Download nipple innervation

The Sensitivity of the Nipple-Areola Complex:
An Anatomic Study
Ingrid Schlenz, M.D., Rafic Kuzbari, M.D., Helmut Gruber, M.D., and Jürgen Holle, M.D.
Vienna, Austria
far, the 2nd, 3rd, 4th, and 5th1 or the 2nd, 3rd,
4th, 5th, and 6th2 or the 3rd, 4th, and 5th3–5 or
the 4th, 5th, and 6th6,7 or only the 4th8 –12 intercostal nerves have been described as supplying nerves to the nipple and areola. The 4th
lateral cutaneous branch is unanimously regarded as the most important nerve for the
sensitivity of the nipple; however, its course
from the point where it perforates the deep
fascia in the midaxillary line to the nipple has
been described controversially. Some authors
describe it as “passing deeply through the
breast tissue,”3,5,9,11 some describe a more superficial course close to the skin,1,2,4,8 and others do not give any details about its course at
all.6,7,12
These controversial reports might be due to
the difficulty in dissecting the thin nerves and
to frequent anatomic variations that bias the
results if the investigation is carried out only in
a small number of cadavers. We undertook this
anatomic study to clarify these controversial
reports and to enable the preservation of the
sensitivity of the nipple and areola during
breast surgery.
Although preservation of the sensitivity of the nipple
and areola is an important goal in breast surgery, only
scant and contradictory information about the course and
distribution of the supplying nerves is found in the literature. The existing controversy might be due to the difficulty in dissecting the thin nerves and to frequent anatomic variations that bias the results if only a small number
of cadavers are dissected. We dissected 28 female cadavers
and found that the nipple and areola were always innervated by the lateral and anterior cutaneous branches of
the 3rd, 4th, and 5th intercostal nerves. The most constant
innervation pattern was by the 4th lateral cutaneous
branch (79 percent) and by the 3rd and 4th anterior
cutaneous branches (57 percent). The anterior cutaneous
branches took a superficial course within the subcutaneous tissue and terminated at the medial areolar border in
all dissected breasts. The lateral cutaneous branches took
a deep course within the pectoral fascia and reached the
nipple from its posterior surface in 93 percent of the
dissected breasts. In 7 percent of the dissected breasts, the
lateral cutaneous branches took a superficial course
within the subcutaneous fat and reached the nipple from
the lateral side. These findings suggest that the nerves
innervating the nipple and areola are best protected if
resections at the base of the breast and skin incisions at the
medial areolar border are avoided. (Plast. Reconstr. Surg.
105: 905, 2000.)
Preservation of the sensitivity of the nipple
and areola is an important goal in breast surgery. Yet, only scant and contradictory information about the course and distribution of the
supplying nerves is available in the literature.
Although most authors agree that the nipple
and areola are innervated by the lateral and
anterior cutaneous branches of the intercostal
nerves, there is a controversy about which intercostal nerves are involved and which course
they take through the breast parenchyma. So
MATERIALS
AND
METHODS
Breast specimens of 28 female Caucasian cadavers were examined. Twenty-six cadavers had
been embalmed with a mixture of 10% phenol/formaldehyde for 6 weeks before dissection; 2 cadavers were dissected 6 hours postmortem. As the course and distribution of the
nerves innervating the nipple-areola complex
seem to vary between different individuals1–12
From the Department of Plastic and Reconstructive Surgery at the Wilhelminenspital. Received for publication April 26, 1999; revised August
9, 1999.
Presented at the 35th Annual Meeting of the Austrian Society of Plastic, Reconstructive and Aesthetic Surgery in Innsbruck-Igls, Austria, in
October of 1997; at the 9th Annual Meeting of the European Association of Plastic Surgeons in Verona, Italy, in May of 1998; and at the 12th
Congress of the International Confederation for Plastic, Reconstructive and Aesthetic Surgery, in San Francisco, California, in June of 1999.
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PLASTIC AND RECONSTRUCTIVE SURGERY,
and only rarely between the left and right side
in the same individual,1 only one breast per
cadaver was examined; the left breast was dissected in 24 cadavers, the right breast in 4
cadavers. The right breast was only used when
a scar or a hematoma indicated prior surgery
of the left breast. The skin was elevated in an
area from the clavicle to 3 cm below the inframammary fold from the sternum to the medial
rim of the areola and from the midaxillary line
to the lateral rim of the areola. Then, the
anterior and lateral cutaneous branches of the
2nd, 3rd, 4th, 5th, and 6th intercostal nerves
were identified at the points where they perforated the chest wall in the parasternal and
midaxillary lines, respectively. The nerves were
dissected with magnifying loupes and traced
until they entered the nipple or the areola or
until they terminated on the surface of the
subcutaneous tissue of the breast. In the two
fresh cadavers, specimens of the nerves supplying the nipple or areola were taken 1 cm proximal to their entry into the skin of the nipple or
areola. These specimens were preserved in
2.5% cacodylate buffer, embedded in epoxy
resin, and cut with a microtome. Then, the
specimens were examined microscopically; the
fascicles were counted, and their diameters
were measured.
RESULTS
We found that in all cadavers the nipple and
areola were innervated by both the anterior
and lateral cutaneous branches of the 3rd, 4th,
or 5th intercostal nerves (Table I). The anterior and lateral cutaneous branches of the 2nd
and 6th intercostal nerves innervated breast
skin only. The diameter of the lateral cutaneous branches was always bigger than the diameter of the anterior cutaneous branches (m ⫽
100 ⫾ 10 ␮m versus m ⫽ 20 ⫾ 5 ␮m). In 93
percent of the dissected breasts, the lateral
cutaneous nerves pierced the deep fascia in the
midaxillary line and took an inferomedial
course within the pectoral fascia or the pectoral muscle (one breast). On reaching the midclavicular line, they turned for almost 90 degrees and continued through the glandular
tissue toward the posterior surface of the nipple, which they entered with several tiny
branches (Figs. 1 and 2). In 7 percent of the
breasts, the lateral cutaneous nerves took a
superficial course. They ran in the subcutaneous tissue close to the skin and reached the
nipple from the lateral side. This course was
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TABLE I
Innervation of the Nipple and Areola
ACB*
Number of
Cadavers
Side
III
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
L
R
R
L
L
L
L
L
L
R
L
L
L
L
L
L
R
L
L
L
L
L
L
L
L
L
L
L
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
IV
LCB
V
III
xA
xN
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xA
xN
xA
xA
xA
IV
xN
xN
xN
xN
xN
xN
xN
xN
xN
xN
xN
xN
xN
xN
xN
xN*
xN*
xN
xN
xN
xN
xN
xN
xN
xA
V
xN
xN
xN
xN
xN
xN
ACB, anterior cutaneous branch of the intercostal nerve III, IV, V. LCB,
lateral cutaneous branch of the intercostal nerve III, IV, V. A, areola. N, nipple.
* Superficial course of the nerve.
similar to that of a constant cutaneous branch
that terminated in the lateral breast skin after
separating from the main stem of the 4th lateral cutaneous branch at the edge of the pectoral muscle (Figs. 1 and 2).
The 4th lateral cutaneous branch supplied
the nipple in 93 percent of the dissected
breasts; in 79 percent it was the only lateral
supply to the nipple. The 3rd and 5th lateral
cutaneous branches were found to innervate
the nipple alone in 3.6 percent and together
with the 4th lateral cutaneous nerve in 7.1
percent of the dissected breasts (Table I).
When multiple innervation was present, the
diameter of the individual nerves was markedly
smaller than in those cases where only one
supplying nerve was present. In two breasts (7.1
percent), the two lateral cutaneous branches of
the 3rd and 4th intercostal nerves formed an
anastomosis lateral to the border of the pectoral muscle and supplied the nipple with the
resulting single nerve branch. In one breast,
the 4th lateral cutaneous branch separated
into two smaller branches shortly after giving
off the cutaneous branch to the skin. The two
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SENSITIVITY OF THE NIPPLE-AREOLA COMPLEX
FIG. 1. Lateral view of a left breast. Double arrow, lateral
cutaneous branch of the 4th intercostal nerve reaching the
posterior surface of the nipple; arrow, cutaneous branch of
the lateral cutaneous branch terminating in the skin of the
lower lateral quadrant.
smaller branches took a parallel course and
reached the posterior surface of the nipple
within 5 mm of each other.
The anterior cutaneous branches contributed to the medial innervation of the nippleareola complex. After piercing the fascia in the
parasternal line, they divided into a lateral and
a medial branch. Whereas the medial branch
crossed the lateral border of the sternum, the
lateral branch divided again into several
smaller branches that took an inferolateral
course through the subcutaneous tissue. They
became progressively more superficial along
their way and terminated in the breast skin or
at the areolar edge. The branches that terminated at the areolar edge originated from the
3rd, 4th, or 5th intercostal nerves; they always
reached the areolar edge between 8 and 11
o’clock in the left breast and between 1 and 4
o’clock in the right breast. Innervation by the
3rd and 4th anterior cutaneous branches was
found in 57.1 percent and by the 4th and 5th
anterior cutaneous branches in 10.7 percent
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FIG. 2. Schematic drawing of the breast and the anterior
(ACB) and lateral cutaneous branches (LCB) of the 4th intercostal nerve innervating the nipple and areola. Modified
from Williams, P. L., Warwick, R., Dyson, M., and Bannister,
L. H. (Eds.), The Course of a Typical Intercostal Nerve. In
Gray’s Anatomy, 37th Ed. New York: Churchill Livingstone,
1989. P. 1138. Reprinted with permission.
(Fig. 3). In 28.6 percent of the dissected
breasts, only one nerve supplied the nippleareola complex from the medial side (the 3rd
anterior cutaneous branch in 21.4 percent and
the 4th anterior cutaneous branch in 7.1 percent). In one breast, the 3rd, 4th, and 5th
anterior cutaneous branches contributed to
the supply of the nipple-areola complex from
the medial side (Table I). Again, there was a
reciprocal relationship between the number
and diameter of the supplying nerves: the
more numerous the nerves, the smaller their
diameter.
DISCUSSION
In the past, the innervation of the nipple and
areola has received little attention in anatomic
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PLASTIC AND RECONSTRUCTIVE SURGERY,
FIG. 3. Anterior view of a left breast. Arrows, 3rd and 4th
anterior cutaneous branch terminating at the medial border
of the areola.
space also contributed to the innervation of
the nipple and areola. The number, distribution, and size of these nerves vary; the smaller
the diameter of the nerves, the more numerous they are. We found that the lateral supply
to the nipple and areola did not show as many
variations as the medial supply (the 4th lateral
cutaneous branch innervated the nipple in 93
percent). Because of its size and constancy,
it has always been recognized as the most important nerve for the innervation of the nipple1–5,8,9 (its course, however, has been described controversially). We found that in 93
percent of the breasts it took a subglandular
course within the pectoral fascia and reached
the nipple from its posterior surface—a course
that has been described by Craig and Sykes3
and Gonzalez et al.9 In 7 percent of the breasts,
however, it took a superficial course close to
the skin as described by Cooper,2 Farina et al.,8
and Sarhadi et al.1 Our dissections show that a
superficial course of the lateral cutaneous
branches is possible, but that a deep course is
by far more common; the controversy in the
existing literature is probably because of the
small number of dissected female cadavers
(three to seven).1,3,4,8,9
Montagna and McPherson13 showed in a histologic study that all neural elements are concentrated at the base of the nipple, only few at the
side of the nipple, and practically none in the
areola. They also found nerves along the major
duct system but none in the smaller ducts and
concluded that these could only be sensory, as
there is no evidence of a motor neural mediation
in the mechanism of mammary secretion; this
supports the view that the nerves supplying the
nipple pass through the gland to the posterior
surface of the nipple and are therefore most
likely to be injured by resections at the base of
the breast. Two studies by Sandsmark et al.14 and
Serletti et al.,15 which documented better preservation of the sensitivity of the nipple and areola
after inferior pedicle techniques in comparison
to superior pedicle techniques, are also in keeping with our findings.
A detailed description of the course of the
anterior cutaneous branches has been omitted in
most of the papers on the innervation of the
nipple and areola, and the two existing descriptions are controversial; Craig and Sykes3 describe
a deep course and Sarhadi et al.1 a superficial
course. We found that the anterior cutaneous
descriptions of the breast.6,7 Recent investigations carried out in a small number of cadavers
have yielded contradictory results and added to
the controversy existing about nipple and areola innervation.1,3,4,8 –10
An exact knowledge of the course and distribution of the nerves innervating the nipple
and areola is, however, essential to enable preservation of these nerves during surgery.
The present investigation demonstrates that
the innervation of the nipple and areola shows
frequent variations of the course and distribution of the supplying nerves and helps to explain the previous controversial findings. Only
when a large number of cadavers are dissected
does it become clear that different types of
innervation are possible; it is then that the
most constant patterns can be found.
The nipple and areola are always innervated
by both the anterior and lateral cutaneous
branches of the 3rd, 4th, or 5th intercostal
nerves; this confirms the results of all other
studies except Sarhadi et al.,1 who found that
the anterior branch of the 2nd intercostal
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SENSITIVITY OF THE NIPPLE-AREOLA COMPLEX
branches always took a superficial course in the
subcutaneous tissue, becoming even more superficial as they approached the areola. Therefore,
they are prone to be injured by surgical incisions
near the medial areolar edge. In our study, the
3rd anterior cutaneous branch was found to be
even more constant (82.1 percent) than the 4th
anterior cutaneous branch (78.6 percent). Unlike our findings, Jaspers et al.4 described a medial supply by the 3rd anterior cutaneous branch
in only 25 percent, Sarhadi et al.1 in 50 percent,
and Craig and Sykes3 did not report any numbers. Because innervation by the 3rd and 4th
anterior cutaneous branch seems to be the most
common pattern, surgical incisions at the medial
areolar edge between 8 and 11 o’clock in the left
breast and between 1 and 4 o’clock in the right
breast should be avoided whenever possible.
In summary, our study shows that the innervation of the nipple and areola is very complex
owing to frequent variations of the course and
distribution of the supplying nerves. In the 28
cadavers we dissected, the most common pattern was a lateral innervation by the 4th lateral
cutaneous branch, which took a “deep” course
within the pectoral fascia and reached the nipple from its posterior surface, and a medial
innervation by the 3rd and 4th anterior cutaneous branch, which took a “superficial”
course within the subcutaneous tissue and
reached the medial areolar edge. These nerves
are best protected if surgical resections at the
base of the breast and skin incisions at the
medial edge of the areola are avoided. However, because variations are possible, breast surgery is still associated with the risk of impairing
the sensitivity of the nipple and areola.
Ingrid Schlenz, M.D.
Department of Plastic and Reconstructive Surgery,
Wilhelminenspital
Montleartstasse 37
A-1171 Vienna, Austria
[email protected]
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