Download Development of the human knee joint

THE ANATOMICAL RECORD 248:269–278 (1997)
Development of the Human Knee Joint
JUAN A. MÉRIDA-VELASCO,1* INDALECIO SÁNCHEZ-MONTESINOS,1
JOAQUÍN ESPÍN-FERRA,1 JOSÉ F. RODRÍGUEZ-VÁZQUEZ,2
JOSÉ R. MÉRIDA-VELASCO,2 AND JUAN JIMÉNEZ-COLLADO2
1Human and Experimental Embryology Research Group, Department of Morphological
Sciences, University of Granada, E-18071 Granada, Spain
2Department of Morphological Sciences II, University Complutense of Madrid,
Madrid, Spain
ABSTRACT
Background: Many studies have been published on the
development of the human knee joint, but different investigators disagree
on its morphogenetic time table. Most discrepancies center on the cavitation of the knee joint and the participation of the superior tibiofibular
joint in the joint knee system.
Methods: We summarize our observations of the development of the knee
joint in 50 serially sectioned human embryonic and fetal lower limbs (26
embryos and 24 fetuses).
Results: The epiphysis of the femur and tibia become condryfied from
O’Rahilly stage 18, and ossification begins during the 13th week of
development. The patella appears as a dense blastema during O’Rahilly
stage 19, becomes condryfied during O’Rahilly stage 22, and begins its
ossification during the 14th week of development. The knee joint cavity
appears during O’Rahilly stage 22, initially as the femoropatellar joint.
This process begins at the periphery of the articular interzone. The
superior tibiofibular joint communicates with the lateral meniscotibial
joint between 10 and 11 weeks of development and becomes separated
from the 13 week on. The menisci arise from the eccentric portions of the
articular interzone during O’Rahilly stage 22; however, until week 9 of
development, they are not easily distinguishable.
Conclusions: We establish the morphogenetic time table of the human
knee joint. Anat. Rec. 248:269–278, 1997. r 1997 Wiley-Liss, Inc.
Key words: articular interzone; superior tibiofibular joint; meniscus; development; human
During recent decades, a wealth of information about
the development of bones and joints has been published
(Bernays, 1878; Hagen-Torn, 1882; Bardeen, 1907;
Walmsley, 1940; Whillis, 1940; Haines, 1947, 1953;
Gray and Gardner, 1950; Gardner and O’Rahilly, 1968;
among others). More attention has been given to the
development of the knee joint than to any other joint.
This intense interest must be seen in the light of the
size of this joint and of its complexity and clinical
importance. The elements that have received the most
attention are the cavitation of the knee joint and the
role of the head of the fibula in the formation of the knee
joint system. The first signs of cavitation of the knee
joint are seen in peripheral areas (Gray and Gardner,
1950; O’Rahilly, 1952; Palacios and Rhode, 1980; Cáceres and Caja, 1980) or near the center (Andersen, 1961;
Andersen and Bro-Rasmussen, 1961) of the medial
layer of the articular interzone; however, Mitrovic
(1978) believed the process to take play simultaneously
in central and peripheral areas. This process is initially
detectable in the femoropatellar interzone (Lucien,
1904; Walmsley, 1940; Gray and Gardner, 1950) and
r 1997 WILEY-LISS, INC.
appears immediately thereafter in the femoromeniscal
interzone.
The role of the head of the fibula in the formation of
the knee joint has been widely debated. The superior
tibiofibular interzone appears during O’Rahilly stage
22 (Gray and Gardner, 1950; Haines, 1952, 1953;
Andersen, 1961; Palacios and Rhode, 1980); nevertheless, McDermott (1943) reported that the superior
tibiofibular interzone is not yet clearly established
during weeks 8 and 9. The cavitation of the superior
tibiofibular joint becomes evident during week 10
(Andersen, 1961), in 60-mm specimens (Gray and Gardner, 1950), or during week 15 of development (Palacios
and Rhode, 1980). A clear communication forms between the superior tibiofibular and lateral meniscotibial articular cavities during weeks 9.5 (Keith, 1933;
Gray and Gardner, 1950) or 10 and 11 of development
*Correspondence to: Juan A. Mérida-Velasco, Departamento de
Ciencias Morfológicas, Facultad de Medicina, Avda. de Madrid 11,
E-18071 Granada, España.
Received 23 July 1996; accepted 11 December 1996.
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J.A. MÉRIDA-VELASCO ET AL.
TABLE 1. Features of the specimens used
Embryos’
C-R length
(mm)
X-12
GG-1
BE-1
BB-5
E-19
JD-7
PT-9
JD-2
R-1
MA-7
X-6
PE-8
HA-2
CH-1
X-14
EA-3
BB-4
GV-4
HE-1
FA-5
NA-1
RI-4
X-18
BB-2
H-23
X-4
15
17
17
18
19
19
20
20
21
22
22.5
23
23
24
24
24.5
26
27
28
28
29
29
30
30
31
31
Plane of
section
O’Rahilly
stage
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Sagittal
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
18
18
19
19
20
20
20
20
21
21
21
22
22
22
22
22
22
22
23
23
23
23
23
23
23
23
(McDermott, 1943; O’Rahilly, 1951; Olivier, 1965). However, Gray and Gardner (1950), Haines (1953), Andersen
(1961), Palacios and Rhode (1980), Cáceres and Caja
(1980) found no evidence that the head of the fibula is
involved in the formation of the knee joint during
development. These studies are now especially pertinent because of the increasing interest in congenital
anomalies of the skeleton. The purpose of this study
was to analyze the development and establish the
morphogenetic time table of the knee joint.
MATERIALS AND METHODS
Fifty human embryos and fetuses from the embryo
collections of the Department of Morphological Sciences
of the universities of Granada and Madrid (Universidad Complutense) were used in the present study.
Crown–rump (C-R) length, plane of section, and stage
of development (O’Rahilly and Müller, 1987) are shown
in Table 1. The usual laboratory procedures were used
to prepare 10–15-µm-thick transverse or sagittal serial
Abbreviations
F
L
P
T
=
1
2
3
4
5
6
7
8
9
lower epiphysis of the femur
cruciate ligaments
patella
upper epiphysis of the tibia
cartilage canal
interzone of the knee joint
interzone of the superior tibiofibular joint
menisci
articular capsule
condylopatellar ligaments
femoropatellar joint cavity
femoromeniscal joint cavity
meniscotibial joint cavity
superior tibiofibular joint cavity
Fetuses’ C-R
length (mm)
CA-1
RI-1
H-19
BB-1
GV-3
AM-1
PE-7
ZO-1
SA-1
GV-1
MA-3
SA-3
X-8
MA-2
MA-1
X-11
BB-3
H-4
SA-4
PE-3
JM-1
OL-1
ZO-2
BU
35
38
39
39
41
41
41
42
44
45
46
48
50
50
52
53
53
62
63
70.5
80
83
102
113
Plane of
section
Weeks of
development
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Sagittal
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Transverse
Sagittal
Transverse
9
9
9
9
10
10
10
10
10
10
10
10
11
11
11
11
11
12
12
12
13
13
14
14
sections, which were stained with hematoxylin–eosin
(McManus and Mowry, 1968) for light microscopic
study.
RESULTS
O’Rahilly Stages 18 and 19
During O’Rahilly stage 18, chondrification began at
the lower portion of the femur and upper part of the
tibia (Fig. 1A). An articular interzone, consisting of a
single band of mesenchymal tissue, formed between
these two areas (Fig. 1A).
At the end of O’Rahilly stage 19, a condensation of
mesenchyme representing the future patella became
visible ventral and cranial to the condyles of the femur
(Fig. 1B).
O’Rahilly Stages 20 and 21
Chondrification continued at the lower end of the
femur and upper part of the tibia. The femoral condyles
Fig. 1. A: Human embryo GG-1. The epiphysis of the femur (F) and
tibia (T) begin their condryfication. Between them is the articular
interzone of the knee (1). Note that the interzone consists of an
unlayered dense mesenchyme. B: Human embryo BB-5. The articular
interzone of the knee (1), as an unlayered dense mesenchyme, is
located between the epiphysis of the femur (F) and tibia (T). Ventrally
to the femur, the organization of the patella (P) begins as a dense
blastema. C: Human embryo MA-7. Condryfication of the epiphysis of
the femur (F) and tibia (T) continue, and the first signs of organization
of the femoral and tibial condyles are observed. Between these, the
articular interzone of the knee (1) begins to form as a three-layered
structure. D: Human embryo CH-1. The articular interzone of the
knee (1) appears as a three-layered structure. Two dense eccentric
layers lean against the condyles of the femur (F) and tibia (T) and
represent the future articular cartilage. Between these layers is a lax
medial layer. Bars 100 µm in A,B, 200 µm in C, 50 µm in D.
Fig. 1.
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J.A. MÉRIDA-VELASCO ET AL.
and upper surface of the tibia began to be distinguishable (Fig. 1C).
The articular interzone of the knee was formed of two
eccentric bands of mesenchymal tissue that covered the
condyles of the femur and upper surface of the tibia
(Fig. 1C) and a medial band that began to appear more
lax in comparison with the eccentric layers (Fig. 1C).
O’Rahilly Stage 22
The eccentric bands of the interzone followed the
shape of the femoral and tibial condyles, forming a
dense band of perichondrial connective tissue (Fig. 1D)
that marked the first sign of organization of the articular cartilage. At the same time, the medial layer of the
interzone appeared more lax than the eccentric layers
(Fig. 1D). The lateral parts of the interzone became
densified and began to form the menisci (Fig. 2A). The
joint capsule began to attach peripherally to the menisci (Fig. 2A & 2B).
The medial layer of the interzone appeared lax.
Laterally, at the level of the medial layer, small cavities
began to appear between the meniscus and the lateral
condyles of the femur and tibia. These cavities were
crossed by conjunctive tissue septae (Fig. 2B).
Chondrification of the patella began, as did cavitation
of the femoropatellar interzone (Fig. 2C).
On the upper surface of the tibia, the intercondylar
eminence began to form, and immediately dorsal to
this, the tibial insertion of the posterior cruciate ligament appeared (Fig. 2C).
In the superior tibiofibular interzone, no sign of
cavitation was apparent (Fig. 2D).
O’Rahilly Stage 23
The articular capsule was visible, and densification of
the condylopatellar ligaments was evident (Fig. 3A).
From the lateral margins of the patella, the articular
capsule surrounded the femoral condyles (Fig. 3A) and
became attached to the eccentric surface of the menisci
(Fig. 3B).
The femoropatellar (Fig. 3A), femoromeniscal, and
meniscotibial joint cavities (Fig. 3A & 3B) were distinguishable. The interzone of the superior tibiofibular
joint was visible but showed no signs of cavitation (Fig.
3C).
Week 9
Development of the menisci proceeded, giving rise to
the femoromeniscal and meniscotibial joint cavities
(Fig. 3D & 3E), in which a few tracts of connective
tissue were still visible.
The patella lay opposite of, and was articulated
mainly with, the lateral condyle. The triangular space
with an anterior base that formed below the patella was
occupied by mesenchymal tissue, which may represent
the first sign of formation of the fat pad (Fig. 3D).
Peripherally, the menisci were attached by the coronary ligaments to the capsule (Fig. 3E).
Weeks 10 and 11
The degree of development of the knee joint at this
time was similar to that seen during week 9, with slight
modifications.
The superior tibiofibular joint cavity first appeared,
and a connection between this cavity and the lateral
meniscotibial cavity was visible (Fig. 4A).
Development of the medial meniscus continued and
brought about the organization of the internal femoromeniscal and meniscotibial joints (Fig. 4B). The anterior horn of the medial meniscus was attached to the
anterior aspect of the upper surface of the tibia (Fig. 4B).
The lateral meniscus was clearly evident, and its
formation brought about the organization of the lateral
femoromeniscal and meniscotibial joints (Fig. 4C).
Weeks 12 and 13
The knee joint cavity attained its adult appearance
during this time, when the communication between the
lateral meniscotibial and superior tibiofibular cavities
disappeared.
During week 13, ossification began in the epiphyses
of the elements comprising the knee joint and first
became apparent in the lower epiphysis of the femur
and upper epiphysis of the tibia (Fig. 5A & 5B).
Cartilage canals invaded the perichondrial zone of the
condyles and penetrated from superficial to deep areas
(Fig. 5A & 5B). In the femur, these canals penetrated
preferentially from the margins and deep portion of the
intercondylar notch of the femur (Fig. 5A). In the tibia,
they penetrated preferentially from the anterior and
superior margins (Fig. 5B). The invading vessels came
from the pericapsular arterial network, which in turn
was dependent on the genus arteries.
Week 14
Ossification of the patella began, with cartilage canals penetrating from the anterior and superior surface
(Fig. 5C).
DISCUSSION
The elements that constitute the knee joint begin to
chondrify during O’Rahilly stage 18 (Gardner and
O’Rahilly, 1968; Cáceres and Caja, 1980; Palacios and
Rhode, 1980; Clark and Odgen, 1983), when the apposed ends of the femur and tibia are covered with a
dense layer of perichondrium. However, Andersen (1961)
noted that in 20-mm embryos, ‘‘the distal end of the
femur as well as the proximal end of the tibia and fibula
still persist as a dense blastemal precartilage.’’ McDermott (1943) reported that chondrification of the femur
and the tibia began on days 47–51 of development, and
O’Rahilly (1952) first observed chondrification during
stage 27. O’Rahilly et al. (1956) reported chondrification of the femur and tibia in a few O’Rahilly stage-17
embryos, whereas Haines (1953) found that this process was first evident in the knees of 13-mm embryos.
The patella first becomes visible at the end of
O’Rahilly stage 19 (Bardeen, 1907; Gardner and
O’Rahilly, 1968). Some investigators have reported that
it makes its first appearance later, when the embryo
has reached 20 mm (Walmsley, 1940; Haines, 1947), 23
mm (Andersen, 1961), 24.5 mm (Caja and Cáceres
1980), 42 mm (Eberl-Rothe and Sonnenschein, 1950), or
7.5 weeks of development (Gray and Gardner, 1950).
According to Gardner and O’Rahilly (1968), the patella
begins to undergo chondrification during O’Rahilly
stage 22, although they also noted that in four of the
HUMAN KNEE JOINT
Fig. 2. A: Human embryo PE-8. The lateral portions of the articular
interzone of the knee form the menisci (3) that are located between the
condyles of the femur (F) and tibia (T). The knee joint capsule (4) is
attached to the eccentric margin of the menisci. B: Human embryo
PE-8. Formation of the meniscofemoral (7) and meniscotibial (8) knee
joint cavities has begun. Both cavities are crossed, at this time, by
mesenchymal trabeculae. Knee joint capsule (4) is attached to the
273
eccentric margin of the menisci. C: Human embryo PE-8. condryfication of the patella (P) and the organization of the femoropatellar cavity
(6) have begun. The posterior cruciate ligament (L) is observed in the
medial layer of the knee joint interzone (1). D: Human embryo EA-3.
The articular interzone of the superior tibiofibular joint (2) is observed. At this time, no sign of cavitation is evident. Bars 200 µm in
A,C,D, 100 µm in B.
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J.A. MÉRIDA-VELASCO ET AL.
Fig. 3.
HUMAN KNEE JOINT
specimens they examined, signs of chondrification were
evident during O’Rahilly stage 21. Walmsley (1940)
reported the earliest signs of chondrification in 30-mm
embryos, whereas McDermott (1943) distinguished this
phenomenon during fetal development at 9 and 10
weeks.
The epiphysis of the femur and tibia begin to ossify
during week 13, and in the patella, ossification begins
during week 14. However, Gray and Gardner (1950)
and Palacios and Rhode (1980) found signs of the
formation of cartilage canals in the knee in 12-week-old
fetuses. The vessels penetrated from superficial to deep
levels after invading the perichondrial zone of the
condyle. In the lower epiphysis of the femur, vessels
invaded from the margins and the deep portion of the
intercondylar notch, and in the upper epiphysis of the
tibia, invasion proceeded from its anterior and superior
part surfaces (Palacios and Rhode, 1980). In the patella, vessels penetrated from the superior and anterior
margins (Kreutz and Kreutz, 1981; Doskocil, 1985) and
not from the inferomedial margin of the kneecap, as
noted by Palacios and Rhode (1980).
Formation of the capsule of the knee joint begins
during O’Rahilly stage 22. According to Archer et al.
(1994), hyaluronan appears to play a central role in this
process. However, in one of the O’Rahilly stage-23
embryos studied by Gardner and O’Rahilly (1968),
there was no evidence of the joint capsule in the knee;
and in another stage-23 embryo, one of the knees
showed signs of incipient cavitation near the femur and
patella. In material studied by Bardeen (1907), Gray
and Gardner (1950), and O’Rahilly and Gardner (1975),
cavitation began during O’Rahilly stage 23; however,
Walmsley (1940), Haines (1947), Moll (1948), and Palacios and Rhode (1980) first observed this process at 9
weeks of development, and Dubinkin and Motnenko
(1931) noted this process in 11.8-cm fetuses.
The first signs of cavitation of the knee joint are seen
in peripheral areas of the medial layer of the articular
interzone (Gray and Gardner, 1950; O’Rahilly, 1952;
Cáceres and Caja, 1980; Palacios and Rhode, 1980).
This process is initially detectable in the femoropatellar
interzone (Lucien, 1904; Walmsley, 1940; Gray and
Gardner, 1950) and appears immediately thereafter in
the femoromeniscal interzone. However, Andersen and
Bro-Rasmussen (1961) and Andersen (1961) reported
that cavitation began near the center of the interzone
and spread toward the periphery, whereas (Mitrovic,
1978) believed the process to take play simultaneously
Fig. 3. A: Human embryo X-4. The femoropatellar (6) and meniscofemoral (7) cavities are observed. The knee joint capsule (4), attached
to the eccentric margin of the menisci (3), is strengtened by the
condylopatellar ligaments (5). B: Human embryo NA-1. The meniscofemoral (7) and meniscotibial (8) cavities are clearly distinguishable.
In the middle of the knee joint, organization of the cruciate ligaments
(L) continues. Knee joint capsule (4). C: Human embryo HE-1. At the
level of the superior tibiofibular joint (2), a three-layered interzone is
present; hence, no sign of articular cavitation is evident. D: Human
fetus RI-1. The patella (P) is basically articulated with the lateral
condyle of the femur (F). Below the patella, a triangular space forms.
This space is occupied by a mesenchymal tissue that gives rise to the
intraarticular pad of fat. Lateral meniscus (3). E: Human fetus RI-1.
Enlargement of D. Observe the knee joint capsule (4) attached to the
eccentric margin of the menisci (3), which organize the coronary
ligament. The femoromeniscal (7) and meniscotibial (8) cavities are
clearly distinguishable. Bars 200 µm in A–D, 100 µm in E.
275
in central and peripheral areas, although this author
noted that cavitation was more advanced at the periphery.
The role of the head of the fibula in the formation of
the knee joint has been widely debated. In our material,
we observed the appearance of a superior tibiofibular
interzone during O’Rahilly stage 22 (Gray and Gardner,
1950; Haines, 1952, 1953; Andersen, 1961; Palacios and
Rhode, 1980). Nevertheless, McDermott (1943) reported that the superior tibiofibular interzone was not
yet clearly established in weeks 8 and 9. We also found
that cavitation of the superior tibiofibular joint became
evident during week 10 (Andersen, 1961) and not in
60-mm specimens (Gray and Gardner, 1950) or during
week 15 of development (Palacios and Rhode, 1980). A
clear communication forms between the superior tibiofibular and lateral meniscotibial joint cavities during
weeks 10 and 11 (McDermott, 1943; O’Rahilly, 1951;
Olivier, 1965). This space was also seen by Keith (1933)
and Gray and Gardner (1950) in a 9.5-week fetus.
However, Gray and Gardner (1950), Haines (1953),
Andersen (1961), Palacios and Rhode (1980), and Cáceres and Caja (1980) found no evidence that the head of
the fibula was involved in the formation of the knee
joint during development, and Gray and Gardner (1950)
reported that in most cases the knee joint cavity was
separated from the superior tibiofibular joint cavity by
either a small amount of very loose tissue or very thin
strands of somewhat denser tissue. O’Rahilly (1951)
described a femorofibular interzone in embryos of 16–20
mm, although in our material no such interzone was
visible.
Discrepancies also exist with regard to the final
organization of joint cavity, considered to arise from the
confluence of five initially separate cavities: the femoropatellar, two femoromeniscal, and two meniscotibial
cavities (McDermott, 1943; Gray and Gardner, 1950;
Palacios and Rhode, 1980). However, one investigator
considered only three cavities to be involved, i.e., the
femoropatellar and two femorotibial cavities (Andersen,
1961), and another investigator (Doskocil, 1985) reported that only two symmetrical cavities initially
separated by a medial mediastinum were involved. Our
observations show that initially a femoropatellar cavity
and two femoromeniscal cavities exist and that subsequently two meniscotibial cavities are formed. Nonetheless, a sixth space, the superior tibiofibular cavity, is in
communication with the meniscotibial cavity during
weeks 10 and 11 of development and thus forms part, at
least temporarily, of the developing knee joint cavity.
The formation of a single cavity, with the disappearance
of communication with the superior tibiofibular cavity,
takes place during weeks 12 and 13 of development
according to Palacios and Rhode (1980) and during the
eighth week according to Keith (1933).
Organization of the menisci begins during O’Rahilly
stage 22 (Haines, 1947; Andersen, 1961; Gardner and
O’Rahilly, 1968; Cáceres and Caja, 1980; Clark and
Odgen, 1983), although Gardner and O’Rahilly (1968)
observed the lateral meniscus in one of the nine
O’Rahilly stage-20 specimens they studied. The menisci
cannot be distinguished clearly until week 9 (Gray and
Gardner, 1950; Palacios and Rhode, 1980); however,
some investigators have reported that they form at
later stages, i.e., week 8 (Palacios and Rhode (1980),
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J.A. MÉRIDA-VELASCO ET AL.
Fig. 4. A: Human fetus GV-1. The superior tibiofibular
joint cavity (9) shows its communication with the lateral
meniscotibial joint cavity (8). Lateral meniscus (3).
Posterior cruciate ligament (L). B: Human fetus GV-1.
The medial meniscus (3) is completely formed, and the
medial meniscofemoral (7) and meniscotibial (8) joint
cavities are established. The anterior horn of the medial
meniscus is attached to the anterior aspect of the upper
surface of the tibia. Anterior cruciate ligament (L). C:
Human fetus BB-3. The lateral meniscus (3) is completely organized, and the lateral meniscofemoral (7)
and meniscotibial (8) joint cavities are established.
Observe the communication between the superior tibiofibular (9) and the lateral meniscotibial (8) joint cavities.
Bars 5 200 µm.
HUMAN KNEE JOINT
277
Fig. 5. A: Human fetus OL-1. Cartilage canal (arrow)
penetrates the lower end of the femur at the level of its
posterior surface. B: Human fetus OL-1. Cartilage canals (arrow) penetrate the upper end of the tibia.
Ossification begins on the superior and anterior surfaces
of the tibia. The anterior horn of the lateral meniscus (3)
is also distinguishable. C: Human fetus ZO-2. Cartilage
canals (arrow) penetrate the superior and anterior surface of the patella (P). Bars 100 µm in A,B, 200 µm in C.
278
J.A. MÉRIDA-VELASCO ET AL.
weeks 9 and 10 (McDermott, 1943), or even as late as in
the 3.5-month fetus (Dubinkin and Motnenko, 1931).
The joint capsule is attached to the anterior margin
of the external meniscus during O’Rahilly stage 22 and
to the eccentric surface of both menisci during O’Rahilly
stage 23. According to McDermott (1943) and Gray and
Gardner (1950), this final attachment does not take
place until week 12 of development. During week 10 of
development, the horns of the menisci clearly become
attached to the anterior and posterior aspects of the
upper surface of the tibia.
ACKNOWLEDGMENTS
We thank Ms. Karen Shashok for translating the
original manuscript into English.
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