for environment education of the Curitiba Zoo, both institutions located in Curitiba-PR, Brazil. The two
dromedarian skull samples (one from a 23 year-old male and the other from an 18
year-old female) belonged to the Veterinary Anatomy Museum of the University of
Contestado, located in Canoinhas-SC, Brazil. One previously macerated skull of an
adult large fruit-eating bat (Artibeus lituratus) was used in this investigation for morphologic and photographic comparisons. This skull belonged to the private collection
of one of the authors (MM).
The camel skulls where previously naturally cleaned by a decomposition process
while the dromedarian skulls where prepared by a laboratorial maceration technique.
The skin and most of the soft tissues and eyes were removed to initially clean the
skulls, and then a maceration technique consisting of a boiling process followed by
cold water immersion in a closed recipient for two weeks was performed. After maceration the skulls were immersed in 50% hydrogen peroxide for approximately 24 h
for bleaching. Following this step they were washed in distilled water and air dried.
The nomenclature used for skull osteology follows previously published work on
osteology and camel anatomy (Smuts and Bezuidenhout, 1987; Olsen, 1988; Neumani,
1911; Shahid and Kausar, 2005; Yahaya et al., 2012 a,b).
The macerated skulls and optic spines were measured with a measuring tape,
a ruler, and a digital pachymeter, and were then digitally photographed. Selected
osteometric parameters were measured, according to Sarma (2006), Karimi 2011 and
Yahaya (2012 a,b) and orbital indexes calculated according to Kaur et al. (2012). Morphometric analysis of the skull included: Skull length, i.e. the interincisive space to
the most caudal aspect of the occipital bone (the intersection point between the sagittal and nuchal crest); skull width, i.e. the distance between the two most lateral
points of the frontal bones (the most lateral parts of the dorsal margin of the orbit)
(Fig. 1); intraorbital bony spine width at the base and at the tip, dorsal and ventral
lengths (Fig. 2C), bilaterally (Fig. 3); orbital horizontal and vertical diameters (Fig.
4). Additionally, orbital indexes were calculated as follows: Orbital index = Vertical
diameter of the orbit × 100/Horizontal diameter of the orbit.
Results are presented as mean ± the standard deviation (SD).
Results
The overall shape of the skull of camels and dromedaries is very similar (Fig. 1).
Both when viewed from above are roughly pentagonal in shape, elongated towards
the maxilla and mandible. Both are wider in the frontal bone region (skull width)
than between the zygomatic bones. The orbits are nearly circular and enclosed (complete) situated laterally and slightly cranially (Figs. 1 and 2). The rim of the frontal
bone is serrated (Fig. 2A). An irregular transverse elevation separates the parietal
and nuchal surfaces (Fig. 1). The occipital bone formed the entire nuchal surface and
invaded upon the dorsal surface. It joined the parietal bone at the transverse suture.
The sagittal and occipital crests on the dromedary are considerably more pronounced
or developed than those found in the camel skull.
Optic spine of camels and dromedaries
141
Figure 1 – Dorsal views of the skulls of a representative adult camel (A) and an adult dromedary (B). Legend:
Arrowheads represents the points to measurement of the skull length (interincisive space and the intersection point between the sagittal and nuchal crest), and arrows represents the points to measurement of the
interorbital length. Note that an irregular transverse elevation separates the parietal and nuchal surfaces.
Bar: 10 cm.
Inside the bony orbit we have observed an unusual osseous spine that is slender
and elongated in shape, directed rostrolaterally, and also slightly ventrally in camels (Camelus bactrianus) (Fig. 2A) and dromedaries (Camelus dromedaries) (Fig. 2B). It
is located bilaterally (Fig. 3) on the bone bridge that separates the optic canal and the
sphenorbital fissure on the sphenoid bone complex (Fig. 2C and Fig. 4) of these species. This bony spine is thin, cylindrical in shape, and tapers at its free rostral end in
both species (Fig. 2C). It is slightly wider at its sphenoid bone base in camels than in
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Gabrielle A. Fornazari et alii
Figure 2 – General topography and form of the optic spine of the sphenoid bone in Old World camelids.
Oblique dorsocaudal view of the left optic spine of the sphenoid bone of a camel (A), dorsolateral view of
the left optic spine of a dromedary (B), and ventrolateral view of the medial and caudal walls of the bony
orbit of a representative adult dromedary skull: note the discrete ridge formed where the optic spine meets
the sphenoid bone (C). The optic spine of the sphenoid (arrow) is clearly seen in these macerated skulls
without the aid of any magnifying device. Note that the orbit is complete and the optic spine of the camel
is slightly irregular at its free end, compared with the dromedaries. Ventral (arrow head) and dorsal (arrow)
bases of the optic spine of the sphenoid (os) can be seem. Legend: ethmoidal foramina (ef ), optic canal (oc),
orbital fissure (of ); orbitorotundum foramen (orf ). Bars: 1 cm.
dromedaries. In camels, the spine is slightly irregular at its free end (Fig. 1A). In both
species the optic spine length from the dorsal base to tip is shorter than the length of
the ventral base to tip, due to the presence of a discrete ridge at its dorsal junction to
the sphenoid bone.
Morphometry on dromedary skulls
The mean skull width was 24.75 ± 1.8 cm and the mean skull length was 41.33 ±
3.44 cm. The mean intraorbital bony optic spine length from the ventral base to tip
was 2.10 ± 1.06 cm and the length from the dorsal base to tip was shorter, measuring 1.25 ± 0.94 cm. The mean width was 0.34 ± 0.42 cm at the base and 0.21 ± 0.03
cm at the tip of the spine. The mean orbital horizontal diameter measured 6.26 ±
0.79 cm. The mean orbital vertical diameter was 6.11 ± 0.73 cm. The mean orbital
index was 102.45.
Morphometry on camel skulls
The mean skull width was 27.4 ± 2.7 cm and the mean skull length was 53.10 ±
2.82 cm. The mean intraorbital bony optic spine length from the ventral base to tip
was 2.11 ± 0.81 cm and the length from the dorsal base to tip was shorter, measuring
1.40 ± 0.30 cm. The mean width was 0.41 ± 0.56 cm at the base and 0.27 ± 0.09 cm at
Optic spine of camels and dromedaries
143
Figure 3 – Detail of the bilateral arrangement of the optic processes (arrows) of the sphenoid bone on a
ventral view of the base of the skulls of a representative adult camel (A; bar = 2 cm), an adult dromedary (B;
bar = 2cm), and an adult large fruit-eating bat (Artibeus lituratus) (C; bar = 2 mm). Note that although both
bony elements are rostrally oriented, the optic spine in the camel and in the dromedary are more laterally
oriented than the optic spine of the large fruit-eating bat .
the tip of the spine. The mean orbital horizontal diameter was 6.15 ± 0.44 cm. The
mean orbital vertical diameter was 5.92 ± 0.50 cm. The mean orbital index was 103.88.
Discussion
General osteology and osteometry of camel and dromedary skulls have been published elsewhere (Neumani, 1911; Olsen, 1988, Yahaya et al., 2012). Mean orbital horizontal diameter found in dromedaries investigated in the present work was similar to
the one (6.01 ± 0.07 cm) reported by Yahaya et al. (2012b). Mean orbital vertical diameter in dromedaries parallels results from Yahaya et al. (2012)b, which varied from
5.74 ± 0.12 cm to 6.12 ± 0.21 cm. Additionally, mean dromedary skull length found in
our investigation also was comparable to the data from Monfared (2013), which was
46.2 ± 2.74 cm and Yahaya (2012), which varied from 45.50 ± 0.65 cm to 49.44 ± 0.86
cm. Nevertheless, none of these previous studies described the presence of the optic
spine of the sphenoid bone. Orbital indexes of both species were considerably large.
Both were larger than the goat 86.11 to 92.14 (Sarma, 2006) but smaller than the Mehraban sheep, which varied from 108.38 from 109.07 (Karimi et al., 2011).
Despite being rather inconspicuous, these spines have remained undescribed in
Old World camelids until now, possibly because of the limited research available in
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Gabrielle A. Fornazari et alii
the literature regarding morphological features of their eye, adnexa and orbit (Neumani, 1911; Tayeb, 1951; Abdalla et al., 1970; Awkati and Al-Bagdadi, 1971; Smuts and
Bezuidenhout, 1987; Olsen, 1988; Abuel-Atta et al., 1997; Wang JL. 2002; Cui et al.,
2004; Shahid and Kausar, 2005; El-Tookhy et al., 2012; Yahaya et al., 2012a,b). Even
detailed studies of the cranioencephalic structures of dromedaries using diagnostic imaging techniques such as radiography (Saber, 1990), computed tomography
(Alsafy et al. 2014) and magnetic resonance (Arencibia et al., 2005) failed to detect
and describe the spines of the sphenoid bone.
Notwithstanding the scant information known about the evolutionary history of
bats, evidence suggests that bats may have originated in the northern supercontinent
of Laurasia, possibly in North America (Teeling et al., 2005) as part of a large group
of placental mammals (Laurasiatheria) including shrews, hedgehogs, pangolins,
whales, carnivorans, and most hoofed mammals such as camels, among others. Several questions still remain regarding how the different orders of several mammalians
in the supraordinal group Laurasiatheria evolved.
Traditionally bats were placed along with primates, flying lemurs, and tree
shrews, forming the Archonta on an anatomical basis (Szalay, 1977; Novacek, 1992).
However, in more recent phylogenetic analyses of the complete mitochondrial
genome of the Jamaican fruit bat (Artibeus jamaicensis), it appeared that bats may be
more closely related to “cetferungulates”, a clade including Cetacea, Artiodactyla,
Perissodactyla, and Carnivora (Pumo et al., 1998). Phylogenetic analyses from the
c-myc gene sequences also support this relationship (Miyamoto, 2000). Other phylogenetic investigations using relationships with genome data started to place bats near
cows (Hallström and Janke, 2008). Posteriorly, phylogenetic analyses investigating a
Figure 4 – Rostrolateral view of the bony orbit through the orbital adit of a representative adult camel skull.
Legend: dorsal margin of the orbit (dm); ethmoidal foramen (ef ), optic canal (oc), orbital fissure (of ); orbitorotundum foramen (orf ); optic spine of the sphenoid (op); ventral margin of the orbit (vm). Stars represent
the points to measurement of the orbital height (dorsoventral axis), and asterisks represents the points to
measurement of the orbital diameter (mediolateral axis). Bar: 1 cm.
very large amount of genomic sequence data have provided even greater and clearer
support for the sister relationship between Chiroptera and Cetartiodactyla (Nery et
al., 2012, Zhang et al., 2013). Cetartiodactyla is the clade in which whales and eventoed ungulates are currently placed. The term was coined by merging the name for
the two orders, Cetacea and Artiodactyla, into a single word. Cetacea includes whales
and dolphins. Artiodactyla includes pigs, peccaries, hippopotamuses, camel, dromedary, llamas, chevrotains (mouse deer), deer, giraffes, pronghorn, antelopes, sheep,
goats, and cattle.
Here, taking the current description into account and following the results from
Machado et al. (2007) in a bat, we provide anatomical evidence for the support of
a possible sister relationship between Chiroptera and Cetartiodactyla in the form of
intraorbital osseous spines. The first intraorbital osseous spine observed in an animal
was on the Artibeus lituratus (a large fruit-eating bat) (Machado et al., 2007). The is
a slender and elongated bony spine, directed rostrolaterally and slightly ventrally. It
is located bilaterally on the bone bridge that separates the optic canal and the sphe-
Optic spine of camels and dromedaries
145
norbital fissure on the alisphenoid bone (from the sphenoid complex) (Fig. 1C). The
group of researchers suggested the name optic spine of the alisphenoid bone. These
equivalent bony optic spines described here in Old World camelids are similar in anatomical position and general shape, but are more rostrolaterally oriented and slightly
less ventral than the spines of the large fruit-eating bat. Nevertheless, the anatomic
feature was thus far exclusively reported to Old World Camelids and the large fruiteating bat and was considered homologous based on the same anatomic position (at
the bone bridge that separates the optic canal and the sphenorbital fissure) and shape
similarities, which surpasses angular differences (Fig. 3).
Function of this osseous spine as well as potential differences in immature animals remains to be investigated. We hypothesize that the optic process of the camelids may serve as an attachment site for extraocular muscles in a similar manner to
the optic spine of the alisphenoid bone in bats (Machado et al., 2007). In order to
prove this assumption, future studies should perform a careful dissection in fresh
or fixed camelid skulls, paying special attention to the delicate attachments of the
extraocular muscles. The observation of an optic spine on the sphenoid bone in camels and dromedaries (Artiodactyla), when combined with the previous finding of a
such anatomic component in a bat (Chiroptera, suborder Microchiroptera), may provide further support to the close proximity of these two apparently very distinct animal orders in the phylogentic tree, and contribute to the understanding of bat evolution and perhaps provide new directions for future research.
Acknowledgements
The authors wish to thank the following: Bret A. Moore (College of Veterinary
Medicine and Department of Biological Sciences, Purdue University, West Lafayette,
IN) for his help in the preparation of this manuscript; Capão da Imbuia - Museum of
Natural History (MHNCI); Veterinary Anatomy Museum - Museu de Anatomia Veterinária da Universidade do Contestado - (MAV-UnC) and Prof. Rogério Lange (UFPR).
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IJA E
Vo l . 121, n . 2: 14 8 -158 , 2016
I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Basic and applied anatomy
The patellofemoral joint alignment in patients with
symptomatic accessory navicular bone
Heba M. Kalbouneh1,*, Abdullah O. Alkhawaldah2, Omar A. Alajoulin2, Mohammad I. Alsalem1
1
2
Department of Anatomy, Faculty of Medicine, University of Jordan, Amman, Jordan
Foot and Ankle Orthopedic Clinic, King Hussein Medical Center, Amman, Jordan
Abstract
Quadriceps angle (Q angle) provides useful information about the alignment of the patellofemoral joint. The aim of the present study was to assess a possible link between malalignment
of the patellofemoral joint and symptomatic accessory navicular (AN) bone as an underlying
cause in early adolescence using Q angle measurements.
This study was performed on patients presenting to the Foot and Ankle Clinic at the Jordanian Royal Medical Services because of pain on the medial side of the foot that worsened
with activities or shoe wearing, with no history of knee pain, between September 2013 and
April 2015. The Q angle was measured using a goniometer in 27 early adolescents aged 10-18
years diagnosed clinically and radiologically with symptomatic AN bone, only seven patients
had associated pes planus deformity; the data were compared with age appropriate normal
arched feet without AN. Navicular drop test (NDT) was used to assess the amount of foot
pronation.
The mean Q angle value among male and female patients with symptomatic AN with/without pes planus was significantly higher than in controls with normal arched feet without AN
(p<0.05). Symptomatic AN feet were also associated with higher NDT values (p<0.001).
The present findings suggest an early change in patellofemoral joint alignment in patients with
symptomatic AN bone with/without arch collapse. Therefore, it is recommended that Q angle
assessment should be an essential component of the examination in patients with symptomatic
AN bone.
Key words
Q angle, pes planus, patellofemoral joint, accessory navicular, navicular drop test
Introduction
An understanding of the normal anatomical and biomechanical features of the
patellofemoral joint is essential to evaluate the patellofemoral joint function and stability. The mechanical analysis of proper alignment and stability of any joint depends
mainly on the study of the effect of the structures surrounding that joint (Hehne,
1990). One such method is to study the effect of the muscles working on the joint by
applying the principles of vectors on each muscle. The angle that is formed by intersection of the muscles forces vectors gives an insight on the stability of that joint. It is
well known that the Quadriceps angle (Q angle) is a meaningful clinical measure to
assess the overall lateral line of pull of the quadriceps relative to the patella and pro* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18488
Q angle in symptomatic accessory navicular bone
149
vides useful information about the alignment of the patellofemoral joint (Biedert and
Warnke, 2001; Mizuno et al., 2001; Sanfridsson et al., 2001; Smith et al., 2008).
Q angle was firstly defined as the acute angle formed by the vector for the combined pull of the quadriceps femoris muscle and the patellar tendon (Brattstroem,
1964; Smith et al., 2008). This angle can be measured in supine or standing position
with the hip and knee extended and the quadriceps muscle relaxed (Omololu et al.,
2009). Many previous investigations have shown people with a larger Q angle (greater than 20 degrees) have a greater likelihood for developing numerous knee complaints (Horton and Hall, 1989).
Accessory navicular (AN) is an accessory ossicle of the foot which is located on
the medial side of foot, proximal to the navicular and in continuity with the tibialis
posterior tendon. It presents in 4-21% of the population. AN has three types; Type I
is a small separated ossicle, sized 2 to 3 mm, located in the distal portion of the tibialis posterior tendon. Type II measures up to 12 mm and is separated from the tuberosity of the navicular bone by less than 2 mm of fibrocartilaginous synchondrosis.
Type III is connected to the navicular tuberosity through a bony bridge. Type II and
III have been associated with pathologic conditions, often causing an alteration of the
line of pull of the tibialis posterior tendon as a result of the AN prominence. This
imbalance was thought to weaken the longitudinal arch and produce pronation of the
foot (Prichasuk and Sinphurmsukskul, 1995; Ugolini and Raikin, 2004). Pes planus
(flatfoot) deformity is characterized by loss of the medial longitudinal arch, forefoot
abduction and hindfoot eversion. There are various types and causes of flatfeet. An
association has been made between AN and pes planus deformity; nevertheless, the
causal relationship is still controversial (Sella et al., 1986; Prichasuk and Sinphurmsukskul, 1995; Leonard and Fortin, 2010; Park et al., 2014).
Based on our clinical experience, middle-aged and elderly patients with long
standing painful AN in their feet had frequent anterior knee complaints. For this
reason, the aim of the present study was to assess whether symptomatic AN bone
could have a possible consequence on malalignment of the patellofemoral joint in
early adolescence using the Q angle measurements, in order to improve the diagnosis
and early treatment, or prevention of the possible patellofemoral joint problems that
might be associated with this type of anatomic variant later in life.
Methods
Measurement of Q angle was recorded from 27 symptomatic patients (9 males, 18
females, age range 10–18 years) presented to our Foot and Ankle Clinic between September 2013 and April 2015 because of pain interfering with walking and sports, or
tenderness on the medial side of the foot that worsens with activities or shoe wearing.
Written informed consent was taken from each subject’s guardian. The research was
approved by the Ethics Committee of King Hussein Medical Center according to the
ethical principles of Helsinki Declaration. Radiologically, all patients had bilateral AN
confirmed by weight-bearing and non weight-bearing anterior-posterior/lateral X rays.
Accessory navicular patients were divided into three groups according to their
symptoms. Group 1 was composed of 20 patients with painful AN and normal arch
height (14 bilateral and six unilateral painful AN; Fig. 1). Group 2 consisted of seven
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Heba M. Kalbouneh et alii
Figure 1 – 14-year old boy with accessory navicular type II (arrow) associated with normal arch. A: AP-radiograph shows no midfoot pronation or forefoot abduction. B: lateral weight-bearing radiograph shows no
hindfoot equinus.
Q angle in symptomatic accessory navicular bone
151
Figure 2 – 10-year-old boy with accessory navicular type II (arrow) associated with pes planus. A: AP-radiograph shows midfoot pronation and forefoot abduction. B: lateral weight-bearing radiograph shows hindfoot equinus.
patients with symptomatic AN associated with pes planus (three unilateral and four
bilateral; Fig. 2). They were documented clinically and radiologically to have flattening of the medial longitudinal arch with an arch index (AI) larger than 0.32 (Murley
et al., 2009). Tarsal coalition or neuromuscular causes of pes planus were excluded.
For a quantitative measure of foot pronation, navicular drop test (NDT) was used.
The test was performed while the subject was in bare feet. Firstly, the navicular tuberosity was marked and the height of the navicular bone (from the floor) with the subtalar joint in neutral was measured by a ruler while the patient was standing and
bearing most of the weight on the contralateral limb. Then, the height of the navicular bone was measured while the patient was standing with equal weight on both
feet. The difference between the first and second measurement was registered as
the navicular drop (Menz, 1998). A difference higher than 10 mm was considered as
significant for foot pronation (Mueller et al., 1993). Group 3 consisted of nine contralateral feet (from the 27 patients) that had AN as incidental finding with no symptoms. An age appropriate control group (30 normal individuals) was screened for the
absence of AN bone, previous foot problems or surgery. Only non-pathological knees
with known individual age and gender were included in this study. The intermalleolar distance with patient supine and knees together was assessed to exclude genu valgum (< 8cm). Patients with a history of traumatic injury or surgery of lower extremities were also excluded.
To measure the Q angle, both mid patellar point and tibial tubercle were determined, thereafter a line was drawn connecting the anterior superior iliac spine and
mid patellar point; another line passing through the tibial tubercle was also drawn.
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Heba M. Kalbouneh et alii
Finally, the Q angle was measured as the value taken between the intersected lines
using a goniometer (Caylor et al., 1993; Smith et al., 2008). It should be noted that
in the present study all measurements were taken during the standing position with
quadriceps relaxed and with the feet together and facing forward, as the normal
weight-bearing forces being applied to the knee joint mimic those occur during daily activity. All measurements were performed in triplicates by a single experienced
orthopaedist and showed excellent intraobserver reliability, with correlation coefficients ranging from 0.84 to 0.89.
Statistical analyses. The data were entered into a spreadsheet and analyzed using
the IBM SPSS Statistics for Windows, version 19 (IBM Corp, Armonk, NY, USA). The
mean (± standard deviation), range and 95% confidence interval for the mean were
calculated. Differences of continuous variables between two independent groups
were assessed with two tailed t test and P<0.05 was taken as significant.
Results
AN group versus control group. No significant difference in age was found between
the two groups. Mean, standard deviation, 95% confidence interval and range of values for Q angle and navicular drop are summarized in Table 1. The mean values of
the Q angle and navicular drop for 54 lower extremities with AN were significantly
higher than those of control subjects (p<0.001; Table 1).
Group 1 versus control group. The Q angle range for individuals with normalarched feet without AN (60 contributing knees) was 12 to 18 in males and 14 to 21 in
females. Among female patients with painful AN not associated with pes planus (22
contributing knees), 18.2 % of the knees had angles greater than 21 degrees. The data
showed that three of the 13 females had angles greater than 21 degrees in at least
one side. For male patients (12 contributing knees), 25 % of the knees had a Q angle
greater than 18 degrees; three male subjects of the seven males had a Q angle greater than 18 degrees in one side. This group had a statistically larger navicular drop
than the control group, but still their values were less than 10 mm. The mean Q angle
and navicular drop values for patients with AN without pes planus were significantly higher than controls with normal arched feet in both males and females (p<0.001;
Table 2).
Group 2 versus control group. Among female patients with AN associated with
pes planus (eight contributing knees), 37.5 % of the knees had angles greater than
21 degrees. For male patients (three contributing knees), 33.3 % of the knees had a
Q angle greater than 18 degrees. The data showed that the concomitant pes planus
deformity was accompanied by a greater risk for developing higher Q angle values in
both males and females. This group had a statistically larger navicular drop than the
control group: all values were greater than 10 mm (p<0.0001; Table 2).
Group 3 versus control group. No significant difference in Q angle was found
between the two groups in both males and females. No significant difference in NDT
values was found between female patients and female controls. A significant difference in NDT values was observed in the AN asymptomatic contralateral feet of male
subjects (p<0.05; Table 2).
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Q angle in symptomatic accessory navicular bone
Table 1 – Q angles and Navicular drop values in AN patients versus controls.
AN group
N=54
Control group
N=60
P
Male
18
20
Age(years)
N
13.83±2.09
14.10±2.73
n.s.
Q angle ±SD
17.89±1.45
15.8±1.88
0.0005
16-21
12-18
17.17-18.61
14.92-16.68
8.56±2.66
6.05±0.94
6-16
5-7
7.23-9.88
5.61-6.49
Range
95% CI
NDT (mm)±SD
Range
95% CI
0.0004
Female
36
40
Age(years)
N
14.33±2.63
14.62±2.65
n.s.
Q angle ±SD
19.67±2.00
18.18±1.58
0.0005
17-24
14-21
18.99-20.34
17.67-18.68
9.12±2.83
6.78±1.51
5-17
4-8
8.15-10.07
6.29-7.26
Range
95% CI
NDT (mm)±SD
Range
95% CI
0.0001
AN: accessory navicular, NDT: navicular drop test, CI: confidence interval. n.s.: not significant.
Discussion
The overall biomechanical effect of accessory navicular bone on foot is debatable.
Typically, AN is of no consequence. However, it can be a source of pain and is often
associated with pes planus (Leonard and Fortin, 2010). Painful AN may also be present in feet with normal arch height and the degree of flat foot is not associated with
the development and severity of symptoms in patients with AN (Sullivan and Miller, 1979; Park et al., 2014). In addition, they can present in several different locations,
which can have an impact on the clinical presentation and the degree of dysfunction
(Fredrick et al., 2005). In this study, we hypothesized a possible relation between the
painful AN bone with or without the loss of arch height and the alignment of patellofemoral joint using Q angle measurement in early adolescence. All patients presented in this study had no knee complaints even in the presence of high Q angle, indicating a possible early sign for future patellofemoral joint complaints in these patients.
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Heba M. Kalbouneh et alii
Table 2 – Mean Q angle and navicular drop values among groups.
AN group
(N=54 feet)
Group 1
Symptomatic
AN/ -pp
Group 2
Symptomatic
AN/ +pp
Group 3
Asymptomatic
AN
Controls /-AN
(N= 60 feet)
Male
N
Q angle
Range
P value
NDT(mm)
Range
P
12 feet
3 feet
3 feet
20 feet
17.58±1.31
19.33±1.53
17.67±1.53
15.8±1.88
16-20
18-21
16-19
12-18
0.0072
0.0056
n.s.
7.58±1.24
13.67±2.08
7.33±0.58
6.05±0.94
5-7
6-9
12-16
7-8
0.0004
<0.0001
0.0344
22 feet
8 feet
6 feet
40 feet
Female
N
Q angle
19.55±1.87
20.88±2.42
18.5±1.05
18.18±1.58
Range
17-22
18-24
17-20
14-21
P
0.0033
0.0002
n.s.
7.86±0.81
12.63±2.39
6.83±1.33
6.78±1.51
7-9
11-17
5-9
4-8
0.0004
<0.0001
n.s.
NDT(mm)
Range
P
AN: accessory navicular, pp: pes planus, NDT: navicular drop test. Values are expressed as means ±SD, n.s.:
not significant.
The posterior tibialis muscle helps maintain the medial arch height, stabilize the
subtalar joint and prevent pronation of the foot. Stabilization of the medial arch of
the foot and foot position can be weakened by the abnormal insertion of its tendon
due to AN, this could lead to posterior tibialis dysfunction (Bernaerts et al., 2004;
Choi et al., 2004). Posterior tibialis dysfunction can lead to tendon tear, collapsing of
the arch, pain and pronation of the foot. Overuse of the posterior tibialis tendon in
AN patients could result in symptoms especially after activity and compromise the
proper muscle function. In this study, NDT was performed to measure foot pronation. Different normal values for the NDT have been suggested in the literature
(Nielsen et al., 2009; Adhikari U., 2014); however, all agree that a difference of more
than 10 mm is considered as excessive foot pronation (Mueller et al., 1993). According to our measurements of control patients, the normal range was 3 to 8 mm in
males and 4 to 8 mm in females. As expected, the minimum values for NDT in pes
planus feet were more than 10 mm (12 mm in males and 13 mm in females), indicating excessive foot pronation in these patients. On the other hand, NDT values in
patients with painful AN without fallen arch was within the high normal range, with
significant higher mean values in these patient than controls (Table 1). This possibly
Q angle in symptomatic accessory navicular bone
155
indicates some biomechanical change, weakened arch or mild pronated position of
the foot, which is mostly due to the irritation of posterior tibialis tendon by the extra
accessory ossicle. The mean NDT value in male subjects with asymptomatic AN on
the contralateral feet was significantly higher than in control feet; the small sample
size in this category certainly has affected the reliability of the analysis. In addition,
we can not preclude that asymptomatic AN is not associated with any pathological
changes: it has been shown that some asymptomatic AN bones had increased radiopharmaceutical uptake using bone scintigraphy (Chiu et al., 2000).
It is well known that pes planus deformity can alter the biomechanical relationship between the foot and knee (Hetsroni et al., 2006; Gross et al., 2011). However, the increase of Q angle in adolescent patients having painful AN bone without
pes planus could be explained by the increase of Q angle stress in the presence of
improper foot pronation. Tiberio et al. (1987) explained in a theoretical model that
a prolonged time in pronation causes excessive internal rotation of the tibia. This
excessive internal tibial rotation transmits abnormal forces upward in the kinetic chain and produces medial knee stress, force vector changes of the quadriceps
mechanism and lateral tracking of the patella. In agreement with this model, when
the Q angle was measured with the foot in different positions, it was found that the
Q angle increased as the foot shifted from outward to inward rotation (pronation)
(Olerud and Berg, 1984). Additionally, a recent study suggested that high navicular
drop measure may be associated with increased peak ankle and knee joint moments
(Eslami et al., 2014).
Hip-knee-ankle alignment influences load distribution at the knee (Sharma et al.,
2001). Any alteration in this alignment can increase the lateral force on the patella. It
should be noted that valgus alignment of the knee is measured as the medial angle
formed by the femur and tibia (femorotibial angle) (Brouwer et al., 2007). The degree
of genu valgum can be estimated by the Q angle, while the Q angle itself is important to assess the overall lateral line of pull of the quadriceps relative to the patella,
so it provides useful information mainly about the alignment of patellofemoral joint.
However, in this study no valgus deformity was documented in any case, all patients
had normal alignment of tibiofemoral joint and the increase in Q angle only indicates
a change in the alignment of patellofemoral joint rather than the tibiofemoral joint.
The normal Q angle in males is 14 degrees ± 3, while normal value for females
is 17 degrees (Aglietti et al., 1983). Values outside these limits are considered pathological burden. According to the upper limits of our measurements, standing Q
angles greater than 18 degrees in males and 21 degrees in females are considered to
be abnormal and indicate a tendency for added biomechanical load on the knee joint
during different forms of weight bearing activity. The upper limit Q angle value for
control females in this study was higher than measurements reported in other studies, reinforcing the effect of population on the Q angle as a result of the anatomical
differences in pelvic anatomy (Handa et al., 2008).
Evaluation of foot deformities must include a comprehensive assessment of the
lower limbs as a whole. Detection of the mechanical consequences of the AN may
have implications for the prevention and/or treatment of patellofemoral complaints.
For example, the use of soft foot orthotics is an effective mean of treatment for the
patient with patellofemoral pain syndrome and can correct foot pronation (Hossain et
al., 2011; Pinto et al., 2012).
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Heba M. Kalbouneh et alii
The limitation of our study was mainly the small sample size, especially in
asymptomatic AN group: a larger sample is needed in order to confirm the exact
association. In addition, there is no good measure of how much pronation of the arch
is optimal. NDT is a static measure of foot pronation, more dynamic parameters such
as measurement of the subtalar joint displacement angle during walking are being
evaluated by studies in progress.
In conclusion, AN bone should not be arbitrary considered as a normal anatomic
variant. We suggest that individuals with painful AN even when it is not associated with arch collapse are more prone to have patellofemoral joint problems later in
life. We recommend that Q angle assessment should be an essential component of the
examination in patients with painful AN. Additionally, we recommend early prophylactic interventions such as quadriceps exercises, posterior tibialis strengthening exercises, and soft foot orthotics to limit foot pronation and prevent the potential future
consequences on patellofemoral joint in early adolescence when it is a common time
for the symptoms to first appear.
Conflict of interest statement
The authors declare that the research was conducted without any commercial or
financial relationships that could be seen as a potential conflict of interest
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IJA E
Vo l . 121, n . 2: 159 -16 4, 2016
I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - History of anatomy and embryology
Caspar Bauhin (1560-1624): Swiss anatomist and
reformer of anatomical nomenclature
Sanjib Kumar Ghosh
Department of Anatomy, ESI- PGIMSR & ESIC Medical College, Joka, Kolkata, West Bengal, India
Abstract
Caspar Bauhin (1560-1624) was a Swiss anatomist, physician and botanist. He commenced
the study of medicine at a young age in Basel but had to move to Padua after an outbreak of
plague in his native place. In Padua, he was privileged to study under Fabricius ab Aquapendente, an accomplished anatomist of his time, and other pioneers in the field of medicine,
surgery and botany. He travelled extensively through Italy, France and Germany before finally
returning to Basel, where he started to conduct public anatomy dissections and in due course
was appointed to the Chair of Anatomy and Botany at the University of Basel. His treatise, Theatrum anatomicum (1605), was considered as the finest comprehensive text in anatomy during
that period. Theatrum was highly appreciated as it followed a systemic approach with focus on
anatomical anomalies and had a useful set of illustrations. His major contribution to Anatomy
was the introduction of a descriptive terminology which replaced the prevalent trend of naming the structures with ordinal numbers and cleared the confusion among anatomists in relation
to identification of structures. He was the first to describe the anterior lingual glands (Bauhin’s
gland), which are seromucous glands located near the tip of tongue. He is presumed to be the
first to report the ileocecal valve, which is also known as Bauhin’s valve. Bauhin’s contributions
are a true testimony of his legacy in the domain of anatomical sciences.
Key words
Anatomical nomenclature, Bauhin’s gland, Bauhin’s valve, theatrum anatomicum, anatomical
illustrations
Introduction
Caspar Bauhin or Gaspard Bauhin was a Swiss anatomist, physician and botanist, who was born in Basel on 17th January, 1560 (Fig. 1). He belonged to a family
spanning six generations of physicians and natural scientists (Whitteridge, 1970). He
was the youngest son of Jean Bauhin (1511-1582), an eminent French physician, who
was compelled to leave his native country on becoming a convert to Protestantism
(Rose et al., 1841). As a child, Bauhin was remarkably weak and feeble and could
not speak clearly until five years of age. However he commenced the study of medicine at a very young age under the guidance of his father and brother Johann Bauhin
(1541-1613), who himself was a famous physician and botanist (Mägdefrau, 1992). In
1572, Bauhin entered the University of Basel, where noted Swiss physicians, Theodor
Zwinger the Elder (1533-1588) and Felix Platter (1536-1614) were among his teachers.
Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18489
160
Sanjib Kumar Ghosh
Figure 1 – A portrait of Caspar Bauhin. Image in public domain.
He received the degree of Bachelor of Philosophy in 1575 and conducted his first medical disputation in 1577 (Martensen, 2001). However a severe epidemic of plague broke
out in Basel in 1577 and he moved to Padua, the most prominent European university
in the field of medicine during that period (Hugh, 1911; Taylor, 2009; Porzionato et al.,
2012). In Padua, Bauhin attended lectures of Fabricius ab Aquapendente (1533-1619)
and Archangelo Piccoluomini (1525-1586), who were pioneers in the field of anatomy.
He attended the dissection of seven human cadavers being performed by Fabricius
and even assisted him in private dissections. He stayed in Padua for 18 months and
the influence of such illuminating personalities were evident as he got passionately
attached to anatomy (Isely, 1994). He then travelled all over Italy, visited Bologna and
received instructions in anatomy from Giulio Cesare Aranzio (1530-1589), before moving to Montpellier, where he signed the register in the spring of 1579 (Hugh, 1911;
Gurunluoglu et al., 2011). However Bauhin spent more time in Paris, attending anatomy sessions conducted by Sévérin Pineau (1550-1619), Professor of Anatomy and Surgery. He even assisted Pineau in undertaking dissection at his request (Whitteridge,
1970). Towards the middle of 1580, Bauhin arrived at the University of Tübingen in
Germany with the purpose of receiving lessons in Botany (Jahn, 2000). He had the
intention of making an extensive tour of Germany, but was recalled to Basel in early
1581, as his father was at the point of death (Rose et al, 1841).
Bauhin and anatomical nomenclature
161
Bauhin’s career at Basel
On his return to Basel, Bauhin began to dissect bodies at the request of the College
of Physicians. He held his first public anatomy dissection on February 27, 1581, when
under the guidance of Felix Platter he conducted the section of a male body in presence of about 70 spectators. The spectacle lasted for five days and was a remarkable
one as no such sections had been executed in Basel for the past ten years (Whitteridge,
1970). Bauhin held his doctoral disputation on the subject De dolore colico on April 19.
He was conferred the title of Doctor of Medicine on May 2, and on May 13 he was
made a member of the Faculty of Medicine at the University of Basel. From that time,
he taught both Anatomy and Botany in Basel. He conducted public anatomical dissections during winter and took the students to botanical expeditions in the summer
(Bergmann and Wendler, 1986). Bauhin was made professor of Greek language in 1582
and two years later he became consiliarius in the Faculty of Medicine, an office he held
until his death. He was dean of the Faculty of Medicine nine times, beginning in 1586,
and was elected rector of the University of Basel four times from 1592 onwards (Rose
et al., 1841). As a result of his efforts, University authorities initiated work for building
a permanent theatre for anatomical demonstrations and a botanical garden was laid
out in the University campus. In 1589, while still a professor of Greek, he was appointed professor of Anatomy and Botany, a special chair created for Bauhin (Jahn, 2000).
During all these years, his reputation as a medical practitioner grew in Basel, and in
1597 he, along with his brother Johann, were appointed personal physician to Duke
Friedrich of Württemberg (1557-1608). After the death of Felix Platter in 1614, Bauhin
succeeded his teacher as archiator (chief medical officer) in the city of Basel, and the
following year was appointed professor of Practical Medicine (Kyle and Shampo,
1979). He died on 5th December, 1624, in Basel (Whitteridge, 1970).
Reformer of anatomical nomenclature
Bauhin’s major contribution to the study of Anatomy was reforming the anatomical nomenclature, which has a long evolutionary history. Hippocrates and other
ancient anatomists had to develop a dictionary in order to communicate their observations. Galen established a comprehensive nomenclature derived from Greek, which
was very extensive (Sakai, 2007). Anatomical nomenclature grew enormously and
haphazardly with innumerable synonyms from the second to the sixteenth century.
Consequently anatomists found it extremely difficult to express themselves (Kachlik et al., 2009). Andreas Vesalius (1514-1564) described the anatomical structures in
De Humani Corporis Fabrica (1543) with the help of a highly sophisticated but difficult
nomenclature system, whereby he replaced all Greek and Arabic terms with Latin
ones. He distinguished between muscles, bones, blood vessels and nerves with ordinal
numbers (Sakai, 2007). During that period, anatomists had named different anatomical structures in this way, however they did not agree on the order of enumeration
(Bradley and Willich, 1799). In the late sixteenth century Bauhin adopted a descriptive
anatomical nomenclature in his publications, in order to clear the confusion over the
ordinal-based one. He collected almost all the synonymous anatomical terms prevalent
in that period and replaced them with more specific ones to describe muscles, vessels
162
Sanjib Kumar Ghosh
and nerves (Sakai, 2007). Bauhin termed some muscles on the basis of their substance
(semimembranosus), others on the basis of their shape (scalene), some on the basis of
their origin (arytenoid), and others on the basis of their origin and insertion (styloglossus, cricothyroid). Some were termed on the basis of their position (pectoralis), some
on the basis of their volume (vastus, gracilis), and others on the basis of their use
(supinator, pronator). Bauhin also introduced the terminologies of veins and arteries
based on their use or course and that of nerves on the basis of their function (Kyle and
Shampo, 1979). His nomenclature system had obvious advantages over the old method and was embraced by all contemporary as well as future anatomists (Sakai, 2007).
Published works in anatomy
Bauhin’s contribution as a teacher of anatomy was substantial, particularly through
his textbooks on the subject. His first text was De corporis humani partibus externis (1588),
which was a succinct, methodical account of the external parts of the human body
suitable for beginners (Bauhin, 1588). In 1590, Bauhin published his first complete
textbook, De corporis humani fabrica libri IIII. It was a systematic account written from
the point of view of dissection and was primarily intended for the students (Bauhin,
1590). An enlarged version of the text was republished in 1597 as Anatomica corporis
virilis et muliebris historia as Bauhin introduced some corrections and added a description of female anatomy (Bauhin, 1597). In 1605 all of Bauhin’s anatomical writings were
brought together, revised, enlarged and published as a comprehensive text entitled Theatrum anatomicum. Theatrum was Bauhin’s most celebrated anatomical textbook and was
accompanied by copper engravings based on illustrations used in Vesalius’s anatomical treatise De Humani Corporis Fabrica. Theatrum was highly appreciated by physicians
as well as students of anatomy and its popularity could be attributed to the facts that
it followed a systematic approach, gave adequate consideration to the ancient authorities, did not dwell too much into controversies, had a series of useful footnotes and
mentioned anatomical anomalies as well as pathological findings (Bauhin, 1605). The
quality of illustrations used in Theatrum were not of the highest standard, particularly if
compared with those in De Humani, however they were adequate for anyone referring
to the text during dissection (Bergmann and Wendler, 1986). Theatrum was probably
the most widely used anatomical text in the period immediately before William Harvey (1578-1657), as Bauhin was the most cited author (after Vesalius) in Harvey’s text.
In fact it was Bauhin’s work that Harvey chose as the basis for his Lumleian Lectures
to the College of Physicians in London in 1616 (French, 2006). Theatrum was translated
into English in 1615 by Helkiah Crooke (1576-1648), court physician to King James I of
England (O’Malley, 1968). Crooke combined Bauhin’s text with that of French anatomist Andreas Laurentius (1558-1609) and published them under the title of Mikrokosmographia: A Description of the Body of Man (Crooke, 1615).
Anatomical findings
Although Bauhin’s anatomical works contained few novelties, he did include
new anatomical findings in his published works. Bauhin is presumed to be the first
Bauhin and anatomical nomenclature
163
to describe the ileocecal valve, which was long known as the Valvula Bauhini or
Bauhin’s Valve (Nesher et al., 2006; Porzionato et al., 2012). In a number of his anatomical writings, he gives an account of how he first found the structure during a
private dissection that he performed as a student in Paris in 1579 (Whitteridge, 1970).
He was the first to describe the anterior lingual glands, which are seromucous glands
located near the tip of tongue on each side of frenulum linguae. After his name,
anterior lingual glands are referred to as Bauhin’s glands or Glandula Bauhini (Dobson, 1962). Bauhin named the phrenic nerve and he is also credited with giving the
name of areole to the pigmented area around the nipple (Singer, 1925). He included
a description of valves present in the veins in his text De corporis humani Fabrica libri
IIII (Bauhin, 1590). Presence of valves in veins were first demonstrated by Fabricius
in 1574 in Padua, however Fabricius’s findings were not published until 1603 (Fabricius, 1603). In De corporis, Bauhin deviated from Galen’s theory and opposed the
existence of pores in the interventricular septum of the heart. He opined that venous
blood could more easily go to the lungs from the right ventricle through the pulmonary artery, refined there and mixed with air, and return to the left ventricle through
the pulmonary veins (Bauhin, 1590). However in his later writings, Bauhin seems to
have rejected his own view and endorsed Galen’s traditional views as he reported the
presence of conspicuous pores in the septum of an ox’s heart (Bauhin, 1597).
Conclusion
Bauhin was a truly original scientist whose influence in Anatomy lasted for well
over a century. His great merit was his unmatched dedication and ability to treat his
subject in an orderly and methodical manner. He was a pioneer as his anatomical
nomenclature system was effective in clearing the confusion related to identification
of anatomical structures and was readily embraced by anatomists. Most of the anatomical terminologies that we are familiar with in present times were introduced by
Bauhin. With an extensive collection of documented works and contributions, he laid
the platform for the advancement of anatomical sciences. Caspar Bauhin should be
recognized and remembered as his exploits inspired generations of anatomists.
Conflict of interest
The author hereby declare that there is no potential conflict of interest in any form
concerning the author
References
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Bauhin C. (1590) De corporis humani fabrica Libri IIII. Basel: Sebastianum Henricpetri.
Bauhin C. (1597) Anatomica corporis virilis et muliebris historia. Lugduni: Apud
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Bauhin C. (1605) Theatrum anatomicum. Frankfurt: Johann Theodor de Bry.
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William Laggard.
Dobson J. (1962) Anatomical Eponyms. 2nd Ed. Edinburgh, Scotland: E & S Livingstone. P. 194.
Fabricius H. (1603) De Venarum Osteolis. Franklin K.J. (Ed). London: Bailliére, Tindall
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Kyle R.A., Shampo M.A. (1979) Gaspard Bauhin. JAMA 242: 1162.
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IJA E
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I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Basic and applied anatomy
Morphometric study of variations of sacral hiatus
among West Bengal population and clinical
implications
Dona Saha1, Santanu Bhattacharya2,*, Akhtar Uzzaman2, Sibani Mazumdar2, Ardhendu Mazumdar3
Departments of 1Anatomy, N.R.S. Medical College; 2Anatomy, Calcutta National Medical College; and 3Physiology, Institute of Postgraduate Medical Education and Research; Kolkata, India
Abstract
The study was conducted on one hundred and seventeen human sacra to categorize the sacral
hiatus of West Bengal population to improve the accuracy of caudal epidural block for anesthesia and analgesia. Various contours of hiatus were observed in this study which included
inverted U (70.09%), inverted V (14.53%), irregular (12.82%), bifid (1.71%) and dumbbell
(0.85%).The most frequently observed positions of apex and base of the hiatus were fourth and
fifth sacral vertebrae respectively (74.36% and 95.73%). The average length, width and depth of
hiatus were 20.21 mm, 12.10 mm and 6.02 mm with standard deviation of 7.7 3mm, 3.13 mm
and 2.43 mm respectively. All the measurements were taken by Vernier calipers. Only in 27.35%
cases the points on the lateral sacral crests at the level of first sacral foramina formed an equilateral triangle with the apex of the hiatus and thus could be used as an important landmark to
locate sacral hiatus.
Key words
Sacrum, sacral hiatus, caudal epidural block, sacral cornua
Introduction
Caudal epidural block (CEB) is used for analgesia and anaesthesia in various clinical procedures where the medication is injected into the epidural space through the
sacral hiatus (Chen et al., 2004). This approach to epidural space produces reliable
and effective block of sacral nerves.
The opening present at the caudal end of sacral canal is known as sacral hiatus,
which is formed due to failure of fusion of laminae of fifth (occasionally fourth)
sacral vertebra. The sacral canal contains sacral and spinal nerve roots, the cauda
equina, filum terminale externum, fibrous and fatty tissue, epidural venous plexus
and spinal meninges (Standring et al., 2008).
In practice, the sacral hiatus is identified by palpation of the sacral cornua keeping
the patient in the lateral position or lying prone over a pelvic pillow. These are felt at
the upper end of the natal cleft 0.5 cm above the tip of the coccyx. Alternatively, the
sacral hiatus may be identified by constructing an equilateral triangle based on a line
joining the posterior superior iliac spines (Standring et al., 2008). Posterior superior
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18490
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iliac spines impose over the lateral sacral crest at the level of first sacral foramina (
Senoglu et al., 2005).
There are considerable variations in the size and shape of sacral hiatus which
cause difficulty in localization of hiatus during CEB (Sekiguchi et al., 2004).
So, the purpose of this study was to explore the variations of sacral hiatus among
the West Bengal population to increase the success rate of CEB. Moreover, the authors
were also inquisitive to verify the significance of the aforesaid triangle for locating
sacral hiatus among the study population.
Materials and Methods
Completely ossified human sacra of undetermined age and sex were collected
from different medical colleges of West Bengal during a study period of one year.
Sacrum with total posterior closure defect (two cases) and agenesis of hiatus (one
case) were excluded and finally the sample size was one hundred and seventeen. The
shape, apex and base of sacral hiatus were noted. Length, depth and intercornual
width of hiatus were measured by Vernier calipers. The gap between the two points
of lateral sacral crests at the level of first sacral foramina and the distance of those
points from the apex of the sacral hiatus were also measured. Finally, collected data
was tabulated on Microsoft Excel Spread Sheet and analyzed by Epi info 3.5.1 software (CDC, Atlanta, GA).
Results
Inverted U was the commonest shape of sacral hiatus and dumbbell was the rarest variant. The result is portrayed in Table 1 and different varieties of sacral hiatus
are demonstrated in Figures 1-5. The level of the apex of hiatus varied from S2 to S5.
(Table 2) but its commonest position was against S4 (74.36% of cases). Base of sacral
hiatus was present in the plane of 4th sacral segment in 5 (4.27%) sacra and at the
level of the 5th sacral segment in 112 (95.73%) sacra.
Several morphometric measurements of the sacrum are depicted in Table 3.
The mean distance between the two points on lateral sacral crests at the level of
first sacral foramina (base of triangle) was 62.38 mm with standard deviation 6.19
mm. The average distances of those two points on right and left lateral sacral crests
from the apex of the sacral hiatus were 63.38 mm (with standard deviation 9.21 mm)
and 63.50 mm (with standard deviation 9.20 mm) respectively. A complete equilateral triangle was demonstrated in 32 cases (27.35%) by union of right and left lateral sacral crests with apex of hiatus. An isosceles triangle was observed in 74 cases
(63.25%) and a scalene triangle was present in 11 cases (9.40%).
Table 1 – Different types of sacral hiatus (n=117).
Inverted U
Inverted V
Irregular
Bifid
Dumbbell
82 (70.09%)
17 (14.53%)
15 (12.82%)
02 (1.71%)
01 (0.85%)
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Morphometry of sacral hiatus for epidural block
Table 2 – Location of the apex of sacral hiatus (n=117).
2nd sacral vertebra
3rd sacral vertebra
4th sacral vertebra
5th sacral vertebra
2 (1.71%)
20 (17.09%)
87 (74.36%)
8 (6.84%)
Figure 1 – Bifid sacral hiatus.
Figure 2 – Dumbbell shaped sacral hiatus.
Figure 3 – Inverted U shaped sacral hiatus.
Figure 4 – Inverted v shaped sacral hiatus.
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Dona Saha et alii
Figure 5 – Irregular sacral hiatus.
Table 3 – Morphometric measurements of the sacrum.
Standard
Mode
Deviation
(mm)
(mm)
Mean
(mm)
Range
(mm)
Length of sacral
hiatus
20.21
8.80-54.00
7.73
15.00
Width of sacral
hiatus
12.10
6.00-21.10
3.13
12.00
Depth of sacral
hiatus
6.02
2.00-12.50
2.43
5.00
Distance between right and left lateral sacral crest at the
level of first sacral foramina
62.38 46.60-89.10
6.19
62.00
Distance between right lateral sacral crest and apex of
sacral hiatus
63.38 37.50-84.10
9.21
60.00
Distance between left lateral sacral crest and apex of
sacral hiatus
63.50 37.50-84.10
9.20
60.00
Parameter (mm)
Discussion
Edward et al. (1942) for the first time took the advantage of this natural gap at
the lower end of sacral canal for continuous caudal analgesia during labor (Edwards
et al., 1942). Tsui et al. (1999) and subsequently Chen et al. (2004) stated that the use
of ultrasound to guide needle placement into the caudal epidural space during CEB
would increase the success rate by 100%. However, using ultrasound or fluorosco-
Morphometry of sacral hiatus for epidural block
169
py is not always possible due to time, cost-effectiveness and personnel availability
(Senoglu et al, 2005). So when ultrasound or fluoroscopy cannot be applied, other
anatomical landmarks are used. But a failure rate of 25% has been reported by some
investigators (Lewis et al., 1992 & Tsui et al., 1999). Stitz and Sommer (1999) reported
a success rate, without fluoroscopy, of 74%. White et al., 1980 reported a failure rate
of 25% in caudal epidural steroid injection.
U shaped sacral hiatus was predominant (70.09%) among the West Bengal population which was favorable for CEB. This finding supported the observation of
Bhattacharya et al. (2013) where the authors reported the same type of hiatus (65%)
among the identical population.
In the present study, the commonest position of the apex of the sacral hiatus was
against the fourth sacral vertebrae (74.36%) which supported the similar observations
of Kumar et al. (2009: 72.01%), Suma et al. (2011: 77.50%) and Sultana et al. (2014:
74.21%). Base of sacral hiatus was most often located against the fifth sacral vertebra
(95.73%, which was close to the value of Sultana et al., 2014: 96.84%).
Previous studies (Patel et al., 2011; Aggarwal et al., 2012; Shewale et al., 2013)
showed the average length of the hiatus to vary from 18.81 mm to 22.87 mm which
was similar to the present study (20.21 mm). But the study by Patil et al. (2012) and
Bhattacharya et al. (2013) described higher average values (34.13 mm and 35.92 mm)
than the current study.
Sacral cornua were considered as an important landmark for identifying sacral
hiatus. Variations in sacral cornua ranging from well-defined projection to flattening
may greatly affect their utility for locating hiatus. In this study, the range of transverse width of the sacral hiatus or the intercornual distance (6-21.1 mm) was similar
to the result of Aggarwal et al. (2009: 6-23.3 mm).
The antero-posterior diameter or the depth of sacral hiatus at the apex is very
important as it should be sufficiently large to admit a needle into the sacral canal. In
the present study it was less than 3 mm in 6.84% cases, where it would be difficult
to insert a 22G needle. Trotter and Letterman (1944) and later Aggarwal et al. (2009)
noticed this finding in 5% and 8.7% cases respectively.
As the apex of the sacral hiatus is difficult to palpate, especially in obese patients,
other landmarks may be of use, such as the triangle formed between the posterior
superior iliac spines or the lateral sacral crest and the apex of sacral hiatus (Senoglu et al., 2005). Aggarwal et al. (2012) and Patil et al. (2012) reported an equilateral triangle in 45% and 23% cases respectively. On the contrary, Bhattacharya et al.
(2013) observed an isosceles triangle in general, but a complete equilateral triangle
was found only in 16% cases. The present study described a scalene triangle (9.40%)
in addition to isosceles triangle (63.25%) and complete equilateral triangle (27.35%)
which was a unique finding of the study.
Conclusion
The present study reports instances of shallow sacral canal at the apex (less than
3 mm) and abnormal shape of hiatus (i.e. irregular, bifid and dumbbell) where needle
insertion may lead to failure. The right and left lateral sacral crests at the level of
first sacral vertebra and the apex of hiatus formed a variety of triangle types which
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were not reliable for caudal epidural block among the West Bengal population. The
study also describes the possible anatomical causes of failure which should always be
kept in mind while attempting caudal epidural block.
Acknowledgement
The authors are grateful to Dr. Sumita Datta, Associate Professor, and all other
members of Dept. of Anatomy, Calcutta National Medical College, for their active
support and participation.
References
Aggarwal A., Aggarwal A., Harjeet, Sahni D. (2009) Morphometry of sacral hiatus
and its clinical relevance in caudal epidural block. Surg. Radiol. Anat. 31: 739800.
Bhattacharya S., Majumdar S., Chakraborty P., Mazumdar S., Mazumdar A. (2013) A
morphometric study of sacral hiatus for caudal epidural block among the population of West Bengal. Indian J. Bas. Appl. Med. Res. 2: 660-667.
Chen P.C., Tang S.F.T., Hsu T.C. (2004) Ultrasound guidance in caudal epidural needle
placement. Anesthesiology 101: 181–184.
Edwards W.B., Hingson R.A. (1942) Continuous caudal anaesthesia in obstetrics. Am.
J. Surg. 57: 459-464.
Kumar V., Nayak S.R., Potu B.K., Palakunta T. (2009) Sacral hiatus in relation to low
back pain in South Indian population. Bratisl. Lek. Listy 110: 436-441.
Lewis M.P.N., Thomas P., Wilson L.F., Mulholland R.C. (1992) The ‘whoosacral hiatus’
test: a clinical test to confirm correct needle placement in caudal epidural injections. Anaesthesia 47: 57–58.
Patel Z.K., Thummar B., Rathod S.P., Singel T.C., Patel S., Zalawadia A. (2011) Multicentric morphometric study of dry human sacrum of Indian population in Gujarat
region. NJIRM 2 (2): 31-35.
Patil S.D., Jadav R.H., Binodkumar, Mehta D.C., Patel D.V. (2012) Anatomical study of
sacral hiatus for caudal epidural block. Natl. J. Med. Res. 2: 272-275.
Sekiguchi M., Yabuki S., Satoh K., Kikuchi S. (2004) An anatomic study of the sacral
hiatus: a basis for successful caudal epidural block. Clin. J. Pain 20: 51–54.
Senoglu N., Senoglu M., Oksuz H. (2005) Landmarks of the sacral hiatus for caudal
epidural block: an anatomical study. Br. J. Anaesth. 95: 692–695.
Shewale S.N., Laeeque M., Kulkarni P.R., Diwan C.V. (2013) Morphological and morphometrical study of sacral hiatus. Int. J. Recent Trends Sci. Technol. 6(1): 48-52.
Standring S., Newell R.L.M., Collins P., Healy J.C. (2008) The Back. In: Gray’s Anatomy. The Anatomical Basis of Clinical Practice, 40th edn. Edinburgh, Churchill Livingstone Elsevier. Pp. 724-728.
Stitz M.Y., Sommer H.M. (1999) Accuracy of blind versus fluoroscopically guided
caudal epidural injection. Spine 24: 1371-1376.
Sultana Q., Shariff H.M.,Jacob M., Rao C., Avadhani R. (2014) A morphometric study
of sacral hiatus with its clinical implications. Indian J. Appl. Res. 4 (2): 17-20.
Morphometry of sacral hiatus for epidural block
171
Suma H.Y ., Kulkarni R. ,Kulkarni R.N.(2011) A study of sacral hiatus among sacra in
South Indian population. Anatomica Karnataka 5(3): 40-44.
Trotter M., Letterman G.S. (1944) Variations of female sacrum: Their significance in
continuous caudal anaesthesia. Surg. Gynecol. Obstet. 78: 419-424.
Tsui B.C, Tarkkila P., Gupta S., Kearney R. (1999) Confirmation of caudal needle
placement using nerve stimulation. Anesthesiology 91: 374–378.
White A.H., Derby R., Wynne G. (1980) Epidural injections for the treatment of low
back pain. Spine 5: 78–86.
IJA E
Vo l . 121, n . 2: 172-178 , 2016
I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Human anatomy case report
Abnormal branching of the axillary artery: an axillohepatic artery
Pranit N Chotai1, Marios Loukas2, R. Shane Tubbs3,*
1
Division of Pediatric Surgery, Department of Surgery, University of Tennessee Health Science Center, Le
Bonheur Children’s Hospital, Memphis, TN, United States; 2 Department of Anatomic Sciences, St. George’s University, Grenada, West Indies; 3 Seattle Science Foundation, Seattle, WA, United States
Abstract
The axillary artery is a continuation of the subclavian at the outer border of first rib. Reports
of anatomic variations of the axillary artery encountered during cadaveric dissection are not
uncommon. However, abnormal branching patterns of the axillary artery identified on imaging studies are rare. We encountered an abnormal branch of the right axillary artery, which
descended along the lateral thoraco-abdominal wall and gave off branches to the liver capsule
before terminating at the level of the ipsilateral iliac crest. Knowledge of this variation, which
we term the axillo-hepatic artery, will be of interest to anatomists, radiologists and adult- and
pediatric- surgeons operating on the upper chest and abdominal regions. To our knowledge,
such a vessel has not been reported previously in the extant medical literature.
Key words
Axillary artery, axillo-hepatic artery, abnormal branching, variation, thoraco-abdominal artery
Introduction
The length of the subclavian artery beyond the lateral border of first rib upto the lateral border of the teres major muscle is defined as the axillary artery (AA)
in standard descriptions of upper limb arterial anatomy (Standring, 2008). Due to
advances and increase in number of interventional cardiovascular procedures, the AA
is now identified as an artery of increasing clinical significance for vascular access.
Additionally, the AA is also of interest to orthopedic, cardiothoracic-, plastic and
general surgeons operating in the upper thoracic region in patients of all age groups
(Astik and Dave, 2012; Ravi et al., 2012; Hwang et al., 2013). Cadaveric reports of
anatomic variations involving the AA have been frequently reported, however abnormal branching patterns of the AA diagnosed on imaging studies have rarely been
reported (Sato and Takafuji, 1992; Kogan and Lewinson, 1998; Cavdar et al., 2000;
Ravi et al., 2012). We report a case of a 13-month-old adolescent male who was found
to have an abnormally high split of his right axillary artery, which descended along
the lateral thoraco-abdominal wall and gave off branches to the liver capsule before
abruptly terminating at the level of the right iliac crest.
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18491
Axillo-hepatic artery
173
Case report
A 13-month-old male child presented to our outpatient clinic with congenital scoliosis. For further evaluation, he underwent a magnetic resonance imaging (MRI) of
his chest and abdomen, which revealed a split axillary artery (Figs 1-3). Imaging was
by Gadevist (Gadobutrol, Bayer, NJ, USA) contrast enhanced MRI using Ingenia 3.0
Tesla (Philips, Andover, MA, USA). The superficial branch travelled horizontally to
assume the normal course of the axillary artery, however a deeper branch descended and travelled along the anterolateral thoraco-abdominal wall. This artery gave
off multiple branches to the liver capsule before abruptly terminating at the level
of the right iliac crest. In addition to the abnormal branching of the axillary artery,
the patient also had an anomalous right-sided aortic arch with a retroesophageal
right subclavian artery as well as a right accessory renal artery. The patient also had
multiple other associated non-vascular congenital abnormalities (Table 1). No other
imaging examination other than the initial MRI was performed to study the course
of the variant artery described above. The patient’s exam was non-focal with appropriate distal pulses.
Figure 1 – Coronal magnetic resonance imaging of chest and abdomen by Gadevist (Gadobutrol, Bayer,
NJ, USA) contrast enhanced MRI using Ingenia 3.0 Tesla (Philips, Andover, MA, USA), showing the abnormal
branching of right axillary artery. The deeper branch is seen descending along the lateral thoraco-abdominal wall.
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Pranit N Chotai et alii
Figure 2 – Coronal magnetic resonance imaging of chest and abdomen showing thoraco-abdominal artery
branching off the right axillary artery.
Figure 3 – Coronal magnetic resonance imaging of chest and abdomen contrast enhanced MRI using
Ingenia 3.0 Telsa, Philips (Andover, MA, USA) MRI) showing branches off the thoraco-abdominal artery feeding the liver capsule.
Axillo-hepatic artery
175
Table 1 – Associated congenital anomalies in our patient (vascular malformations in italics).
Micrognathia/ Retrognathia
Cleft palate
Polydactyly
Right sided aortic arch with right retroesophageal subclavian artery
right accessory renal artery
Duplicated right renal collecting system
Right hydronephrosis
Hemivertebra / Butterfly vertebra / Scoliosis
Bilateral hip dislocation
Absent right femur
Conus medullaris termination at L2/L3
Mild hydromyelia
Discussion
Anatomy and Embryology
Embryologically, multiple theories have been proposed regarding the upper limb
arterial origin. The most recent theory from the last decade suggests that the arterial
system of the upper limb develops by selective enlargement or regression of a capillary plexus and not by budding from a main axial trunk and this development is
closely related to bone development (Rodriguez-Niedenfuhr et al., 2001; Natsis et al.,
2014). In contrast, another theory suggests that only one upper limb arterial bud (subclavian) persists, which continues to form axillary and brachial arteries, which supply
the lateral thorax as well as the upper limb (Kogan and Lewinson, 1998). An arrest
or defect in the embryonic development of the vascular plexuses of the upper limb
buds is thought to play a role in development of variations in the arterial origins and
courses of the major upper limb vessels (Cavdar et al., 2000).
In standard anatomic texts, the AA is described as the continuation of the ipsilateral subclavian artery at the outer border of first rib up to the outer border of the
teres major muscle, beyond that point it continues in the arm as the brachial artery
(Standring, 2008). In relation to the pectoralis minor muscle, the course of the AA is
divided into three parts - the proximal (1st), posterior (2nd) and distal (3rd) (Standring,
2008). Six major branches are given off the axillary artery, namely superior thoracic,
thoracoacromial, lateral thoracic, subscapular, and anterior and posterior circumflex
humeral (Standring, 2008).
Anatomic variations of upper extremity arteries are not rare. In a study if 100
upper extremity arteriograms, a 9% incidence of arterial variations involving the
upper extremity vessels was identified (Uglietta and Kadir, 1989). The overall incidence of these anomalies in the upper extremity is estimated to be as high as 24%
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Pranit N Chotai et alii
(Cavdar et al., 2000). Additionally, branching variations involving the AA are also
not uncommon (Astik and Dave, 2012). However, there are only a limited number
of reports describing branching patterns similar to our case report: none of these
reports has the same unique branching pattern with axillo-hepatic branches, as seen
in our case (Sato and Takafuji, 1992; Kogan and Lewinson, 1998; Ravi et al., 2012).
In a previous study by Sato and Takafuji (1992) a branch of the AA supplying the
abdominal part of the pectoralis major muscle was mentioned. The authors named
this branch as arteria partis abdominalis (Sato and Takafuji, 1992). Another report
mentioned a “thoarco-epigastric” branch of the AA, which descended on the anterior
aspect of the axillary fossa and anastomosed with the superficial epigastric artery in
the hypogastric region (Kogan and Lewinson, 1998). In another cadaveric study, one
of the two branches off the second part of the AA was designated as an axillo-thoracic artery (Ravi et al., 2012). In contrast, in our case, an additional branch off the right
AA descended along the lateral thoraco-abdominal wall and gave off branches to the
liver capsule before abruptly terminating at the level of the right iliac crest (Figs 1-3).
Our review of reports in the extant literature did not find any cases mentioning a
similar abnormal branching pattern.
Numerous other branching variations involving the AA are also reported (Cavdar
et al., 2000; Astik and Dave, 2012). In another cadaveric report, a high division of the
AA into superficial and deep brachial arteries without any mention of thoraco-abdominal branching was reported (Cavdar et al., 2000). In a cadaveric study of 80 limbs, the
authors reported that the AA variations were found in 62.5% limbs (Astik and Dave,
2012). The variations included a lateral thoracic artery originating from the subscapular
artery; absent thoracoacromial trunk, or its branches arising directly from the second
part of the axillary artery; division of the thoracoacromial trunk into deltoacromial and
clavipectoral trunks, which were further divided into all the branches of the thoracoacromial trunk; origin of subscapular, anterior circumflex humeral, posterior circumflex
humeral and profunda brachii arteries from a common trunk from the third part of the
axillary artery; and an origin of the posterior circumflex humeral artery from brachial
artery in addition to third part of the axillary artery (Astik and Dave, 2012). There was
no mention of an abnormal thoraco-abdominal branch similar to the one seen in our
case. In another cadaveric report, bifurcation of second part of AA into superficial and
deep brachial arteries has also been reported (Cavdar et al., 2000; Natsis et al., 2014).
In contrast to our report, cadaveric reports describing various branching variations of the AA are able to provide a detailed anatomical description of the course of
the variant branch (Kogan and Lewinson, 1998; Cavdar et al., 2000; Astik and Dave,
2012). However, we encountered this variant branch in our patient on MRI, and since
no other vascular imaging was obtained to further characterize this variation, we are
unable to provide a more detailed anatomic description of this abnormal branch of
the AA in terms of the caliber of the vessel, other abnormal branches not visible on
the MRI or presence of any aneurysms or other structural defects in the vessel wall.
Clinical Correlation
Knowledge of the normal anatomy as well as variations of AA is significant in
multiple clinical interventions and procedures. Cardiothoracic surgeons utilize the
AA during antegrade cerebral perfusion in aortic surgery in high risk patients. The
Axillo-hepatic artery
177
AA is also being increasingly used as the access vessel for invasive cardiovascular
procedures. Orthopedic surgeons encounter the axillary artery while dealing with
brachial plexus repairs or during surgical intervention of shoulder dislocations or
proximal humeral fractures (Astik and Dave, 2012). Trauma and general surgeons
deal with the AA during axillary reconstruction or while treating AA hematoma after
trauma, and during radical mastectomy (Ravi et al., 2012). Vascular surgeons and
vascular radiologists cannulate the AA for several procedures or while treating the
AA thrombosis or AA aneurysm (Astik and Dave, 2012). The AA is also important to
plastic surgeons performing a musculocutaneous flap for wound or defect reconstruction or during harvesting the AA for microvascular graft to repair damaged arteries
(Hwang et al., 2013). In particular, the variation found in our patient might be significant to the hepato-biliary surgeon due to the presence of the hepatic branches off
the variant axillary artery branch. When pre-operative angiogram is available, these
variant branching patterns can be potentially identified, however, we recommend
that surgeons operating in this region be mindful of this abnormal branching pattern
when pre-operative imaging is not available or in emergency situations such as trauma patients so as to be well-equipped to deal with any hemorrhagic complications
arising due to such unpredictable branching of the AA.
In conclusion, awareness of this variation involving an abnormal branching of
right axillary artery into a thoraco-abdominal artery with branches to liver capsule
is not only interesting to anatomists but also to radiologists and interventional cardiologists who frequently use the AA as a vascular access for invasive procedures. It
is also of clinical interest to orthopedic, cardiothoracic, plastic, vascular and general
surgeons operating on thoraco-abdominal and proximal shoulder girdle regions in
patients of all age groups. Anatomical variations involving AA should be reported as
discovered in view of their potential clinical and anatomical importance.
References
Astik R., Dave U. (2012) Variations in branching pattern of the axillary artery: a study
in 40 human cadavers. Jornal Vascular Brasileiro 11: 12-17.
Cavdar S., Zeybek A., Bayramicli M. (2000) Rare variation of the axillary artery. Clin.
Anat. 13: 66-68.
Hwang K.T., Kim S.W., Kim Y.H. (2013) Anatomical variation of the accessory thoracodorsal artery as a direct cutaneous perforator. Clin. Anat. 26: 1024-1027.
Kogan I., Lewinson D. (1998) Variation in the branching of the axillary artery. A
description of a rare case. Acta Anat. (Basel) 162: 238-240.
Natsis K., Piagkou M., Panagiotopoulos N.A., Apostolidis S. (2014) An unusual high
bifurcation and variable branching of the axillary artery in a Greek male cadaver.
Springerplus 3: 640.
Ravi K.S., Mehta V., Arora J., Suri R.K., Rath G. (2012) Clinico-embryological submission of an unilateral anomalous presentation of axillary artery. Bratisl. Lek. Listy
113: 725-727.
Rodriguez-Niedenfuhr M., Burton G.J., Deu J., Sanudo J.R. (2001) Development of the
arterial pattern in the upper limb of staged human embryos: normal development
and anatomic variations. J. Anat. 199: 407-417.
178
Pranit N Chotai et alii
Sato Y., Takafuji T. (1992) Abdominal part artery of axillary artery: proposed term for
the artery supplying the abdominal part of the musculus pectoralis major. Acta
Anat. (Basel) 145: 220-228.
Standring S. (2008) Gray’s Anatomy: The Anatomical Basis of Clinical Practice. 40th
edn. Churchill-Livingstone: Elsevier. Pp. 1412-1414.
Uglietta J.P., Kadir S. (1989) Arteriographic study of variant arterial anatomy of the
upper extremities. Cardiovasc. Intervent. Radiol. 12: 145-148.
IJA E
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I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Human anatomy case report
An anatomic variant causing a previously unreported
complication of transcutaneous treatment of
trigeminal neuralgia
R. Shane Tubbs1,*, Kimberly P. Kicielinski2, Joel Curé3, Benjamin J. Ditty2, Barton L. Guithrie2
1Seattle Science Foundation, Seattle, WA and Departments of 2Neurosurgery and 3Neuroradiology, University of
Alabama, Birmingham, AL
Abstract
This case report describes a patient with an anatomic variant of the foramen ovale that was
encountered during an attempted glycerol rhizolysis for trigeminal neuralgia. Various complications have been reported during transcutaneous trigeminal neuralgia treatment. We report an
adult female on whom transcutaneous cannulation of the foramen ovale was not possible. Subsequent imaging revealed a causative elongation of the spine of the sphenoid that distorted the
foramen ovale and effectively blocked it. Variations in bony anatomy may complicate transcutaneous approaches to the foramen ovale for the treatment of trigeminal neuralgia.
Key words
Skull base, trigeminal nerve, pain syndromes, neurosurgery, foramen ovale, spine of sphenoid,
anatomy
Introduction
Trigeminal neuralgia can be a life altering problem and probably has several etiologies. Transcutaneous methods for accurately identifying the foramen ovale (Fig.
1) for the placement of needles (for injection of various neurotoxic substances), radiofrequency thermocoagulation probes and compressive balloons into the trigeminal
cistern have been used for the treatment of trigeminal neuralgia, including stereotactic frames, CT-guided techniques, image-guided fluoroscopy, and plain radiographs
(Browsher, 1997; Taha and Tew, 1997). In general, complications from such procedures
include dysesthesia, transient bradycardia, corneal ulceration, and recalcitrant facial
pain (Taha and Tew, 1997). Herein, we report a very unusual complication from an
enlarged spine of the sphenoid bone that resulted in abandoning a transcutaneous
procedure for the treatment of trigeminal neuralgia.
Case report
A 41-year-old African American female presented with the acute onset of severe,
lancinating left jaw pain while chewing in January of 2011. The pain was exacerbated
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
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DOI: 10.13128/IJAE-18492
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R. Shane Tubbs et alii
Figure 1 – Dry skull specimen illustrating the normal anatomy of the left sphenoid spine (SS). For reference,
note the clivus, left foramen ovale (FO) and left foramen spinosum (FS).
by drafts, extreme temperature, palpation of the face, as well as speaking and swallowing. She described the pain primarily under her left eye, jaw, and extending to
the left tongue. Though she noted the pain originated acutely in January, her medical record indicates several emergency department visits for discrete episodes of
self-limited left jaw and neck pain dating back to April 2011. She underwent diagnostic work up with non-contrast computerized tomography of the head and magnetic resonance imaging of the brain with and without contrast as well as magnetic
resonance angiography which were unrevealing for intracranial pathology, specifically no demyelinating or inflammatory lesions were identified. She was evaluated by
neurologists and diagnosed with trigeminal neuralgia. Her face pain was refractory
to medical treatment with carbamezapine, baclofen, gabapentin, and pregabalin. She
was then referred to the neurosurgery service in May 2012 where surgical intervention with glycerol rhizolysis, microvascular decompression, or gamma knife stereotactic radiosurgery were discussed. The patient opted for glycerol rhizolysis. Following
alcohol skin prep and initiation of monitored anesthesia, a spinal needle was inserted
1 centimeter lateral and below the left corner of the mouth and directed towards the
foramen ovale. Jaw jerk and patient wince correlated with fluoroscopic evidence of
penetration of the region of the V3 branch of the trigeminal nerve. Iohexol contrast
was injected through the spinal needle under live fluoroscopy, revealing the spinal
needle not to have penetrated the foramen ovale. Four attempts were made to access
the foramen ovale before the procedure was aborted. Post-procedural imaging noted
bilateral enlargement and elongation of the spine of the sphenoid bones that caused
Elongated sphenoid spine
181
Figure 2 – 3D reconstructed CT of the skull base from the patient presented herein. Not the enlarged spines
of the sphenoid and bilateral foramina ovalia (FO). The ipsilateral foramen ovale is deformed and effectively
blocked by the sphenoid spine elongation when a needle is advanced in the typical anterolateral approach
used in transcutaneous approaches to treat trigeminal neuralgia.
deformation of the foramen ovale and effectively blocked this structure from the
approaching transcutaneous needle (Fig. 2).
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R. Shane Tubbs et alii
Discussion
Typical needle pathways used for transfacial transcutaneous approaches to the
foramen ovale include a skin insertion 2 to 3 cm lateral to the corner of the mouth
aimed at the medial aspect of the ipsilateral pupil in the left-right plane and at a
point 2.5 cm anterior to the tragus in the anteroposterior and superior-inferior planes.
This takes the needle along a pathway toward the junction of the medial and inferior walls of the orbit, 0.5 cm anterior to the condyle of the mandible and aimed at a
point 1 cm behind the posterior clinoid along the angle of the clivus (Browsher, 1997).
A needle entry site that is too medial results in the placement of its tip lateral to the
foramen ovale, and a needle entry site that is too lateral results in the placement of
the needle medial to the foramen ovale.
The spine of sphenoid bone is an irregularly shaped projection originating
from the posterolateral edge of the greater wing just lateral. Placed just lateral to the
foramen spinosum and posterolateral to the foramen ovale, the spine of sphenoid
is an attachment site for the sphenomandibular and pterygospinous ligaments. The
sphenomandibular ligament widens as it descends and attaches to the lingula of the
mandibular foramen. Along with the stylomandibular ligament and temporomandibular ligament, these support the temporomandibular joint. The pterygospinous
ligament connects the posterior border of the lateral pterygoid plate to the spine of
sphenoid. The chorda tympani and auriculotemporal nerves travel medial to the
spine of the sphenoid. Both these nerves are at risk of damage in cases of fracture of
the spine of the sphenoid with resultant loss of salivary gland innervation and taste
on the anterior two-thirds of the tongue and sensory loss anterior and superior to
the tragus.
With the mandibular branch of the trigeminal nerve coursing through the foramen
ovale and Meckel’s cave being a site for treatment of trigeminal neuralgia through
transcutaneous injections, understanding the anatomy and possible causes of obstruction to the site is important for clinicians to take into account before and during the
procedure. Included as a cause of obstruction of the foramen ovale are bony bars.
For example, ossification of the pterygospinous ligament creates a foramen through
which the mandibular segment of the trigeminal nerve travels before innervating the
masseter, temporalis and lateral pterygoid muscles. These foramina have been shown
as a possible cause of obstruction and increased difficulty of access to the foramen
ovale for percutaneous injections and possible compression of the mandibular branch
of the trigeminal nerve (Tubbs et al., 2009). Ossification of either the pterygospinous
or stylomandibular ligament could result in an enlarged spine of the sphenoid causing obstruction in the foramen ovale.
To our knowledge, obstruction of the foramen ovale due to an enlarged spine of
the sphenoid bone has not been described. Although apparently very rare, such a
cause may be considered by the neurosurgeon during procedures where the foramen
ovale cannot be entered via a transcutaneous route. In our case, the elongation distorted the normal anatomical position of the foramen ovale and effectively blocked it
from the typical anterolateral transcutaneous approach used to treat trigeminal neuralgia.
Elongated sphenoid spine
183
Ethics
This study complies with ethical standards of the United States. The authors deny
any conflict of interest.
References
Bowsher D. (1997) Trigeminal neuralgia: an anatomically oriented review. Clin. Anat.
10: 409-415.
Taha J.M., Tew J.M. Jr. (1997) Treatment of trigeminal neuralgia by percutaneous radiofrequency rhizotomy. Neurosurg. Clin. N. Am. 8: 31-39
Tubbs R., May W.R. Jr, Apaydin N., Shoja M.M., Shokouhi G., Loukas M., CohenGadol A.A. (2009) Ossification of ligaments near the foramen ovale: an anatomic
study with potential clinical significance regarding transcutaneous approaches to
the skull base. Neurosurgery 65: 60-64.
IJA E
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I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Human anatomy case report
Unilateral duplication of parotid duct – a rare cadaveric
case report
Sumathi Shanmugam*, Nithiyapriya Raju, Kalaiyarasi Subbiah, Sivakami Thiagarajan
Thanjavur Medical College, Thanjavur, India
Abstract
The parotid gland is drained by the parotid duct which normally measures 50 mm in length
and 3 mm in width. The parotid duct emerges at the anterior border of the gland and runs
horizontally across the masseter muscle to pierce the buccinator and open into the vestibule of
the mouth. The occurrence of double parotid duct is 7% and there are only very few literature
references. The parotid gland develops as an epithelial bud arising from the oral ectoderm and
invaginating into the underlying mesenchyme. The proximal part canalises to form the duct
and the distal end differentiates to form the acini. An early division of the parotid duct with
acini from both ducts intermingling with each other results in the formation of double parotid
duct. The cytodifferentiation and morphogenesis of parotid gland are influenced by cell specific gene expression and cell-matrix interactions that produce collagen responsible for branching and hyaluronidase responsible for acini formation. The awareness of presence of a double
parotid duct is significant in ductal endoscopic procedures and in performing surgery in the
parotid region.
Key words
Parotid gland, parotid duct, duplication, autopsy
Introduction
The parotid gland is the largest of the salivary glands. The secretion of this gland
reaches the oral cavity through the parotid duct (Stensen`s duct). The normal parotid
duct measures about 50 mm in length and 3 mm in width. It runs horizontally forwards across the masseter and turns medially at its anterior border to pierce the buccinator. The duct opens into the vestibule of the mouth by piercing the mucous membrane of the cheek opposite the upper second molar tooth (Williams et al., 1995). The
occurrence of double parotid duct is seen in 7% of population (Bailey, 1971). On the
contrary there are few reports in the literature about the parotid duct variations.
The awareness of the normal topographic anatomy and variations of parotid duct
is highly relevant to analysis of radiographic images and computerised tomography
scans used in sialography as well as for duct endoscopy, lithotripsy and transductal
facial nerve stimulation in early stages of facial nerve palsy (Zenk et al., 1998; Moore
et al., 2005). We report here a case of double parotid duct on one side, a very rare
presentation.
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18493
Unilateral duplication of parotid duct
185
Case report
During routine cadaver dissection in the department of Anatomy, we found a
double parotid duct on the left side of the face of a 78 year old male subject. Both
the parotid ducts - the superior and inferior one - were carefully dissected and traced
from the anterior border of parotid gland to their fusion with each other to form the
main parotid duct at a distance of 7 mm from the anterior border of parotid gland.
The main parotid duct was traced up to its piercing the buccal fat pad. The length of
the ducts and the outer diameter of the parotid ducts were measured using digital
calipers. The anterior border of parotid gland was taken as the reference to measure
the length of the ducts. The lengths of the superior (D1) and inferior ducts (D2) were
8 mm and 22 mm respectively. The diameters of the superior and inferior ducts were
2.5 mm and 3 mm respectively. The length of the main parotid duct was 23 mm and
Figure 1 – Double left parotid duct (D1 and D2) in a 78 year old male. MPD: Main parotid duct.
186
Sumathi Shanmugam et alii
its diameter at the anterior border of masseter was 4 mm. The distance between the
superior and inferior ducts at the anterior border of parotid gland was 17 mm. On
the right side, there was a single parotid duct measuring 55 mm in length and 4 mm
in diameter at the anterior border of masseter.
Discussion
The parotid gland is located below the external acoustic meatus and zygomatic
arch and between the ramus of mandible and sternocleidomastoid muscle. The parotid duct is formed by the confluence of two or three ducts within the anterior part of
the gland at the centre of the posterior border of ramus of mandible. The main parotid duct emerges at the anterior border of the gland.
The parotid gland begins to form during the sixth to seventh week of development. On each side, a solid epithelial bud arises from the primordial oral ectodermal
lining that invaginates into the underlying mesenchyme as an elongated furrow running dorsally towards the ears between the maxillary and mandibular prominences.
This cord of cells later becomes canalised to form a duct by about the tenth week.
The rounded posterior end of the cord branches and differentiates to form the secretory acini. The gland commences its secretions at around 18 weeks of gestation. As
the size of oral fissures decreases the duct opens into the inside of the cheek (Moore
et al., 2002). Sometimes an early division of the parotid duct occurs and the epithelial
sprouts from both ducts invaginate individually into the surrounding mesenchyme
and intermingle with each other. This may lead to development of two parotid ducts
with acini from both ducts ramifying to form the parotid gland.
This case of double parotid duct on the right side of a male cadaver adds to the
small list of cases in the literature. The ascending and descending intraparotid ducts
should normally merge within the gland to form the main parotid duct (Aktan et al.,
2001). Double parotid ducts measuring 26.49 mm and 37.25 mm in length and merging 3.35 mm proximal to the piercing of buccinator were present on the right side of
a 46 year old male cadaver (Fernandes et al., 2009). Also, double parotid ducts were
seen bilaterally in a 50 year old male cadaver. The length of the ducts on the right
side was 29 mm and 36 mm and that of the ducts on the left side was 28 mm and 34
mm. The ducts merged with each other at the level of the anterior border of masseter on both sides (Astik and Dave, 2011). An unilateral double parotid duct with the
superior duct measuring 28 mm and the inferior duct measuring 37 mm merged to
form the main parotid duct within an accessory parotid gland and then emerged to
run forward to pierce the buccinator; the length of the main parotid duct was 25 mm
(Mohammed et al., 2014).
The branching of a tubular duct occurs as a result of interaction between the proliferating epithelium of the duct and its surrounding mesenchyme. During tubular
and acinar development, hyalouranidase secreted by the underlying mesenchymal
cells breaks down the basal lamina produced by the epithelial cells thus increasing
the epithelial mitoses locally and resulting in the formation of an acinus.The cleft
formation for branching is initiated by the collagen III fibrils produced by the mesenchyme.The collagen acts to protect the basal lamina and the overlying epithelia from
the effects of hyalouranidase resulting in a series of clefts that produce a characteris-
Unilateral duplication of parotid duct
187
tic branching pattern. If the collagen is removed no clefts develop whereas if excess
collagen is produced then supernumary clefts appear (Standring et al., 2005).
The development of parotid gland occurs in six stages pertaining to the growth,
cytodifferentiation and morphogenesis influenced by intrinsic and extrinsic factors.
The cell specific gene expression and cell-cell and cell-matrix interaction and growth
factors influence the synthesis and deposition of type I and type III collagen. These
are required for branching morphogenesis. The collagen synthesis stabilizes and
maintains the branch points and specific growth factors regulate the branching patterns (Avery et al., 2002).
This variant anatomy of parotid duct has been reported as a very rare occurrence
with only a handful of literature reports. The knowledge of such variations of parotid
duct is significant in investigative procedures like diagnostic sialography, miniaturised salivary duct endoscopy and in planning surgical interventions in the parotid
region. This awareness helps to avoid accidental damage to these duplicated parotid
ducts.
References
Aktan Z.A., Bilge O., PinarY.A., Ikiz A.O. (2001) Duplication of the parotid duct: a
previously unreported anomaly. Surg. Radiol. Anat. 23: 353-354.
Astik R.B., Dave U.H. (2011) Embryological basis of bilateral double parotid ducts: a
rare anatomical variation. Int. J. Anat. Variat. 4: 141-143.
Avery J.K., Steele P.F., Avery N. (2002) Oral Development and Histology, 3rd edn.
Thieme, New York. Pp. 293-296.
Bailey L. (1971) Short Practice of Surgery, 15th edn. Lewis, London. P. 533.
Fernandes A.C.S., Lima G.R., Rossi A.M., Agular C.M. (2009) Parotid gland with double duct: An anatomic variation description. Int. J. Morphol. 27: 129-132.
Hassanzadeh Taheri M.M., Afshar M., Zardast M. (2015) Unilateral duplication of the
parotid duct, its embryological basis and clinical significance: a rare cadaveric case
report. Anat. Sci. Int. 90: 197-200.
Moore K.L., Dalley A.F. (2005) Clinically Oriented Anatomy, 5th edn. Lippincott Williams & Wilkins, Toronto. Pp. 926-927.
Moore K.L., Persaud T.V.N. (2002) The Developing Human: Clinically Oriented
Embryology, 7th edn. Saunders, Philadelphia. Pp. 220-221.
Standring S. (2005) Gray`s Anatomy, 39th edn. Churchill Livingstone, Edinburgh. Pp.
204-206.
Williams P.L., Bannister L.H., Berry M.M., Collins P., Dyson M., Dussek J.E. (1995)
Gray`s Anatomy, 38th edn. Churchill Livingstone, New York. Pp. 1692-1699.
Zenk J., Hoseman W.G., Iro H. (1998) Diameters of the main excretory ducts of the
adult human submandibular and parotid gland. Oral Surg. Oral Med. Oral Pathol.
Oral Radiol. Endod. 85: 576-580.
IJA E
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I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Human anatomy case report
A rare anomaly of the human spleen with nine notches
associated with multiple accessory spleens. A case
study, hypothesis on origin and review of clinical
significance
Thanya I. Pathirana1, Matthew J. Barton2,*, Mark George3, Mark R. Forwood4, Sujeewa P.W.
Palagama5,6
1 Centre for Research in Evidence Based Practice, Faculty of Health Sciences and Medicine, Bond University, Gold
Coast, Australia; 2 Centre for Musculoskeletal Research, Menzies Health Institute Queensland, Griffith University,
Gold Coast, Australia; 3 Surgery Department, Redcliffe Hospital Queensland Health, Redcliffe, Australia; 4 School
of Medical Sciences, Griffith University, Gold Coast, Australia; 5 School of Medicine, Griffith University, Gold
Coast, Australia; 6 Post Graduate Institute of Medicine, University of Colombo, Sri Lanka
Abstract
In humans, the spleen is the body’s largest secondary lymphoid organ and filterer of blood.
The trabeculated structure of the spleen, which is formed in its early embryonic development,
provides its three-dimensional framework designed to remove senescent erythrocytes and
eliminate blood-borne microorganisms and/or dubious antigens. At a later date this lobulated
framework can develop into notches which usually manifest along its anterior (superior) border. This study addresses the clinical significance and developmental basis of both numerous
notches and multiple accessory spleens observed in a male human cadaver. The nine notches
were all observed on the anterior and inferior borders, whilst the accessory spleens numbered
four, with two localized at the splenic hilum and the other two upon the splenorenal and splenocolic ligaments respectively. In the present study, we propose an aetiological origin for the
anomalous multi-notches and accessory spleens, which will provide primary benefit for surgeons and radiologists because of clinical significance.
Key words
Spleen, splenic notch, accessory spleen, anatomy, spleen anomaly
Introduction
The spleen is the largest secondary lymphoid organ in the human body (Borley,
2005). It plays an important role in regulating the number and quality of erythrocytes,
eliminating cellular debris from the blood, and responding against antigens and/or
virulent pathogens that may have entered the systemic circulation (Mebius and Kraal,
2005). In all mammals the spleen is enclosed by a capsule (Fig. 1) of variable thickness
(Onkar and Govardhan, 2013), the capsule in distinct regions ventures into the spleen's
parenchyma through trabeculae (Fig. 1). The tissue residing between the capsule and
trabeculae forms the cords or pulp (Fig. 1), which by histological appearance can be
categorised as red or white pulp and takes upon either storage or defensive functions
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18494
Human spleen anomaly
189
Figure 1 – Schematic drawing of spleen, anterior view. Insert box: cut through anterior border, illustrating
the typical histology of the spleen with: a) capsule; b) cords; c) trabecula; A) artery; V) vein.
respectively. The embryonic development of the human spleen is yet to be fully elucidated, nonetheless within the left dorsal mesogastrium around the 5th week of gestation multiple mesenchymal (reticular) cells aggregate and give rise to a lacuna of haematopoietic tissues. By the 8th week, the spleen has a segmented morphology based
on arterial lobules, which gradually disappear around week 30, as the spleen develops
its lymphoid structures (Balogh and Labadi, 2010). The immune function of the spleen
is mediated initially by the migration of B lymphocytes which colonize these lacunae peripherally and then by T lymphocytes centrally around arterioles (Mebius and
Kraal, 2005). As this tissue develops, the scant few nodules eventually fuse to form
the spleen proper. The points of union of these nodules are believed to be the reason
behind the spleen’s lobulation and notching on its anterior (superior) border (Coetzee,
1982). However, in some instances, some of these nodules may remain independent of
the spleen proper and form accessory spleens (Nayak et al., 2014).
An enlarged spleen can be clinically detected in the left hypochondriac region
of the abdomen through palpation. The notch on its anterior border aids in identifying the spleen and differentiating it from other abdominal organs (Coetzee, 1982;
Standring, 2008). Therefore, a variation in the number and location of notches may
impede the clinical diagnosis of an enlarged spleen (Gandhi et al., 2013). Although
traditional anatomical literature has invariably reported that the spleen has only one
or two main notches (Standring, 2008), Michels (1942) maintained that the number of
190
Thanya I. Pathirana
notches may vary from one to six, while more recently Gandhi et al (2013) described
a case where one spleen had seven notches.
Islands of healthy, functional splenic tissue located separately from the main
spleen are known as accessory spleens; splenules or supranumerary spleens (Freeman
et al., 1993), a phenomenon which surprisingly is not that uncommon. Curtis and
Movitz (1946) confirmed the presence of accessory spleens in 56 patients out of 174
while Halpert and Gyorkey (1959) revealed 364 accessory spleens in 3000 patients.
The presence of accessory spleens has not yet been correlated to any pathological
consequences. However, accessory spleens may become highly significant in specific
circumstances where their presence could lead to a recurrence in certain haematological conditions such as thalassemia following splenectomy (Curtis and Movitz, 1946;
Facon et al., 1992; Budzynski et al., 2003). Conversely, accessory spleens have been
shown to be advantageous by providing innate immunity following splenectomy
subsequent to trauma (Leemans et al., 1999). Splenectomised patients may be unable
to mount appropriate immune responses to bacterial insult, which can be exacerbated
when the patient’s immune system is already compromised (i.e schistosomiasis) and
may be further susceptible to bacterial translocation and sepsis (Lima et al., 2015),
thus requiring preoperative vaccinations and ongoing boosters (Dogan et al., 2015;
Nived et al., 2015), or lifelong prophylactic antibiotics. Although the number of accessory spleens can vary from 1 to 10, more than 3 accessory spleens are considered very
rare (Curtis and Movitz, 1946). Moreover, if accessory spleens are indeed present,
they tend to be located in only one anatomical locations such as splenic hilum or
pedicle (Curtis and Movitz, 1946). In the present specimen, we report a spleen with
nine notches associated with four accessory spleens located in three different anatomical locations rendering this a very rare anomaly and the first to be described in the
anatomical literature to the best of the authors’ knowledge.
Material and methods
This anomalous spleen was detected during a routine dissection on a formalin
fixed male human cadaver (71 years of age). Once the anomaly was identified, the
spleen along with its arterial and venous supply was resected, including: the stomach, from the lower oesophageal junction, the duodenum, the short gastric vessels,
pancreas, coeliac arterial trunk and mesenteric veins up to the formation of portal
vein. All structures were removed out en block for permanent fixation and plastination. All material was made available by the School of Anatomy, Griffith University,
in accordance with the Queensland Transplantation and Anatomy Act,1979, and the
signed informed consent of the donor.
Results
The spleen was situated under the diaphragm between the stomach and left kidney, posterior to the splenic flexure of the colon. It was intraperitoneal and attached
to the stomach and kidney via the gastrosplenic and splenorenal ligaments respectively. The size of the spleen (Fig. 2) was 13 cm in length, 9 cm in width and 5 cm
Human spleen anomaly
191
Figure 2 – A) Photograph of adult spleen with nine notches (numbered 1 to 9) along the anterior border
and two accessory spleens (As); two other accessory spleens are not shown. Splenic artery trifurcates before
entering the hilum, superior to the pancreas. The two accessory spleens are magnified in panels B) and C) to
demonstrate the blood vessel supply.
in thickness; the weight was 322.2 grams which is heavier than normally described
(Gray, 1897). Along the anterior (superior) border eight notches (Fig. 2A) of variable
depth were present at variable distances from each other. Another shallow notch facing the renal surface was present in the inferior border. There were four accessory
spleens, two at the splenic hilum (Fig. 2; size 1 cm x 1.5 cm x 1 cm and 2.5 cm x 2
cm x 1.5 cm) which had dedicated arterial twigs (Fig. 2B ultimate branch and Fig.
2C inferior polar arteries) branching out of the main splenic artery (Fig. 2A) and two
others (not shown) each of 1.5 cm x 1 cm x 1 cm, one on the splenorenal ligament
(arterial supply by superior polar artery) and the other on the splenocolic ligament
(arterial supply by inferior polar artery). The arterial supply of the spleen was via a
tortuous but direct splenic artery (Fig. 2A), a branch of the coeliac trunk. The splenic artery trifurcated (Fig. 2A) into three main branches: superior, middle (ultimate)
and inferior polar arteries. These arteries were paralleled by their respective venous
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Thanya I. Pathirana
counterparts, which drained the respective accessory spleens into the splenic vein.
The small arterial branches supplying the spleen did not correlate to the individual
splenic notches. Other intra-abdominal organs appeared normal in their gross anatomical morphology, and there was no evidence of situs inversus. The cadaver exhibited hypospadias but the heart and lungs showed no gross anomalies.
Discussion
Anatomical significance
The number of notches on the spleen has been a topic of scientific discussion since
1901 whence Parsons (1901) documented it to range from 0 to 7, with 2 notches being
most common. Furthermore, he claimed a spleen with 7 notches to be exceptionally
rare, reporting only one specimen out of 113. After Parsons (1901), the highest number of notches to be noted in anatomical literature is 7, which was recently reported
in India (Gandhi et al., 2013). Prior to that, there have been other reports of splenic
notches ranging in number from 0 to 7 (Michels, 1942; Redmond et al., 1989; Das et
al., 2008). The present specimen is unique, given that there are 8 notches on the anterior surface and another distinct notch on the inferior surface (Fig. 2).
Accessory spleens are the most common anomaly associated with the spleen and
are identified in 10-30% of cadavers at autopsy (Dodds et al., 1990; Freeman et al.,
1993; Gayer et al., 2001). Previous evidence from cadaveric studies has demonstrated the occurrence of one, two and three accessory spleens to be 79-86%, 10.5-14%
and 1-10.5% respectively (Mortelé et al., 2004; Mendi et al., 2006; Üngör et al., 2007;
Unver Dogan et al., 2011). In a large study examining accessory spleens in CT scans,
13% subjects had one or more accessory spleens (Mortelé et al., 2004). Although the
presence of more than three accessory spleens has been reported, it is considered a
very rare occurrence (Curtis and Movitz, 1946). Moreover, accessory spleens tend to
be located around a single anatomical location and thus accessory spleens in multiple anatomical locations are considered exceedingly rare (Curtis and Movitz, 1946).
The present specimen had four accessory spleens located in three different locations
rendering it unique. Two of the four accessory spleens were situated at the splenic
hilum, which is the most common site for accessory spleens (Halpert and Gyorkey,
1959; George et al., 2012), while the other two were located within the splenorenal
and splenocolic ligaments respectively.
Previous anatomical literature of human spleens with multiple notches is devoid
of any description for associated accessory spleens. Nor have there been reports of
accessory spleens described with the concomitance of multiple notches. Thus, this
study is exclusive to anatomical literature in that it reports 9 splenic notches associated with 4 accessory spleens.
Basis of multiple notches
The causality of splenic notches or accessory spleens has not been fully explained
by phylogenetic studies in literature. Schabadash (1935) investigated a total number
of 255 animals consisting of fish, amphibians, reptiles, birds and mammals and did
Human spleen anomaly
193
not outline the phylogenetic significance of the size and form of the spleen in terms
of evolution (cited by Michels, 1942). Nevertheless, the hypothesis for the spleen’s
embryological formation is through the union of multiple splenic mesenchymal masses derived from the dorsal mesogastrium (Thiel and Downey, 1921; Michels, 1942),
colonized by progenitor cells of erythroid and myeloid origins (Mebius and Kraal,
2005), and by the differentiation and maturation of a milieu of lymphoid cells (Asma
et al., 1986). If that was the case, the presence of multiple splenic notches should
appear more frequently in foetuses than in adults, akin to the embryonic development of kidneys (Parsons, 1901). However, it has been established that spleens are
less notched in foetuses than in adults (Parsons, 1901). Thus the presence of splenic
notches is not adequately explained on an embryological basis.
Alternatively, the number of splenic notches may be explained by food pattern of
animals. Studies on carnivore and omnivore species such as cat, lion, dog, fox, otter
and seals demonstrated a higher number of notches (on all borders), while herbivore
species such as deer, ox, sheep, goat and horse show no notches or, rarely, one notch
(Parsons, 1901). This may be explained by the differences in histology of the splenic
capsule, where the thickness in humans has been shown to be significantly less when
compared to herbivories (cow and goat; Alim et al., 2012); in humans specifically the
splenic capsule appears to change with age. Rodrigues and colleagues (1999) showed
that within aging humans the elastic fibers within the capsule condense and fragment, thus affecting spleen integrity as one grows older.
As meat contains more immune active substances than plants (Masilamani et
al., 2012), it is conceivable that spleens of carnivores experience greater immunological insults than that of herbivores. As the human spleen ages and loses cortical
rigidity, while being challenged immunologically, the ensuing immune responses
may result in the remodelling of the spleen’s extracellular matrix (Mebius and
Kraal, 2005), thus causing cleavage points between splenic cords which later give
rise to notches (Joo and Kim, 2014). Structural alterations of the spleen have been
demonstrated in amphibians when immune responses have been stimulated by
viral and bacterial pathogens (Balogh and Labadi, 2010). The spleen is the principal organ of immunity and it is via food that the body is exposed to the largest load of immune active substances. We hypothesise that it may be the food
(through immune active substances) along with histological alterations of the
spleen’s capsule that govern the development of multiple foci of the spleen and
may explain the presence of multiple notches in adults. This will occur postnatally
when the body is exposed to exogenous antigens in food, which is distinct to the
embryo where it would be exposed to negligible immune active material. This is
consistent with the observation of foetal spleen having less pronounced notches
than that of adults (Parsons, 1901).
Clinical significance
Identifying splenomegaly is extremely important in clinical practice when diagnosing diseases. Variations in the size of the spleen, particularly an enlargement,
usually reflect an underlying pathology of either the reticuloendothelial system
or the lymphoid system (Kumar et al., 2009; Rayhan et al., 2011. Even though the
splenic size is routinely gauged ultrasonographically (Lamb et al., 2002), it is com-
194
Thanya I. Pathirana
monly through clinical palpation that splenomegaly is diagnosed. When examining
the spleen clinically, one of the most characteristic findings is the splenic notch which
distinguishes it from other organs in the left hypochondriac region. Therefore multiple notches may lead to a false positive clinical diagnosis of splenomegaly (Gandhi
et al., 2013). Furthermore, when there are multiple notches present in the anterior
border, these lobulations may easily be mistaken for neoplasms of the kidney and/
or adrenal gland radiologically. Moreover, in patients with blunt abdominal trauma
to the left hypochondrium, the presence of multiple deep and sharp notches on the
spleen may inaccurately be misinterpreted as splenic lacerations, possibly resulting in
an unnecessary exploratory laparotomy (Gayer et al., 2006; Joo and Kim, 2014).
Accessory spleens are usually asymptomatic. However, if present, they can be
mistaken for neoplasms or lymph node enlargements in organs such as the pancreas, kidney, or adrenal gland (Servais et al., 2008; George et al., 2012). Cognisance of
accessory spleens by health professionals may facilitate correct diagnosis and avoid
unnecessary invasive interventions (Zhang and Zhang, 2011). Rarely, accessory
spleens may present with abdominal pain if they undergo torsion (Wacha et al., 2002;
Grinbaum et al., 2006).
Where the spleen necessitates removal for therapeutic interventions, such as idiopathic thrombocytopaenic purpura, accessory spleens may remain inadvertently after
surgery and thus impede complete resolution (Facon et al., 1992; Budzynski et al.,
2003). This is because accessory spleens can also be involved in any condition involving the spleen (Joo and Kim, 2014). Therefore, the European Association of Endoscopic Surgeons has recommended that accessory spleens be investigated routinely during
laparoscopic surgery for splenectomy especially in autoimmune haematological disorders (Rudowski, 1985; Gigot et al., 1998; Unver Dogan et al., 2011).
The presence of multiple spleens is associated with congenital anomalies of other
visceral organs and some syndromes (Rose et al., 1975; Gayer et al., 2006; Tawfik et
al., 2013). Heterotaxy syndrome is one such syndrome that is characterized by abnormal arrangement of organs and vessels across left right axis of the body (Strickland
et al., 2008). In this syndrome, polysplenia is associated with bilateral left sidedness
(Gayer et al., 2006) such as bilateral bilobed lungs (Peoples et al., 1983), inferior vena
cava obstruction with azygous continuation (Gayer et al., 1999), none of which was
seen in the present specimen. Conversely however, a favourable outcome of having
accessory spleens has been demonstrated in patients who had undergone emergency splenectomy, where functional accessory spleens accommodated some humoral
immunity (Leemans et al., 1999).
Conclusions
The present study reports a unique specimen with a variation in splenic anatomy,
including the highest number of splenic notches reported in the known anatomical
literature. It was also accompanied by multiple accessory spleens in three different
anatomical locations. A novel hypothesis on the occurrence of multiple splenic notches based on exposure to immunologically active substances after birth is proposed.
Human spleen anomaly
195
Acknowledgments
The authors express their gratitude to the donor cadavers and their families who
participated in the body donation program at Griffith University, and the technical
staff in the Department of Anatomy, in particular Mr. Peter Bentley-Brown, for assistance with specimen preparation.
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IJA E
Vo l . 121, n . 2: 19 8 -20 4, 2016
I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Basic and applied anatomy
The anatomy of the medial collateral ligament of the
knee and its significance in joint stability
Konstantinos Markatos1,*, Georgios Tzagkarakis¹, Maria Kyriaki Kaseta², Nikolaos Efstathopoulos²,
Panagiotis Mystidis1, Demetrios Korres2
¹ First Orthopaedics Department, Henry Dunant Hospital, Athens, Greece
² Second Department of Orthopaedic Surgery, University of Athens, Medical School, Athens, Greece
Abstract
The medial collateral ligament (MCL) is the most important stabilizer of the medial side of the
knee together with the capsuloligamentous complex. As such, it has a distinctive role in joint
stability, as far as its biomechanics are concerned, and major joint stability issues onset when it
is injured or deficient. One of the main functions of the medial collateral ligament is mechanical as it passively stabilizes the knee and help in guiding it through its normal range of motion
when a tensile load is applied. It exhibits nonlinear anisotropic mechanical behaviour, like all
ligaments, and under low loading conditions it is relatively compliant, perhaps due to recruitment of “crimped” collagen fibres as well as to viscoelastic behaviours and interactions of collagen and other matrix materials. Continued ligament-loading results in increasing stiffness until
a stage is reached where it exhibits nearly linear stiffness and beyond this it continues to absorb
energy until it is disrupted. In addition, the function of the MCL has to do with its viscoelasticity which assists the maintainance of joint congruity and homeostasis. The treatment of grade III
medial collateral ligament injuries (with gross valgus instability at 0° of flexion) is still controversial. The most severe injuries (especially with severe valgus alignment, intra-articular medial
collateral ligament entrapment, large bony avulsions, or multiple ligament involvement) may
require acute operative repair or augmentation. In addition, surgical reconstruction is indicated
for isolated symptomatic chronic medial collateral ligament laxity. The optimal surgical treatment remains controversial. More studies with evidence of level I and II are required in order
to clarify the pros and cons of any solution.
Key words
Medial collateral ligament, knee, anatomy, biomechanics, reconstruction, review
Introduction
The medial collateral ligament (MCL) is the most important stabilizer of the medial side of the knee together with the capsuloligamentous complex. As such, it has a
distinctive role in joint stability, as far as its biomechanics are concerned, and major
joint stability issues onset when it is injured or deficient (Drake, 2005).
The purpose of this review is to summarize MCL anatomy, to pinpoint its role in
knee stability, as far as its biomechanics are concerned, and to present its main reconstruction techniques. Thus, emphasis will be given to laxity after MCL tears and synergy of the MCL complex and cruciate ligaments. The most significant question pre* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18495
Medial collateral ligament anatomy and function
199
sented is when and how to repair the MCL because of the controversy between conservative and surgical treatment. This problem presents because of the absence of any
significant algorithm for decision making in the treatment of the MCL pathology.
Anatomy
The traditional anatomic description of the MCL regards it as a structure broadly
attached by most of its surface to the fibrous membrane. Superiorly it is described
attached to the medial femoral epicondyle inferior to the adductor tubercle, inferiorly,. it attaches to the medial surface of the tibia, above and behind the attachment of
sartorius, gracilis and semitendinosus (Drake, 2005).
A more detailed presentation of the anatomy of the medial aspect of the knee by
Warren and Marshall divides the underlying structures in three layers (Warren and
Marshall, 1979). Layer 1 mainly consists superficially of the sartorius muscle and posteriorly of fatty tissue. More deeply one can find the gracilis and the semitendinosus tendons. Next, layer 2 is the plane of the superficial MCL made of parallel and
oblique bundles of connective tissue fibres. The anterior part consists of parallel fibres
from the medial femoral epicondyle to the medial surface of the tibia posterior to the
pes anserinus. Posterior oblique fibres are connected to layer 3 fibres and form the
posteromedial capsule of the knee joint.
According to Sinclair et al. (2011) ligament attachment strength can be attributed
to several factors, including the ligament’s area of attachment, regional thickness, and
mineral content of the MCL. The MCL consists of two major components: an abundant extracellular matrix (ECM) and ligament cells embedded in the ECM. Benjamin
et al. (1986) report that cells in ligaments like the MCL are arranged into a series of
widely spaced rows with cytoplasmic extensions that extend from cells in one row
to those in another. In addition Chi et al. (2005) showed that in addition to gap junctions, adherens junctions and desmosomes are also expressed by MCL cells both in
vivo and in vitro and map to sites of cell–cell contact.
According to Laprade et al. (2007) and Bonasia et al. (2012), as far as the superficial
MCL is concerned, the femoral attachment is elliptical and placed on average 3.2 mm
proximal and 4.8 mm posterior to the medial epicondyle. The proximal tibial attachment
is primarily to the semimembranosus tendon. The distal tibial attachment is anterior to
the posteromedial crest of the tibia. The length from the proximal tibial attachment to
the tibial joint line is 12.2 mm. The average distance of the distal tibial attachment is 94.8
mm from the femoral attachment, and 61.2 mm from the tibial joint line. The average
distance from the distal tibial attachment to proximal tibial attachment is 49.2 mm.
In addition, according to Warren and Marshall (1979) the deep MCL is an anatomic component of the medial joint capsule. It consists of the meniscofemoral and
meniscotibial ligaments. The meniscofemoral ligament is longer than the meniscotibial ligament and is found posterior and distal to the medial epicondyle. The meniscotibial component is shorter, thicker and attached distal to the medial tibial plateau.
According to Phisitkul et al. (2006) the ligament length and its insertion areas on
the femur and tibia have been measured upon dissection of cadaveric human knees
in full extension. The superficial MCL has been described by James (1978) as triangular in shape and with the proximal and distal parts composed of parallel fibres,
200
Konstantinos Markatos et alii
whereas the middle part of the superficial MCL as composed of parallel and oblique
fibres. They described the width of proximal and distal parts as similar in the anterior-posterior direction. The anterior portion does not seem to be connected to the
medial meniscus and it is distinguished from the capsule of the knee joint. However,
the posterior portion is connected very closely to the medial meniscus.
A number of anatomic studies have compared the two individual components of the
MCL. LaPrade et al. (2007) showed that the distal tibial insertion area is larger than the
femoral insertion area. Nevertheless, there is a debate in the description of the location
of the femoral insertion of the superficial MCL. There are those authors who describe
the femoral insertion of the superficial MCL as located on the medial epicondyle of the
femur while others report that the femoral insertion site of the superficial MCL is located slightly proximal to the medial epicondyle. Brantigan and Voshell (1946) propose that
a part of the superficial MCL is indistinguishable from the capsule, and anatomically
and functionally is connected to the medial meniscus. Last (1948) also observed that the
posterior part of the superficial medial ligament is attached to the medial meniscus. The
attachment of the superficial MCL to the medial meniscus cannot be overemphasized
since its removal during total knee arthroplasty can affect the stability of the superficial
MCL and allow varus correction without further soft tissue release.
The deep medial collateral ligament is a layer and a part of the medial joint capsule. The deep MCL consists of the meniscofemoral and meniscotibial ligaments. The
meniscofemoral ligament is longer than the meniscotibial ligament and its attachment
is located posterior and distal to the medial epicondyle. The meniscotibial ligament
is shorter, thicker and attaches just distal to the cartilage of the medial tibial plateau.
According to Robinson et al the disagreement whether the oblique fibres in the posterior third are part of the superficial MCL - or a thickening of the capsule - has no
practical significance. The most important point is that they seem to be a functional
unit with links to the semimembranosus tendon sheath (Robinson et al., 2004).
Biomechanics and function
One of the main functions of the MCL is mechanical as it passively stabilizes the
knee and helps in guiding it through its normal range of motion when a tensile load
is applied. It exhibits nonlinear anisotropic mechanical behaviour, like all ligaments,
and under low loading conditions it is relatively compliant, perhaps due to recruitment of “crimped” collagen fibres as well as to viscoelastic behaviour and interaction of collagen and other matrix materials. Continued ligament-loading results in
increasing stiffness until a stage is reached where it exhibits nearly linear stiffness
and beyond this it continues to absorb energy until it is disrupted (Frank, 2004).
In addition, the function of the MCL has to do with its viscoelasticity which
assists the maintenance of joint congruity and homeostasis. Load and stress to the
joint are diminished due to the action of the MCL and its inefficiency leads to constant deformation. The creep of the MCL is also an important parameter which is
referred to as the deformation-elongation under a constant or repetitive load. The
importance of creep cannot be underestimated since in knee reconstruction excessive creep could result in laxity of the joint thus predisposing it to further injury or
prosthesis failure (Woo and Young, 1991). The MCL has also an important role affect-
Medial collateral ligament anatomy and function
201
ing knee proprioception which concerns the conscious perception of limb position in
space. In the human knee, proprioception is provided principally by receptors in the
joint, muscle and cutaneous tissue (soft tissue). Strained ligaments evoke neurological
feedback signals that then activate muscular contraction and this appears to play a
role in joint position sense (Liu et al., 2010).
Biomechanically, the MCL is the main reacting ligament to valgus forces and a
secondary restraint to rotation forces and posterior translation of the tibia. The superficial MCL is the main stability to valgus forces from full extension to full flexion of
the knee. Resistance of the MCL against rotational forces starts being significant at 30o
of knee flexion with the relaxation of the posteromedial capsule. The superficial MCL
is the main ligament for medial stability even when the deep MCL is inefficient. On
the other hand, the posteromedial capsule is in tension and provides significant stability reacting to valgus forces, posterior tibial translation, and internal rotation with
the knee extended (Fuss, 1992).
The action of the posterior oblique ligament is crucial for the stability of the knee
joint. The posterior oblique ligament provides stability to tibial internal and external
rotation at knee flexion and posterior stability to the tibia in knee extension. The role
of the posterior oblique ligament becomes even more important when the MCL is
deficient for both valgus and rotational stability (Fuss, 1991).
According to Wilson et al. (2012), despite differences in geometry and strength,
there was no significant difference in stiffness of the MCL and lateral collateral ligament when tested in vitro. This means that stiffness is of secondary importance to
biological structure. Biological structure seems to be similar for both ligaments.
In their biomechanical studies, Stein et al. (2009) showed that there are only some
deep and tender fibrous bundles of the medial collateral ligament radiating into the
medial meniscus proximally and posteriorly. Their findings suggest that there is no relevant influence of the medial collateral ligament on the stability of the medial meniscus.
In their thorough review, Robinson et al. (2004) suggest that the posteromedial capsule functions as a passive restraint to internal rotation of the tibia with the knee in
extension. In addition, Hughston and Eilers (1973) suggested that the semimembranosus may play a role in the stability of the medial knee compartment. There is perhaps
a relation to the proximity of the semimembranosus to the MCL for this function.
Treatment of MCL injury
Although there is significant knowledge on the MCL, its anatomy and biomechanics,
there is a controversy concerning MCL injury treatment. The traditional rule expressed
by Hughston and Eilers (1973) that injuries grade I and II should be treated conservatively and injuries of the grade III should be treated operatively does not seem to be
adequate. Other factors affecting decision making should be MCL entrapment, bony
avulsion, co-existence of other injuries (especially anterior collateral ligament tears), valgus knee misalignment and finally acute or chronic injury (Fetto and Marshall, 1978).
Additional controversy rises when treating an anterior cruciate ligament tear coexisting with an MCL tear. In this case most authors suggest conservative treatment
of the MCL injury with surgical repair of the anterior cruciate ligament injury. The
MCL is proposed to be treated surgically only if instability of the knee remains after
202
Konstantinos Markatos et alii
the anterior cruciate ligament reconstruction (Marshall et al., 1977; Kannus, 1988;
Indelicato, 1995).
According to Phisitkul et al. (2006) conservative treatment should consist of a
hinged knee brace with weight bearing as tolerated and crutches for initial pain
relief. Isometric and range of motion exercises should be encouraged immediately in
order to ensure knee stability. Crutches are discontinued when the patient can walk
without limping. Anti-inflammatory medication are used as a common practice by
most physicians, but limited evidence support their use.
Surgical procedures for the MCL reconstruction comprise Kim ’s and Stannard ’s
techniques who both use a semitendinosus graft looped around a k-wire in a femoral attachment (Kim et al., 2008; Stannard, 2010), Lind ’s technique using tunnels for
the graft insertion into the femoral and the tibial insertion points with interference
screws (Lind et al., 2009), Yoshiya ’s single-bundle technique (Yoshiya et al., 2005),
Coobs’ technique for separate reconstruction of the MCL and posterior oblique ligament (Coobs et al., 2010), Borden ’s double-bundle technique using an anterior tibialis
graft and certain variations to the above main techniques (Borden et al., 2002). All of
them if executed properly seem to provide for adequate to excellent results.
What is particularly interesting in the literature is the absence of studies with high
level of evidence concerning the outcome of these surgical techniques, their complications and their advantages and disadvantages in general. Therefore it is pretty difficult to
make an unbiased conclusion as far as the comparison of these techniques is concerned.
In addition, there is little evidence on the different effectiveness of the rehabilitation protocols depending on the preferred reconstruction technique. More data are required to
evaluate which is the most efficient rehabilitation technique following each reconstruction
method. In order to clarify such issues, multi-centre, randomized studies are necessary.
Conclusion
The attachment strength of the MCL can be attributed to several factors, including
the ligament’s area of attachment, regional thickness, and mineral content.
The superficial MCL has a femoral insertion proximal and posterior to the medial
epicondyle. The proximal tibial attachment is primarily to the semimembranosus tendon. The distal tibial attachment is anterior to the posteromedial crest of the tibia.
The deep MCL is an anatomic component of the medial joint capsule. It consists
of the meniscofemoral and meniscotibial ligaments. The meniscofemoral ligament is
longer than the meniscotibial ligament and is found posterior and distal to the medial
epicondyle. The meniscotibial component is shorter, thicker and attached distal to the
medial tibial plateau.
Biomechanically, the MCL is the main reacting ligament to valgus forces and a
secondary restraint to rotation forces and posterior translation of the tibia. The superficial MCL is the main stability to valgus forces from full extension to full flexion of
the knee. Resistance of the MCL against rotational forces starts being significant at 30o
of knee flexion with the relaxation of the posteromedial capsule. The superficial MCL
is the main ligament for medial stability even when the deep MCL is inefficient.
The posterior part of the superficial medial ligament is attached to the medial
meniscus. The attachment of the superficial MCL to the medial meniscus is important
Medial collateral ligament anatomy and function
203
since its removal during total knee arthroplasty can affect the stability of the superficial MCL and lead to change preoperative planning and prevent further soft tissue
release. Removing a medial meniscus during a total knee arthroplasty can loosen the
MCL if the two are connected. This means that in a varus knee there is usually sufficient soft tissue release to correct for the varus deformity. However removing the
medial meniscus does not always affect the MCL which then needs further release
on its own. Basically what we do is to remove the medial meniscus and place the
implants. Then we test the movement of the knee to see if any varus deformity
remains. If this is the case we proceed with further MCL release.
Ethical standards
This article does not contain any studies with human participants or animals performed by any of the authors. All the authors declare to have no conflict of interest.
No funds were received in support of this study. No benefits in any form have been
or will be received from a commercial party related directly or indirectly to the subject of this manuscript.
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IJA E
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I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - Human anatomy case report
Formation of suprascapular foramen as a result of
ossification of superior transverse scapular ligament: a
case report and short review of the literature
Stylianos Kapetanakis*, Nikolaos Gkantsinikoudis, Aliki Fiska
Department of Anatomy, Medical School of Alexandroupolis, Democritus University of Thrace, Greece
Abstract
Ossification of superior transverse scapular ligament resulting in a bony suprascapular foramen
is of fundamental anatomical and clinical importance. In this case report, we describe a special case of a suprascapular foramen. Its specificity lies in foraminal dimensions, resulting in
a unique morphometrical pattern in comparison with reported similar cases. This pattern is of
great anatomical and clinical importance, because ossification of suprascapular foramen leads
to limitation of suprascapular notch, over which suprascapular nerve passes. Ossification can
consequently constitute a major predisposing factor for suprascapular nerve entrapment and
subsequent neuropathy. Therefore, this anatomic variation should be considered from surgeons
and other healthcare professionals.
Key words
Suprascapular foramen, superior transverse scapular ligament, ossification, variations, case
report, review
Introduction
The suprascapular foramen is formed normally by the suprascapular notch, which
is converted in a foramen by the superior trasverse scapular ligament in the scapular region (Moore et al., 2014). A recently reported ligament is present in the anterior
aspect, which leads to a significant decrease in the foraminal vertical diameter and
has been named anterior coracoscapular ligament (Avery et al., 2002).
However, the stability of this anatomic standard is disputed, as featured by the
report of many anatomical variations in current population. In 1979, six different
types of suprascapular notch were reported, which lead automatically to different
types of suprascapular foramen and complicate the possible foramen morphology
(Rengachary et al., 1979). In recent years, two cases involving double suprascapular
foramen were described and primarily attributed to ossification of superior transverse scapular ligament and anterior coracoscapular ligament, and to ossification of
bifid superior transverse scapular ligament (Polguj et al., 2012; Joy et al., 2015). Ossification of a single-bundle anterior coracoscapular ligament constitutes the cause of
another additional reported anatomical variation, the coexistence of suprascapular
notch and suprascapular foramen (Polguj et al., 2013).
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18496
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Stylianos Kapetanakis et alii
In this case report, we describe a single bony suprascapular foramen in a right
dry scapula, caused by ossification of superior transverse scapular ligament. To
our knowledge, this anatomic variation has been reported only three times (Das et
al., 2007; Tubbs et al., 2013; Polguj et al., 2014) and was additionally analyzed as a
special case in two other wide morphological studies (Albino et al., 2013; Kannan et
al., 2014). Nevertheless, it is interesting that in morphological analysis none of those
authors described a suprascapular foramen with so small diameters. Morphologically,
the originality lies in foraminal dimensions, which would not be expected according
to the recent classification settled in 2014 (Polguj et al., 2014). As a result, this morphology creates new perspectives in the clinical standards for suprascapular nerve
entrapment.
Case report
This anatomic variation was found during laboratory anatomical research. A total
of 20 scapulae were stored in the laboratory, 10 right and 10 left scapulae. Dry scapulae were derived from six men and four women of Greek ancestry. Mean age was
64,5 years with range from 63 to 66 years. Only one right dry scapula presented this
anatomically important feature. Based on the above, the percentage is 0,05% but the
sample was not wide enough for statistics. Measurements were performed to better
define the finding.
The morphology of the ossified superior transverse scapular ligament put it in
the category of fan-shaped ossified superior transverse scapular ligament according
to the classification first established in 2014 (Polguj et al., 2014). The length was 11.7
mm (black line in Fig. 1), and the ossified superior transverse scapular ligament (lateral part) formed the superior border of the foramen at the medial and posterior end of
coracoid process. The width was 9.5 mm in the middle (red line in Fig. 1), just over the
foraminal apex. The medial part of superior transverse scapular ligament adhered to
the superior border of scapula along an oblique line (yellow line in Fig. 1) 17 mm long.
The foramen has an ellipsoid shape with the superior apex laterally and the inferior medially. The maximum transverse diameter was only 3.88 mm, while the average vertical diameter was 6.46 mm with a maximum of 8.00 mm. The anteroposterior thickness was 3.04 mm. The distance from the superior angle of the scapula was
58.04 mm (Fig. 2), while the distance from the glenoid notch was 28.95 mm (Fig. 3).
The foramen surface area was 24.36 mm2. Osteological deformities were not noticed
in general during anatomical examination, except for two imperceptible breaks in
the lower part of subscapularis fossa, which could be also observed in the posterior
aspect, in the infraspinatus fossa. Osteophytes were also present on the lateral side of
acromion.
Discussion
The scapula constitutes embryologically a bone of the upper limb. During the fifth
week, mesenchyme migrates along central axis of the limb bud, originating from lateral
plate mesoderm, and its condensation results in the formation of mesenchymal bone
207
Suprascapular foramen: a case report and review
FIGURE 1
FIGURE 2
Figure 1 – Morphology of ossified superior transverse Figure 2 – Overview of the scapula with suprascapscapular ligament. Black line: ligament length; red line: ular foramen. Green line: distance between foramen
ligament width; yellow line: line of fusion between the and superior angle of the scapula.
ligament and the scapula on the medial site.
models. Chondrification occurs in
the sixth week. Ossification of hyaline cartilage models leads to bone
formation by endochondral ossification (Singh, 2012).
The suprascapular foramen is
formed normally by the suprascapular notch, which is converted into a
foramen by the superior transverse
scapular ligament which bridges the
borders of the notch. The suprascapular nerve, an important branch of
the brachial plexus, and the transverse scapular vein pass through the
foramen. The suprascapular artery
FIGURE 3
Figure 3 – Detail of suprascapular foramen with dispasses in general over the superior
tance from glenoid notch (blue line).
transverse scapular ligament (Moore
et al., 2014).
The different types of suprascapular notch were first described in 1979. The notch
can even be absent (Rengachary et al., 1979). In type VI, found in 4% of subjects, the
notch is converted into a bony foramen as the superior transverse scapular ligament
is completely ossified.
Our anatomical case is peculiar because the foraminal diameters were very small
in comparison with previously reported cases (Das et al., 2007; Polguj et al., 2014;
208
Stylianos Kapetanakis et alii
Table 1 – Previous reports on suprascapular bony foramen.
Authors
Vertical diameter
(mm)
Transverse diameter (mm)
Surface area
(mm2)
Tubbs et al. (2013)
No specific measurement information have been reported
Das et al. (2007)
12.00 (maximum)
8.00 (maximum)
Not reported
Polguj et al. (2014) (fan-shaped
superior transverse scapular
ligament)
7.15 (mean)
8.75 (mean)
50.75
Polguj et.al. (2014) (band-shaped
superior transverse scapular
ligament)
7.03 (mean)
5.35 (mean)
30.43
· 8.00 (maximum)
· 6.46 (mean)
3.88
24.36
Present case
Table 1). Even if our case belongs to fan-shaped type of superior transverse scapular ligament, the resulting foramen was even narrower than in cases of band-shaped
superior transverse scapular ligament (Polguj et al., 2014). A fan-shaped superior
transverse scapular ligament, as in this case, may therefore be a predisposing factor
for suprascapular nerve entrapment (a condition first described by Thomas, 1936)
because of the extremely narrow foramen from which the suprascapular nerve passes.
Ossification of superior transverse scapular ligament constitutes a cause of suprascapular nerve entrapment (Ticker et al., 1998, Osuagwu et al., 2000; Silva et al., 2007)
and the superior transverse scapular ligament peculiar shape or ossification should
be considered as predisposing factor for such entrapment (Bruce and Dorizas, 2013).
Other predisposing factors for suprascapular nerve entrapment are supraspinatus
fascia and hypertrophied subscapularis muscle (Duparc et al., 2010), double suprascapular foramen (Joy et al., 2015), anomalous position of suprascapular artery (Tubbs
et al., 2003) and presence of anterior coracoscapular ligament. The incidence of this
last condition was 60% in patients who suffered from suprascapular nerve entrapment in U.S.A. (Avery et al., 2002), 18,8% in Turkey (Bayramoğlu et al., 2003) and 28%
in Thai population (Piyawinijwong and Tantipoon, 2012).
Repeated overhead movements (Tubbs et al., 2003), such as volleyball (Witvrouw et
al., 2000) and overhead throwing sports (Seroyer et al., 2009) may lead to suprascapular nerve entrapment through the “sling effect”: during such movements the suprascapular nerve can be pressed on the sharp suprascapular notch border, causing, on
repetition, nerve irritation and eventually neuropathy (Rengachary et al., 1979).
The typical symptoms of suprascapular nerve entrapment include pain or weakness in the posterior and lateral part of shoulder and atrophy of supra- and infraspinatus muscles. However, the similarity of symptoms with other shoulder pathologies,
such as rotator cuff tears, make differential diagnosis difficult (Zehetgruber et al.,
2002). The treatment is in the beginning conservative, with physiotherapy directed at
strengthening rotator’s cuff musculature. In case of failure, surgical decompression is
recommended (Tubbs et al., 2003). In the case of a bony suprascapular foramen, special arthroscopic decompression can be proposed (Agrawal, 2009).
Suprascapular foramen: a case report and review
209
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IJA E
Vo l . 121, n . 2: 211-217, 2016
I TA L I A N J O U R N A L O F A N ATO M Y A N D EM B RYO LO G Y
Research article - History of anatomy and embryology
The good anatomist according to Jean Riolan Jr.
František Šimon1,*, Ján Danko2
1Department
of Classical Languages, Faculty of Arts, Pavol Jozef Šafárik University, and 2Institute of Anatomy,
Histology and Physiology, University of Veterinary Medicine and Pharmacology; Košice, Slovakia
Abstract
The important French anatomist Jean Riolan Jr. specifies in his work Anthropographia comprehensively for the first time in the history of anatomy several conditions which anatomy adepts
should fulfill during their preparation. Good anatomists should be prepared for their work
physically, mentally, culturally and ethically. The teacher of anatomy should abide by three
rules: have experience in anatomical dissection, possess the proper skills and correct approach
to dissection, and use an appropriate teaching method.
Key words
History of anatomy, Jean Riolan Jr.
Back in Antiquity the development of medicine induced several authors to discuss
the question of what makes a good physician. The short Hippocrates’ (430-350 BC)
treatise called The Law contains a brief summary of the requirements for an Ancient
Greek doctor (Hippocrates, edited 1998), and Galen (129-210 AD) wrote two pieces
on this subject: How to Recognise the Best Physician (Galen, edited 1988) and The Best
Physician is also a Philosopher (Galen, edited 1977). In the transition from Middle Ages
to Renaissance, Zerbi in the treatise De cautelis medicorum designed rules for a good
physician based on Hippocratic, Arabic and Christian authorities. However, only in
the Modern Age, when anatomy became a central point of medical education, specific reflections on the necessary qualities of an anatomist first appeared. The question „Who is a good anatomist“ was tackled by Berengario da Carpi (1460–1530) (da
Carpi, 1521; Bondio, 2010) and Vesalius (1514–1564) (Vesalius, 1543; French, 2003), but
the author who set out these requirements most comprehensively was the important
French anatomist Jean Riolan Jr. (1577/1580–1657). The father of this physician and
anatomist was himself a famous anatomist, and he himself was an influential member of the Faculty of Medicine in Paris and personal physician to the French queen
Maria de’ Medici. He was productive as an author of medical literature, a known
supporter of Galen (Siraisi, 2010), but he opposed Harvey’s theory of blood circulation (French, 1994) and Bartholin’s lymphatic system (Loukas et al., 2011). In the history of medicine he ranks among the anatomists who were called princeps anatomicorum, prince of anatomists, and he was addressed in this way also by his opponents,
* Corresponding author. E-mail: [email protected]
© 2016 Firenze University Press
ht tp://w w w.fupress.com/ijae
DOI: 10.13128/IJAE-18497
212
František Šimon, Ján Danko
who nonetheless respected him, e.g. William Harvey (1578–1657) (Harvey, 1649). Traces of him remain in anatomical terminology, in the form of several eponyms: anastomosis Riolani (joining of a. colica media and sinistra), musculus Riolani (m. cremaster), and
ossa Riolani (ossa suturarum) (Bartolucci and Forbis, 2005).
In one of his very first books Riolan tackles the issue of the various known ways
of learning anatomy, concluding that they are basically three: doctrina, theoretical education, inspectio, the method of visual observation, and operatio, the manual work of
dissection during autopsy. Doctrina is mediated through lectures and reading, but a
better way of learning is inspectio, because watching a dissection is better than trusting in books of anatomy. The third condition for perfect knowledge of anatomy,
however, is operatio, the autopsy itself, which must be performed by everyone who
intends to master anatomy, so as not to be dependent on other people’s eyes and
hands (Riolan, 1608).
These ideas are developed in more detail in Riolan’s most significant work on anatomy, Anthropographia, published in several successive editions. Referring back to Aristotle and Galen, in the introduction he divides medicine into the theoretical aspect aiming at gnósis, knowledge, and theória, theory, and the practical aspect aiming at chrésis,
usefulness, and praxis, practice. The former are learnt through the ears and eyes, that
is by means of lectures and reading, and the latter by means of manual work (Riolan,
1626). It is this, working with the hands, that the author emphasises, giving it a great
deal of space in his introduction. Up until mid 16th century the traditional way of performing an autopsy was that the professor, magister, read out and explained the theory,
the demonstrator identified and exhibited the body parts, and the third, the prosector,
did the dissection. Development in science brought change, however, and there was
increasing demand for anatomists to carry out these three activities themselves, i.e. the
dissection, demonstration and explanation (Mandressi, 2011). Riolan’s emphasis on the
necessity of performing autopsies accords with the opinions of several of his predecessors: Berengario da Carpi claimed that anatomy could not be learnt solely by means
of the voice (i.e. by listening) and the letter (i.e. by reading), but that it also required
sight and touch (visus et tactus) (da Carpi, 1521). Jacques Dubois (known as Jacobus Sylvius) (1478–1555), Vesalius’ teacher, wrote in his introduction to anatomy that autopsy
should be learnt through sight and touch (visu et tactu) rather than by listening and
reading (auditu et lectione) (Sylvius, 1560). In the introduction to his epochal work De
corporis humani fabrica, Andreas Vesalius in turn described the categorisation of specialists based on the traditional form of treatment they provided (change in life-style, prescription of medicines and surgical operations) as misguided, because the anatomical
description of a human being is the basis for the whole of medicine (Vesalius, 1543).
One chapter in Riolan’s work Anthropographia is called: Qualis esse debeat anatomiae studiosus, i.e. What should the student of anatomy be like? (Riolan, 1526). The
author specifies several conditions which anatomy adepts should fulfil during their
preparation:
1. Everyone who wants to know anatomy perfectly must be trained from an early
age; in Greek this was called paidomathia. This was maintained by the Ancient
Greek authorities Hippocrates and Galen themselves, who emphasised working with the hands. Older anatomists who avoided “anatomical work”, labor anatomicus, were quite happy with theory alone and overlooked the skills they had
learned when young, with the result that they undervalued and neglected this art.
The good anatomist
213
2. Anatomists must maintain their characteristic diligence, philoponia in Greek, and
good physical health, so that they can patiently bear all the difficulties and strain
which they have to deal with in anatomical work.
3. Anatomists must also be fearless, i.e. they must not be afraid of ghosts. Otherwise
they might suffer the same misfortune as a certain Phaylos, who the Greek author
Pausanias writes about in connection with the famous oracle at Delphi. Supposedly there was a metal skeleton set up there, a statue of a man made of bones and
without flesh, like a person who had died of some fatal wasting disease. It was
said that Hippocrates himself had donated the statue to the oracle. When Phaylos
saw it, he had a dream the following night in which he resembled the figure, and
shortly after that he really contracted a malignant disease and died (Pausanias X
2.6). Today we might understand this requirement in the sense that anatomists
must not be afraid that they might be affected by some supernatural force during
their anatomical work, i.e. they should not be prone to mental problems due to
the fact that they work with corpses.
4. The whole of the next passage is in fact a compilation of many quotations from
classical as well as modern age authorities, and Riolan appears here as an expert
in classical literature. The fundamental idea which he develops here is that in
anatomy, as in medicine generally, the most important thing is autopsy, seeing
with one’s own eyes. It is more advisable to trust in what one sees, rather than
hearing other people’s ideas or reading them in books. Aristotle however, in his
treatise On Breathing appears to give priority to reading rather than autopsy when
he says that the linkage between the heart and the lungs is studied with the eyes
during dissection, and then in detailed reading (Greek akribeia) of his work Historia animalium (On respiration XVI). This apparent contradiction is taken from the
commentary on Aristotle’s works by the well known Swiss polyhistorian Conrad
Gessner (1516–1565), and Riolan used Gessner’s interpretation as well: it must be
said that this description has not been passed down to us by just anyone, but by
trustworthy writers who had seen it not once, not twice, but more often and very
thoroughly (Gessner, 1586). In support of his opinion Riolan also quotes Galen,
who stated that anyone who wants to practise anatomy properly should believe
his own eyes rather than books (De usu partium II,3 : III,98 K).
5. The author goes on to emphasise that the human body must be viewed as a
whole. He cites Pliny Senior, according to whom the strength and magnitude of
Nature become less trustworthy if only parts of it are considered, and not the
whole (Naturalis historia VII,1,7).
6. Riolan is also against anatomical pictures, which he alleges to show only figures
of people and animals. He supports his claim by again citing Pliny Senior, who
says that a picture is deceptive (pictura fallax), especially as far as colours are concerned, and it shows only the surface, not the inside (Naturalis historia XXV,4).
So any iconica anatomia, or anatomy in pictures as Riolan calls it, can please and
impress uneducated people, but the same comment applies to them as Hippocratic author makes in his treatise Regimen: Many admire it, but few understand (De
diaeta I,24). Virgil takes a similar view of his Roman hero Aeneas, when he studies his shield: He admires it and, although he doesn’t understand it, he is pleased
by the pictures (Aeneis VIII,730). After further quotations from Roman authors
Lucilius and Martial, Galen and Aristotle again, and Modern Age anatomists
214
František Šimon, Ján Danko
André du Laurens (1558–1609) and Jacques Dubois, Riolan concludes by stating
that many anatomists fill their explanations with symbols, registers and lists of
their illstrations, but in his view that is an ineffective, unclear way of writing, and
it would be easier to decipher the codes of the Spartans, the inscriptions on the
statue of the Ephesian goddess Artemis or the stenography of Tyron, which were
all classical examples of incomprehensible texts. Illustrations were a relatively
new element in the anatomical literature, the first truly anatomic work with illustrations was the treatise Isagoge breves perlucide ac uberrime in anatomia[m] humani
corporis (1530) by Berengario da Carpi. He is appreciated for his efforts to integrate text and illustrations, although they were not of the best quality (O´Malley,
1964). Later illustrations from Vesalius´ De corporis humani fabrica have indeed
become famous for their quality and beauty (Nutton, 2003), nevertheless, the value of anatomical illustrations was not unanimously recognised. Riolan was one of
their opponents and he applied this attitude of his regarding illustrations of anatomical parts in his own work Anthropographia as well, which contains not a single picture. Riolan was no pioneer of this negative attitude to anatomical illustrations either, however, because his predecessor and countryman Jacques Dubois, in
dispute with his own student Vesalius, had already criticised anatomical pictures,
opining that they were purely for the amusement of women or the authors’ own
self presentation (Sylvius, 1548). Elsewhere he wrote that these pictures could be
puzzled out only with great difficulty (Sylvius, 1561). In time, though, Riolan’s
strict rejection of illustrations softened, because his later work Encheiridium anatomicum et pathologicum included 26 tables with illustrations and explanatory notes
(Riolan, 1649). Apparently we must understand Riolan’s attitude as a demonstrative rejection of the study of anatomy based exclusively on lower–quality illustrations in textbooks without the practical support of dissection.
7. Moreover, it is not sufficient to see the structure of the human body once or
twice, because we cannot know thoroughly anything which we have perceived
through our senses, unless we see it frequently enough. Even those who have
devoted their whole life to this art know to have erred in many cases, so what
can be expected of those who started studying anatomy today, yesterday, or just
the other day, and are convinced that something they have never seen before
must always be the same and they do not need to see it all over again? Riolan
cites Galen’s observation that there were many things he had previously overlooked, and which he only recognised on repeated dissection (Anat. admin.
VII,10 : II,621 K.).
8. The final requirement was the proper place to study, that is the correct choice of
school. The point was that not many schools provided good opportunities for
studying anatomy, because in Riolan’s time apart from in Paris, whether in the
rest of France, or in Italy, Spain or Germany, very few human dissections were
performed. In each year there was probably only one corpse available, and in
some places anatomy was even considered unsavoury and inhumane. In 1556 the
Spanish king and emperor Charles the Fifth asked the University of Salamanca to
confirm whether Christian physicians were permitted to dissect human corpses,
and he received the reply that for physicians it was both useful and necessary. The
University of Paris was fortunate in the sense that it had between ten and fifteen
corpses at its disposal every semester.
The good anatomist
215
In conclusion Riolan briefly summarises once again all the requirements which
Galen supposedly set up: paidomathia, filoponia, assiduitas, locus, exercitatio. It is not
possible to find one place in Galen’s works where these requirements are assembled with such brevity, but similar requirements for those who wish to learn the art
of medicine are contained in Hippocratic above-mentioned treatise The Law. These
read as follows: natura (inborn ability), doctrina (teaching), locus (suitable place), paidomathia (learning from childhood), filoponia, diligentia (endeavour, diligence), tempus
(appropriate time) (Hippocrates, 1998).
It is interesting that in Riolan’s reflections presented so far on what makes a good
anatomist, only “technical” requirements are considered, and no ethical content is
mentioned, in contrast to thoughts on a good physician. In the 1649 edition however,
Riolan adds precisely such content (Riolan, 1649). During dissection the anatomist
must treat the human body kindly and mercifully, thinking all the while that he too
is mortal and must soon die, and will then be a corpse himself, that “useless burden on the earth” as Homer puts it (Ilias XVIII,104). Moreover, he should not make
jokes about the poor wretch who was alive until just recently, and may not speak
shamelessly about the male or female genitals, which people are normally ashamed
of revealing, let alone make fun of them and use vulgar language to refer to them.
Finally the anatomist must carefully store away any pieces of muscle he removes to
prevent dogs or cats devouring them, and he must not throw entrails out with the
common refuse, but carefully gather everything away. When the dissection is completed, the remains of the corpse must be consigned to hallowed ground, accompanied by devout prayers and entreaties to God to preserve his soul and allow his body
upon the resurrection of the dead to enjoy eternal glory and bliss.
Whereas this chapter sets out the requirements which should be fulfilled in the
training of a good anatomist, the next chapter named Conditiones doctoris anatomici,
dealing with the qualities or rules for the doctor, i.e. teacher, of anatomy, consists of
unsystematically presented thoughts which are more or less just developments on the
preceding part. It contains a large number of quotations from the literature of antiquity as well as the Modern Age, and ends with a summary of three rules which the
teacher of anatomy should abide by: peritia, having experience in anatomical dissection, encheirisis, having the proper skills and correct approach to dissection, and optima methodus, using an appropriate teaching method (Riolan, 1626).
In conclusion we can state that for the first time in the history of anatomy, Riolan’s works provide a comprehensive overview of what is required of good anatomists. The requirements are that they should be prepared for their work physically,
mentally, expertly and ethically. Most of his rules for the good anatomist belong to
the commonplace of medical ethics (diligence, good physical health, education,
behaviour towards the patients), but Riolan updated them specifically for anatomy.
Similarly as in other examples from the history of medicine, these principles can still
serve well as inspiration for today’s and future anatomists.
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Gabrielle A. Fornazari, Fabiano Montiani-Ferreira, Jeverson C. Silva, Ivan R. Barros,
Marcello Z. Machado
The patellofemoral joint alignment in patients with symptomatic accessory
navicular bone
Heba M. Kalbouneh, Abdullah O. Alkhawaldah, Omar A. Alajoulin, Mohammad I.
Alsalem
15
20
30
Caspar Bauhin (1560-1624): Swiss anatomist and reformer of anatomical nomenclature 41
Sanjib Kumar Ghosh
Morphometric study of variations of sacral hiatus among West Bengal population
and clinical implications
Dona Saha, Santanu Bhattacharya, Akhtar Uzzaman, Sibani Mazumdar, Ardhendu
Mazumdar
Abnormal branching of the axillary artery: an axillo-hepatic artery
Pranit N Chotai, Marios Loukas, R. Shane Tubbs
47
54
An anatomic variant causing a previously unreported complication of
transcutaneous treatment of trigeminal neuralgia
R. Shane Tubbs, Kimberly P. Kicielinski, Joel Curé, Benjamin J. Ditty, Barton L.
Guithrie
Unilateral duplication of parotid duct – a rare cadaveric case report
Sumathi Shanmugam, Nithiyapriya Raju, Kalaiyarasi Subbiah, Sivakami Thiagarajan
61
66
A rare anomaly of the human spleen with nine notches associated with multiple
accessory spleens. A case study, hypothesis on origin and review of clinical significance 70
Thanya I. Pathirana, Matthew J. Barton, Mark George, Mark R. Forwood, Sujeewa
P.W. Palagama
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