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The cutaneous innervation of the human female breast.

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The Cutaneous Innervation of the Human
Female Breast'
MALCOLM R. MILLER AND MICHIKO KASAHARA
Biomechanics Laboratory a n d Department o f Anatomy, University of
California School of Medicine, S a n Francisco, California
Although the anatomy and physiology
of the breast has long been a subject of
intense interest, little attention has been
devoted to the problem of the innervation
of the skin of this area. The historical
summaries in Cathcart et al. ('48), Keiffer ('40), and von Eggeling ('27) on the
innervation of breast skin reveal the poverty of our knowledge of this subject.
In particular, neither a comparative study
of the different areas of the breast nor a
comparison of the innervation of breast
skin with the innervation of other cutaneous areas has been undertaken. The present study will describe and compare the
innervation of the skin of the nipple and
areola with that of all the breast skin peripheral to the areola and will also compare
the innervation i n these areas with cutaneous innervation elsewhere in the body.
MATERIALS AND METHODS
The skin of the nipple and areola and
the surrounding unspecialized breast skin
was studied in freshly amputated breasts
from 15 women whose ages ranged from
30 to 50. In all cases reported here, the
skin was from normal-appearing areas.
The nerve endings were stained by the
methylene-blue immersion method described by Meyling ('53).
OBSERVATIONS
We have learned from our studies of
the skin of the extremities that the types
of nerve endings and their pattern of arrangement are closely related to the disposition of the epidermal and dermal elements (Miller et al., '58). In skin that
lacks hair follicles (glabrous skin), free
fibers are everywhere present, expandedtip endings (Merkel's disks) are found in
association with the undersurf ace of the
epithelium, and encapsulated endings are
most commonly found in the dermal papillae. In hair-covered skin, the same types
of nerve endings are present, but are related to the components of the hair follicle:
Free fibers end between the cells of the
connective-tissue sheath, and expandedtip endings usually terminate on the cells
of the outer root sheath.
Similarly, the innervation of the breast
skin can best be understood in terms of
the degree of development of dermal papillae and the presence or absence of hair
follicles and other specialized dermal
structures.
The breast skin peripheral to the areola
is hair-covered skin and has, at least in
its superficial layers, a pattern of innervation resembling that of hair-covered skin
elsewhere. The areola and the nipple,
however, are specialized areas. While hair
follicles are generally absent from the
areola, a few may be found there. Their
presence, together with the presence of
specialized sebaceous gIands (glands of
Montgomery) in the areolar dermis, attests to the close affinity of areolar skin
with hairy skin. The nipple, on the other
hand, contains no hair follicles and has
well-developed dermal papillae; thus, i t is
more like glabrous skin. It is highly
specialized, containing the openings of the
lactiferous ducts. The presence of large
amounts of smooth muscle and elastic
tissue in the dermis of the areola and nipple further complicates their structure.
T h e innervation of the nipple
and areola
The most frequently occurring nerve
terminals in the nipple and areola are
This investigation was supported by United
States Public Health Service Grant RG-4856.
153
154
M A L C O L M R . M I L L E R A N D MICHIKO KASAHARA
free-fiber endings. These may be single
or multibranched groups and are derived
from small myelinated fibers. The single
endings and those with only a few
branches terminate in the dermis (figs. 2,
4 ) or in the dermal papillae or extend a
short distance between the epithelial cells.
The more abundant multibranched freefiber endings are usually encountered in
the dermal connective tissue of the nipple
in close proximity to the mouths of the
lactiferous ducts. These endings are less
frequent in the areolar dermis.
While we have always found expandedtip endings (Merkel's disks) associated
with the undersurface of the glabrous epidermis in the hand and foot, we have not
observed any such structures in either
the nipple or the areola at this level.
The dermal papillae always contain a
few free fibers, but only infrequently more
organized types of endings. In the areola
we have found a few endings that are
vaguely reminiscent of Meissner's corpuscles; they are elongated, somewhat
compact and confined, but not well encapsulated. We have termed them Meissner-like endings (fig. 3 ) .
A few hair follicles are found at the
peripheral border of the areola. They are
innervated similarly to hair follicles elsewhere.
The dermis of the nipple and areola
contains, in addition to free fibers, unencapsulated loops or whorls of varying
sizes, Ruffini-like endings, and a variety
of encapsulated Krause-like endings. Besides these more recognizable types of
nerve endings there are sometimes found
unusual nerve end formations that have
greatly enlarged expanded tips and may
be multibranched.
The numerous bundles of smooth muscle (fig. 5 ) , the small arteries and arterioles, the arrectores pilorum (fig. 17), the
sweat glands (figs. 18, 19), the glands of
Montgomery, and the lactiferous ducts
(fig. 6 ) are all richly innervated by amyelinated fibers.
T h e inneruation of the breast shin
peripheral to the areola
The skin of the breast peripheral to the
areola is essentially hair-covered skin.
However, i t contains not only the same
types of nerve endings found in the haircovered skin of the extremities, but also
some of the endings usually found only
in glabrous skin.
Although the hair follicles are small,
the endings associated with them are the
same as those found in these structures
elsewhere: The circular fibers end as free
terminations, and the palisade fibers end
with expanded tips (Merkel's disks) (figs.
7, 8). Besides these endings associated
with the hair follicle, there are free fibers
ending in the dermis and in the dermal
papillae, and extending a short distance
between the cells of the epidermis.
In addition to the above-described usual
types of nerve endings which are found in
all hair-covered skin, we have encountered
medium sized groups of expanded-tip endings (Merkel's disks) attached to the undersurface of the epithelium (figs. 9, l o ) ,
and both Ruffini endings (figs. 11-15)
and Krause end bulbs (figs. 11, 16) in the
dermis. In the skin of the extremities,
Merkel's disks, Ruffini endings, and Krause
end bulbs are usually limited to glabrous
skin.
It should be noted, however, that whereas groups of Merkel's disks have been
Fig. 1 A diagrammatic representation showing the types and relative disposition of
the nerve endings i n the skin of the adult human female breast. The left-hand portion of
the figure is the nipple area; the midportion, the areola; and the right-hand portion, the
breast skin peripheral to the areola (breast skin proper). The most abundant nerve endings
i n the nipple area are multibranched dermal free-fiber endings (Bf). These are also found
i n the areolar dermis. Ending in the connective tissue of the papillae are small free-fiber
endings ( f ) . Small looped fiber endings (LE) which may or may not be encapsulated are
found i n the dermis throughout the breast skin. Deeper in the nipple dermis are lactiferous
ducts (LD) innervated by amyelinated fibers ( a f ) .
In the papillae of the areola are elongate, poorly encapsulated structures which we have
termed Meissner-like endings (ML). In the breast skin peripheral to the areola a hair follicle
( H F ) is shown; it is innervated by the usual circular free fibers and vertical palisade fibers.
Apposed to the undersurface of the breast skin epidermis is seen a group of expanded-tip
endings (MD). The dermis of the hairy skin contains Krause-like end bulbs (K-L) and
Ruffini endings (R-L 1.
CUTANEOUS INNERVATION O F BREAST
155
156
MALCOLM R. MILLER A N D MICHIKO KASAHARA
found in the hairy breast skin, they are
neither abundant nor regular in their
occurrence; in previous studies, only Leontowitsch ('01) has commented on their
presence in breast skin. Furthermore,
there are no encapsulated endings in the
shallow papillae of the hairy breast skin.
Thus, the superficial sensory mechanism
of the breast skin peripheral to the areola
must depend largely on the free fibers
and the innervating elements associated
with the hair follicles. In this respect its
innervation is basically the same as that
of hair-covered skin elsewhere.
The dermis of the breast skin is exceptional, however, in that Ruffini and
Krause endings are more regularly found
in this area than in other hair-covered
skin. Although we found no Pacinian corpuscles in the breast skin, Cathcart et al.
('48) and Lefkbure ('09) noted their
presence.
DISCUSSION
The studies of Cathcart et al. ('48),
Keiffer ('4O), and Lefkbure ('09) are generally in agreement concerning the types
of nerve endings found in the skin of the
breast. No studies to date, however, have
specified the exact distribution of the various endings, nor have they compared the
innervation of the breast skin with that of
other areas of the body.
Lefkbure ('09) is, to our knowledge, the
only author who has described the innervation of the hair follicles in breast
skin. In our opinion, a basic role in sensory reception in the major portion of the
breast skin, as in the hairy skin of the
extremities, should be ascribed to the hair
follicle.
Cathcart et al. ('48) emphasized the
richness of innervation of the dermis of
the nipple areas, particularly in relation
to the openings of the lactiferous ducts.
While we agree with Cathcart and his
colleagues on this point, we failed to find
a sympathetic ground plexus as they did.
We believe that there are two significant
aspects of the innervation of the breast
skin. First, the nipple and the areolar area
are poor in the number and types of nerve
endings associated with the epidermis and
the immediately underlying dermis, while
the deeper portions of the dermis, as well
as those elements contained within it
(smooth muscle, lactiferous ducts, sweat
glands), are richly innervated. Secondly,
the breast skin peripheral to the areola,
while basically innervated by the nerve
endings associated with the hair follicles,
contains additional dermal receptors in
the form of Ruffini endings and Krause
end bulbs.
It has been demonstrated that the areolar
and nipple skin has limited sensory discriniination: Light touch is not well perceived, the quality of objects cannot be
determined, and two-point discrimination
is very poor ( Wood-Jones and Turner, '31 ).
This inability of the nipple and the areolar
area to discriminate among certain sensory phenomena is probably associated
with its relative poverty in epidermal and
superficial dermal nerve endings. This
assumption correlates well with the observation that in areas where sensory discrimination is acute, as in the finger tips,
the nerve endings associated with the epidermis and the superficial dermis are
abundant and have a regular pattern of
distribution (Miller et al., '58).
The large number and variety of dermal
nerve endings in the nipple area, on the
other hand, are probably associated with
the phenomena of suckling and of lactation. These nerve endings may be concerned with stimulation of the dermal
smooth muscle for erection of the nipple
to facilitate sucking, with regulation of
blood flow in the mammary gland, with
regulation of the flow of milk, and with
reflex stimulation of the pituitary gland.
It is also possible that the presence of
Ruffini endings and Krause end bulbs in
the dermis of the breast skin peripheral
to the areola may aid in making the breast
sensitive to the oral or manual kneadings
and caresses of the suckling infant. This
stimulation may in turn activate milk flow
through the mechanism mentioned above.
SUMMARY
1. The nerve endings in the skin of the
nipple, the areola, and the breast skin
peripheral to the areola were studied in 15
freshly amputated breasts from women
whose ages ranged from 30 to 50. Meyling's methylene-blue immersion technic
was used.
2. The skin of the nipple is hairless and
has well developed dermal papillae. The
CUTANEOUS INNERVATION OF BREAST
areola contains a few hairs in its peripheral portions, does not have well developed papillae, contains modified sebaceous glands, and thus has many of the
characteristics of hair-covered skin. The
dermis of the nipple and areola is rich
in smooth muscle, elastic tissue, and blood
vessels. It contains sweat glands, modified
sebaceous glands, and the mouths of the
lactiferous ducts.
3 . The epidermis and the papillary dermis of the nipple and the areola are relatively poor in the number and types of
nerve endings. In this region are found
free-fiber endings and an occasional elongated and poorly confined dermal papillary
(Meissner-like) ending. The dermis, on
the other hand, contains a large number
of single and multibranched free-fiber endings. The latter are especially abundant
in the region of the mouths of the lactiferous ducts. Less abundant, but frequent,
are Ruffini-like endings, Krause end bulbs,
and a variety of unencapsulated loops and
whorls that do not fit into a specific category of endings. The small arteries and
arterioles, sweat glands, dermal smooth
muscle, lactiferous ducts, and modified
sebaceous glands are richly innervated by
amyelinated fibers.
4. The breast skin peripheral to the
areola is hair-covered skin. For the most
part, the nerve endings here are free fibers
terminating in the dermis, the dermal papillae, and the epidermis, and those endings
associated with the hair follicle (the free
endings of the circular fibers and the expanded tips of the palisade fibers). In
addition, there are infrequent mediumsized groups of expanded-tip endings associated with the undersurface of the epi-
157
dermis, and there are Ruffini-like endings
and Krause end bulbs in the dermis.
5. The poverty of epidermal and papillary dermal endings in the nipple and
areola is probably related to the lack of
superficial sensory acuity characteristic of
this area. The large number of multibranched free-fiber endings in the dermis
of the nipple and the presence of Ruffinilike endings and Krause end bulbs in the
dermis of the areola and peripheral breast
skin is probably associated with the processes of erection of the nipple for sucking,
of milk flow, and of reflex stimulation of
the pituitary gland.
LITERATURE CITED
Cathcart, E. P., F. W. Gairns and H. S. D. Garven
1948-49 The innervation of the human quiescent nipple, with notes on pigmentation, erection, and hyperneury. Trans. Roy. SOC.Edinburgh, 61: 699-7118].
von Eggeling, H. 1927 Die Milchdruse. I n :
von Mollendorffs Handbuch der mikroskopischen Anatomie des Menschen. Springer-Verlag, Berlin, 3 ( 1 , B ) : 117-153.
Keiffer, M. H. 1940 L'histophysiologie
du
mamelon humain. Bull. Acad. Roy. Med. Belg.,
s. 6, 5: 84-106.
LefCbure, M. 1909 Les terminaisons nerveuses
dans la peau du sein en dehors du mamelon.
J. Anat. Physiol., 45: 339-352.
Leontowitsch, A. 1901 Die Innervation der
menschlichen Haut. Internat. Monatsschr.
Anat. Physiol., 18: 142-310.
Meyling, H. A. 1953 Structure and significance
of the peripheral extension of the autonomic
nervous system. J. Comp. Neur., 99: 495-544.
Qliller, M. R., H. J. Ralston I11 and M. Kasahara
1958 The pattern of cutaneous innervation
of the human hand. Am. J. Anat., 102: 183218.
Wood-Jones, F., and J. B. Turner 1931 A note
on the sensory characters of the nipple and
areola. Med. J. Australia, 1: 778-779.
CUTANEOUS INNERVATION OF BREAST
Malcolm R. Miller and Michiko Kasahara
PLATE 1
The nerve endings in all figures were demonstrated by means of methylene-blue immersion
of specimens of the breast skin of women 30 to 50 years of age.
158
2
Small free fibers i n the superficial dermis of the areola. The view is through the epidermis; the plane of focus is just under the epidermis. X 250.
3
A vertical section through the areola showing a papillary dermal ending which is
elongated and confined but poorly encapsulated. We have termed this structure a
Meissner-like ending. X 300.
CUTANEOUS INNERVATION O F BREAST
Malcolm R. Miller and Michiko Kasahara
PLATE 2
4
Nipple dermis showing several multibranched free-fiber endings. These are abundant
throughout the dermis of the nipple and are especially numerous in the connective
tissue surrounding the lactiferous ducts. x 200.
5
Nipple dermis showing an unencapsulated looped-fiber ending ( L ) and a Ruffini (or
Ruffini-like) ending ( R ) . The numerous fibers in the background are amyelinated
fibers innervating the dermal smooth muscle. X 250.
159
CUTANEOUS INNERVATION OF BREAST
Malcolm R. Miller and Michiko Kasahara
6
A lactiferous duct in the nipple dermis innervated by amyelinated fibers. While some
of the amyelinated fibers form an anastomotic network, it is our opinion that the
ultimate terminals are free. X 300.
160
PLATE 3
CUTANEOUS INNERVATION OF BREAST
Malcolm R. Miller and Michiko Kasahara
PLATE 4
7
A vertical section of the breast skin peripheral to the areola showing a hair follicle.
The skin surface is outside the photograph, on the upper left-hand side. In focus are
the vertically running palisade fibers ( P ) which terminate in expanded tips on the cells
of the outer root sheath. X 100.
8
A portion of another hair follicle showing both circular ( C ) and palisade ( P ) fibers.
x 100.
161
CUTANEOUS INNERVATION OF BREAST
Malcolm R. Miller and Michiko Kasahara
PLATE 5
9 A view through the surface of the breast skin peripheral t o the areola showing a group
of expanded-tip endings apposed t o the undersurface of the epidermis. A single terminal
expansion is labelled ( M ) . X 300.
162
PLATE 6
10 A vertical section of the breast skin peripheral to the areola showing a group of expanded-tip endings apposed to the epithelial undersurface. A single terminal expansion is labelled (M). X 400.
CUTANEOUS INNERVATION OF BREAST
Malcolm R. Miller and Michiko Kasahara
CUTANEOUS INNERVATION OF BREAST
Malcolin R. Miller and Michiko Kasahara
PLATE 7
11 A small Krause-like ending ( K ) and a Ruffini ending ( R ) in the dermis of the breast
skin peripheral to the areola. X 200.
12, 13, 14 Ruffini endings in the dermis of the breast skin peripheral to the areola.
164
x
200.
CUTANEOUS INNERVATION OF BREAST
Malcolm R. Miller and Michiko Kasahara
PLATE 8
15 A Ruffini ending in the dermis of the breast skin peripheral to the areola. x 500.
16
Krause end bulbs i n the dermis of the breast skin peripheral to the areola.
x 300,
165
CUTANEOUS INNERVATION OF BREAST
Malcolm R. Miller a n d Michiko Kasahara
PLATE 9
17 Small amyelinated fibers innervating an arrector pili muscle in the dermis of the breast
skin peripheral to the areola. X 300.
166
CUTANEOUS INNERVATION OF BREAST
Malcolm R. Miller and Michiko Kasahara
PLATE 10
Sweat gland coils in the dermis of the breast skin peripheral to the areola. Note
the amyelinated fibers innervating these structures. Both figures are of the same gland,
but the plane of focus is higher in figure 18. X 250.
18, 19
167
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