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Surgical Embryology and Anatomy of the Breast and its Related Anatomic Structures
SURGICAL ANATOMY AND EMBRYOLOGY
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SURGICAL EMBRYOLOGY AND ANATOMY OF THE BREAST AND ITS RELATED ANATOMIC STRUCTURES Harold Ellis, CBE, FRCS, FACS (Hon), Gene L. Colborn, PhD, and John E. Skandalakis, MD, PhD, FACS
In man (for to explain man is my present task) the mammae are properly placed upon the breast, first, because this is the most suitable location for them if there is nothing else to prevent; second, because the breasts, placed one on each side of the part called the sternum, afford additional protection to the heart lying beneath it; and third, because it is possible in man's case for a residue of useful nutriment to accumulate very abundantly in this location. GALEN, 175 A.D.
De usu partium
The mammary gland is one of the characteristic features of the mammal. Indeed, the term "mammal" derives from the Latin mamma, the breast. It should be noted that the terms "mammary gland" and "breast" are not exactly synonymous, although they will be used in this way for convenience in the following discussion. The word "breast" refers to the mammary gland, plus the additional connective tissue elements and fat that surround and support the gland. Although present in both sexes, the breast is rudimentary in the male. In the female it is undeveloped until puberty but then undergoes considerable growth and differentiation, which is particularly marked during pregnancy and lactation. From the University of Cambridge, Cambridge, United Kingdom (HE); The Medical College of Georgia, Augusta, Georgia (GLC, JES); Emory University School of Medicine, Atlanta, Georgia (JES); and Piedmont Hospital, Atlanta, Georgia (JES)
SURGICAL CLINICS OF NORTH AMERICA VOLUME 73' NUMBER 4· AUGUST 1993
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This article describes the embryology of the breast, its histologic appearances during the various phases of life, the gross anatomy of the breast, and the anatomy of the male breast. The surgical significance of each of these aspects will be considered.
EMBRYOLOGY The breasts develop as downgrowths of the skin. The first evidence of this takes place in the 5-week human fetus when a bilateral thickening develops along the ventral body wall from the axillae to the medial aspect of the proximal part of the thigh. These are termed the mammary ridges or milk lines, which represent potential mammary gland tissue (Fig. 1). In many mammals, a series of paired mammary glands develop along this ridge. In humans, however, most of the ridges disappear apart from the area of the chest wall at the definitive site of the adult nipple. Here, cords of epithelium extend into the underlying mesoderm as solid epithelial columns, comprising some 15 to 20 branches. The epithelial system becomes surrounded by invading mesenchyme, which develops into the supporting connective tissue and fat of the breast. During the last 8 weeks of fetal life, the solid ducts become canalized, and the epidermis at the point of origin of the gland forms a depression, the mammary pit, into which the lactiferous tubules open. At about the time of birth, this pit evaginates to form the definitive nipple. Not infrequently, this process fails, resulting in a congenitally inverted nipple, which may be unilateral or bilateral (Fig. 2). Other congenital abnormalities can be readily explained embryologically.
Figure 1. The milk line. Mammary glands normally develop in humans from the pectoral portion of the line. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 38; with permission.)
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,...,..,....;;~. Epidermis
.. Mesenchyme
A
B
C
D --. Nipple
. Lactiferous ducts
E Figure 2. Development of the breast. A-D, Stages in the development of the duct system and potential glandular tissue from the epidermis. Connective tissue septa form from the epidermis. E, Eversion of the nipple near giving birth. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, P 38; with permission.)
Amastia
Amastia is congenital absence of the breast. It is a rare condition that can be unilateral or bilateral and can occur in either sex. There can be a familial tendency, and there can be an associated hypoplasia of the underlying pectoralis major. A number of cases, all in males, have been reported in which absence of the breast was associated with a thin, dry skin, absence of hair and sweat glands, saddle nose, atrophic nasal mucosa, and underdeveloped or missing teeth. These patients seem to have a generalized defect of ectodermal tissues. Kowlessar and Ortp4 reported complete breast absence in siblings.
Amazia
Amazia is a more commonly seen condition in which the breast tissue fails to form but the nipple is present. More common still than this is hypoplasia of one or both breasts in the presence of a normal nipple.
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Athelia
Athelia is the absence of the nipple in the presence of underlying breast tissue. This is rare at the normal site but is not infrequent in accessory breasts. Accessory Breasts
Accessory breasts (supernumerary breasts or polymastia) usually are found along the embryonic milk line and are nearly always either axillary or thoracic. Accessory breasts below the thorax are rare, occasionally being found on the abdominal wall, groin, or inner side of the thigh. Breast tissue found outside of the milk line is said to be "ectopic." Rare examples have been found on the face, buttock, shoulder, and back. These rare cases are explicable only on the basis that mammary glands are related to sweat glands and apocrine glands. In addition to these, a few cases of midline thoracic or abdominal breast tissue have been described, which may represent displacement of the milk line or may be truly ectopic. About 65% of these supernumerary organs are single, 30% are double, and occasionally three or more supernumerary breasts may occur in the same subject. Polythelia, the presence of accessory nipples, is most commonly observed just inferior and medial to the position of the normal breast. Polymastia and polythelia are not usually accompanied by other congenital anomalies. Gray and Skandalakisl l stated that among whites supernumerary breasts are 90% thoracic, 5% axillary, and 5% abdominal. The condition of polymastia is far from unusual and has been reported to occur, in various series, in between 1% and 5% of subjects. There does not appear to be a sex difference. Subhuman primates appear to be equally subject to polymastia. If no glandular tissue exists, enlargement may occur at puberty or, more often, in late pregnancy. Indeed, if a nipple is present, milk may be secreted. Occasionally the mass may become tender and more painful before each period. Congenital Inversion of the Nipple
The embryologic contribution to the formation of congenital inversion of the nipple has been noted previously. A history showing that the condition was present from birth enables differentiation from the more sinister symptom of recent inversion of the nipple, which so often denotes an underlying carcinoma.
STRUCTURE The breast is made up of lactiferous ducts but no alveoli at birth; it possesses no alveoli until puberty. Prior to puberty, little branching of
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the ducts occurs. At puberty, however, which commences about the age of 10 to 12 in the western world, the ducts proliferate and their terminal branches form solid masses of polythelial cells, the future alveoli. At this time, the nipple becomes more prominent, and the breast, which hitherto has been flat, becomes enlarged. Most of the increase in size is due to accumulation of fat in the connective tissue between the breast lobules. These changes continue during the next 4 or 5 years of adolescent development. The adult breast comprises a collection of tuboalveolar glandular tissue of a firm pinkish-red appearance. This tissue is arranged in 15 to 20 lobes, each of which contains many lobules, which terminate in clusters of rounded alveoli. Histologically, the duct walls are generally composed of two layers of epithelial cells with pale cytoplasm and a pale-staining oval nucleus. The epithelial cells rest on a basement membrane. Each duct is surrounded by cellular intralobular connective tissue, and the lobules themselves are surrounded by relatively noncellular interlobular connective tissue that contains lobules of fat, which make up the bulk of the breast tissue. This stroma of connective tissue contains the supplying blood vessels, lymphatics, and nerves of the breast. Although textbook diagrams show lobules clearly differentiated from their encasing connective tissue, a section of a fresh operative mastectomy specimen will show that the epithelial elements and the connective tissue are closely bound with each other and do not allow a plane of dissection one from the other. Moreover, although the mammary gland is functionally segregated into lobes, dissection of the breast from the premenopausal female demonstrates that the parenchyma forms a continuous and rather dense mass of secretory tissue, not separable into visible "lobes." The 15 to 20 lactiferous ducts converge under the areola of the nipple. Here they expand into lactiferous sinuses, which are lined by a stratified squamous epithelium. Each of these sinuses then constricts into a terminal duct, which runs vertically upward to end at the papilla of the nipple at a visible but narrow orifice. It is probable that the so-called lactiferous sinuses exist only when the lumen of the lactiferous duct just proximal to the base of the nipple is enlarged by the presence of secretions or epithelial cells that have been sloughed from the lining of the duct. The nipple is pink in color in the nulliparous breast but becomes pigmented to a dark brown color in early pregnancy. Some of this pigmentation persists post-partus. The nipple is covered by a stratified squamous keratinized epithelium. Its stroma is composed of dense connective tissue, which contains smooth muscle around the lactiferous ducts. The skin that surrounds the nipple is the areola. The areola undergoes the same pigment changes as does the nipple during pregnancy. Beneath the areola and opening onto its surface are the large areolar glands of Montgomery, which are often visible to the naked eye. Not infrequently, one of these glands becomes obstructed, distended, and infected, forming an abscess.
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Marked changes occur during the early weeks of pregnancy. Ductal sprouting and lobular proliferation occur, and by the eighth week of pregnancy, breast enlargement is clinically obvious, with dilatation of superficial veins over the breast and with increased pigmentation of the areola and nipple. Most epithelial growth in the breast occurs before the end of the sixth month, by which time the lobules are greatly expanded with alveoli, which are composed of a single layer of columnar cells. After the sixth month, the breast continues to enlarge owing to the alveoli becoming distended with colostrum. This contains fat globules and corpuscles that may represent shed lining cells of the alveoli or macrophages. True milk secretion does not commence until a few days after parturition. At this stage, the alveolar cells are distended with large secretory vacuoles, which discharge into the alveolar lumen by apocrine secretion. After lactation ceases, the glandular tissue returns to its resting state, and the alveoli in most cases lose their lumen. After menopause, the glandular tissue of the breast atrophies, and the connective tissue stroma becomes less cellular. In some subjects marked fatty infiltration of the breast occurs at this stage, whereas in others considerable shrinkage of the breast tissue takes place.
TOPOGRAPHY The adult female breast extends from the second rib or upper border of the third rib superiorly to the sixth rib below. Its medial border extends to the lateral edge of the sternum or, in some cases, close to the mid sternal plane, and its lateral border reaches the mid-axillary line. Superolaterally, the breast tissue extends as a projection into the axilla around the lateral, or inferior, border of pectoralis major (the axillary tail of Spence). This may form a palpable or even visible swelling, and its apex may reach as far as the pectoral group of axillary lymph nodes. A tumor in this location may not infrequently be mistaken for an enlarged lymph node and vice versa. The main bulk of the tissue of the breast is concentrated in its upper outer quadrant, which is thus the most usual site for both breast cancer and most benign breast pathologies. The nipple is usually situated at the level of the fourth intercostal space in men and nulliparous females, but its position is inconstant when the breasts are pendulous. About two thirds of the breast lies on the pectoralis major muscle. Inferiorly it extends onto the upper part of the rectus sheath, and laterally it overlaps onto the serratus anterior. 5 The breast is contained within a pocket of superficial fascia (Fig. 3). The subcutaneous layer of this lies immediately deep to the dermis. It is in this plane that cutaneous flaps of skin are raised in the operation of mastectomy. It is relatively avascular. Fibrous processes and irregular strands, the retinacula cutis, extend deeply from the dermis into the underlying tissues of the breast. Such connective tissue bands (the suspen-
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Cenllcal !ascia
Intercostal m.-------;,;u
Aetinaculae cutiS . Cooper's ligament (superficial fascia)
Pectoralis , _ _--+ majorm .
Submammary
space
Superficial fascia
Figure 3. Sagittal cross section of the non lactating female breast and anterior thoracic wall. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 39; with permission.)
,
sory ligaments of Cooper) attach the skin of the breast, the areola, and the nipple to the underlying elements, including the breast parenchyma. The so-called suspensory ligaments of the breast are more developed over the upper part of the breast. Contraction of this fascia by infiltration with malignant cells produces the characteristic dimpling of the skin over a carcinoma of the breast. The deep layer, or membranous layer, of superficial fascia covers the deep aspect of the breast and is separated by a layer of filmy areolar tissue from the underlying fascial covering of pectoralis major and serratus anterior. This areolar layer forms the retromammary or submammary space and enables the normal breast to move freely over the underlying muscles. Deep infiltration of a carcinoma through this space into the
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underlying pectoralis fascia or muscle produces deep tethering of the tumor. The retromammary space enables rapid and relatively avascular dissection of the deep aspect of the breast in simple mastectomy.
Deep Fascia-Related Muscles and Nerves
The deep pectoral fascia encases the pectoralis major muscle and is continuous caudally with the deep fascia of the anterior abdominal wall. Deep to the pectoralis major, the pectoralis minor is ensheathed with a layer of fascia that begins cranially at the clavicle, the clavipectoral fascia. Inferior to the clavicle, this fascial layer envelops the subclavius muscle, and after crossing the region of the infraclavicular fossa, it reaches and covers the pectoralis minor. Between the subclavius and the pectoralis minor, the clavipectoral fascia is pierced by the cephalic vein, the thoracoacromial artery, and the nerve supply to the clavicular head of the pectoralis major. Below the lower border of the pectoralis minor, this fascial layer joins that of the pectoralis major, forming the so-called suspensory ligament of the axilla, by continuity with the fascia of the latissimus dorsi muscle. In some cases, the fascial connection between the pectoral muscles and the latissimus dorsi may contain a more or less distinct band of muscle, in which case it is called the suspensory muscle of
the axilla. The axillary fascia resting at the base of the axillary pyramidal space is an extension of the pectoralis major fascia. It continues as the fascia of latissimus dorsi. The axillary fascia forms the axilla's dome (Fig. 6A). The prevertebral fascia produces a sheet that covers the floor of the posterior triangle of the neck. Where the axillary vessels and the nerves to the arm pass through it, they carry a tubular fascial sleeve, the axillary sheath. The clavipectoral fascia is thus composed of four parts (see Fig. 6A): (1) the attachment to the clavicle and the envelope of the subclavius muscle; (2) the costocoracoid ligament, a thickening of the lateral portion of the clavipectoral fascia between the subclavius and pectoralis minor muscle; (3) the pectoralis minor envelope; and (4) caudally, the clavipectoral fascia joins the muscle fascia of the pectoralis major. The resulting fascial layer passes posteriorly to become continuous with the fascia of the latissimus dorsi, thereby forming the suspensory ligament of the axilla.
MUSCLES
The muscles and nerves of the breast with which the surgeon must be familiar are listed in Table 1.
Table 1. MUSCLES AND NERVES INVOLVED IN MASTECTOMY Muscle
Origin
Insertion
Nerve Supply
Comments
Pectoralis major
Medial half of clavicle, lateral half of sternum, 2nd to 6th costal cartilages, aponeurosis of external oblique muscle
Greater tubercle of humerus
Lateral anterior thoracic nerve
Pectoralis minor
2nd to 5th ribs
Coracoid process of scapula
Medial anterior thoracic nerve
Deltoid
Lateral half of clavicle, lateral border of acromion process, spine of scapula
Deltoid tuberosity of humerus
Axillary nerve
Serratus anterior (3 parts)
1. 1st and 2nd ribs
Costal surface of scapula at superior angle Vertebral border of scapula Costal surface of scapula at inferior angle
Long thoracic nerve
Injury produces "winged scapula."
The anterior border forms the lateral extent of radical mastectomy; injury results in weakness of rotation and abduction of arm.
2. 2nd to 4th ribs 3. 4th to 8th ribs Latissimus dorsi
Back, to crest of ilium
Crest of lesser tubercle and intertubercular groove of humerus
Thoracodorsal nerve
Subclavius
Junction of 1st rib and its cartilage
Groove of lower surface of clavicle
Subclavian nerve
Subscapularis
Costal surface of scapula
Lesser tubercle of humerus
Subscapular nerve
External oblique aponeurosis
External oblique muscle
Rectus sheath and linea alba, crest of ilium
Rectus abdominis
Ventral surface of 5th to 7th costal cartilages and xiphoid process
Crest and superior ramus of pubis
Clavicular portion of pectoralis forms upper extent of radical mastectomy; lateral border forms medial boundary of modified radical mastectomy; both nerves should be preserved in modified radical procedure.
Subscapular nerve should be spared. Remember the interdigitation with serratus anterior and pectoralis muscles.
Branches of 12th thoracic nerve
The rectus sheath is the lower limit of radical mastectomy.
From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili, 1983, p 42; with permission.
a-
.... ~
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BLOOD SUPPLY
The arterial supply of the breast forms a rich anastomotic plexus derived from the internal thoracic, axillary, and intercostal arteries (Fig. 4). The largest vessels supplying the breast arise from the internal thoracic artery via its perforating branches, which pierce the thoracic wall adjacent to the sternal edge in the first to the fourth intercostal spaces. The vessel in the second space is usually the largest of these. A secondary perforating branch is usually found about 2 cm lateral to the main perforating vessel. Thus, the principal vascular supply, both arterial and venous, passes inferiorly and laterally from the upper intercostal spaces, to reach the parenchyma and surrounding tissues superior to a horizontal plane through the nipple. Branches from the axillary artery to the breast include the small supreme thoracic artery, the pectoral branches of the thoracoacromial artery, the lateral thoracic artery, and the subscapular artery, which gives twigs of supply to the lateral aspect of the breast. Small branches of the intercostal arteries in the second, third, and fourth spaces pass to the overlying breast tissue. Venous drainage corresponds to the arteries listed previously, although as with veins everywhere in the body, there are marked anatomic variations. Surgeons who perform a radical mastectomy are well aware
A
B
I c.
Figure 4. Blood supply to the breast. A, The breast may be supplied with blood from the internal thoracic, the axillary, and the intercostal arteries in 18% of individuals. B, The contribution from the axillary artery is negli· gible in 30% of individuals. C, The intercostal arteries contribute little or no blood to the breast in 50% of individuals. Other variations may be found in the remaining 2%. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 43; with permission.)
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of the variable distribution of the tributaries that drain into the axillary vein (Fig. 5). AXILLA
The axilla (Figs. 6 and 7) is a pyramidal space having an apex, a base, and four walls. Its apex is at the junction of the clavicle, the upper border of the scapula, and the first rib. The base is formed by axillary fascia beneath the skin of the axillary fossa. The anterior wall consists of three muscles-the pectoralis major, the pectoralis minor, and the subclavius-together with the fasciae that envelop these muscles and fill the spaces between them. The posterior wall is composed of the scapula and
Sternum
A In!. thoracic v. to right heart . &lungs
Figure 5. Frontal section through the right breast showing pathways of venous drainage. A, Medial drainage through the thoracic vein to the right heart. B, Posterior drainage to vertebral veins. C, Lateral drainage to intercostal vein, superior epigastric veins, and liver. D, Lateral superior drainage through axillary vein to the right heart. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGrawHill Book Company, 1983, p 44; with permission.)
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_Clavi pectoral fascia .... ,.."..,--Axillary a.
Pectoralis major m.
\~hn---
Pectoralis minor m.
Subscapularis
~~--Suspensory
ligament (clavi pectoral fascia) - Teres major
Deep fascia of armpit (axillary) ~~~---
Latissimus dorsi
B .
Serratus anterior
Humerus --4-...f,I~~
Serratus anterior
o
major m.
c Figure 6. The walls of the axilla. A. Anterior wall. B, Posterior wall. C, Medial wall. D, Lateral wall. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili, 1983, P 40; with permission.)
three muscles: the subscapularis, the latissimus dorsi, and the teres major. The medial wall is formed by the lateral chest wall, which includes the second to sixth ribs and the serratus anterior muscle. The lateral wall, the narrowest wall, is formed by the bicipital groove of the humerus. The axilla contains lymph nodes, the axillary sheath, and its contained elements of the brachial plexus of nerves, the tendon of the long head of the biceps brachii, the short head of the biceps, and the coracobrachialis muscles.
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Pectoralis " minor Pectoralis . major
Medial
~~~~~~I-- pectoral n.
Lateral thoracic a.
Th'lrl"'nrlnr~.,,1
n.
Long thoracic n.
Figure 7. Anterior view of the topography of the axilla. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw·Hili Book Company, 1983, p 41; with permission.)
LYMPHATIC DRAINAGE
A plexus of lymphatic vessels lies in the interlobular connective tissue and communicates with a subareolar plexus around the nipple (the subareolar plexus of Sappey). Efferent vessels pass from the breast tissue around the anterior axillary fold to the pectoral (anterior) group of axillary nodes, which lie along the lateral thoracic artery and vein at about the level of attachment of the pectoralis minor to the fifth rib. Some channels pass directly to the subscapular (posterior) group. Efferent vessels drain from the superior aspect of the breast directly to the apical axillary nodes deep to the clavipectoral fascia, just inferior to the clavicle, sometimes interrupted by small interpectoral and infraclavicular nodes. From the medial part of the breast, lymphatics drain along the perforat-
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ing vessels to the internal thoracic chain of nodes. Some drainage occurs along the lateral cutaneous branches of the posterior intercostal veins to the intercostal chain of nodes near the rib heads. About three quarters of all lymphatic drainage of the breast passes to the axillary nodes; the remainder drains principally to the internal thoracic group. Any part of the breast may drain to either group, although there is a greater tendency for tumors in the medial part of the breast to disseminate to the internal thoracic nodes than for growths in the lateral part of the breast. Involvement of the supraclavicular nodes in the spread of breast cancer usually represents retrograde spread along blocked lymphatic channels when the apical nodes are heavily involved. However, efferent channels do pass directly from these nodes to the inferior deep cervical chain, so that involvement of the cervical nodes may occur via this route. Lymphatic do not normally drain to lymphatics across the opposite side of the body. However, in very advanced tumors, extensive blockage of lymphatic channels allows subcutaneous lymphatic permeation to occur to the opposite side. Lymphatic drainage of the breast typically accompanies the blood supply. Drainage from any quadrant of the breast passes to axillary nodes (75%) or to the internal mammary chain (25%), according to Hultborn et al.13 The lymph flow was traced upward and laterally through the tail of the breast to the central lymph nodes by HaagensenP Metastases are most frequently found at this location. Another drainage route follows lymphatics that pierce the pectoralis major and pass upward between the pectoralis major and minor to reach the axillary vein group or the sub clavicular group of nodes. A few interpectoral nodes (of Rotter) may be encountered between the two muscles. The subclavicular group of nodes is important, because Haagensen believes metastasis to these nodes renders surgical cure impossible (Fig. 8). The mortality rates from lesions in different locations in the breast vary greatly despite anatomic evidence. The inner lower quadrant was the least frequently affected, but it had the highest relative mortality in a series of 142 patients recorded by Gray and Skandalakisl l (Fig. 9). Fisher et a19 stated that regional lymph nodes are primary indicators and not instigators of distal disease. They assert that lower axillary dissection is more than adequate to fulfill the aims of axillary node dissection. The qualitative axillary nodal status (positive or negative) can be accurately determined with the removal of a few lymph nodes according to the same authors. Re-examination of surgical specimens taken from 24 radical mastectomies by Skandalakis et aP9 revealed that 19.5% of the lymph nodes removed during surgery escaped examination by the pathologist. In a second group of 20 modified radical mastectomies, re-examination found that 7.7% were not initially removed. In one patient, a malignant node was sectioned only during re-examination. With this in mind, we agree with Stone and Cady,2° who stated that the goals of axillary dissection may be diagnostic or therapeutic. Lymph nodes appear in inconstant groups of varying numbers. This
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Subclavicular (apical) nodes Axillary nodes
/
Central nodes
I
Scapular nodes
\
Ext. mammary (pectoral) nodes
Figure 8. Lymphatic drainage of the breast. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 45; with permission.)
inconstancy is reflected and perhaps magnified by the inconsistency of the terminology for the lymph nodes as used by various authors. We recommend the terminology of Haagensen et al,l2 Because lymph nodes vary in occurrence and many are very small (Fig. 10), only acute examination will reveal all those present. 19 The major groups of lymph nodes, as described by Haagensen et al/ 2 with the average number of nodes in each, are as follows.
37 ~
A
/ /
//~
13
La!.
Med.
28.6
B
~/
/
1
32.0/
71.5
"-
~"-
50.0
Figure 9. A, Localization of breast tumors in 328 patients. B, Five-year mortality from breast tumors by location (percentage dying < 5 years; 142 patients, all ages). (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 46; with permission.)
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Internal mammary nodes
Axillary vein nodes
Central nodes
External . mammary nodes
Figure 10. Lymph nodes of the breast and axilla. Classification is that of Haagensen et al.'2 (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 45; with permission.)
Axillary Drainage (35_3 Nodes) Group 1: External mammary nodes (1.7 nodes). These lie under the lateral edge of the pectoralis major, along the medial side of the axilla. They follow the course of the lateral thoracic artery on the chest wall from the second to the sixth rib. Group 2: Scapular nodes (5.8 nodes). These rest on the subscapular vessels and their thoracodorsal branches. Group 3: Central nodes (12.1 nodes). Embedded in fat in the axilla's center, these form the largest group of lymph nodes and are the most easily palpated in the axilla. Group 4: Interpectoral nodes (Rotter's nodes) (1.4 nodes). These are located between the pectoralis major and minor muscles. Often occurring singularly, this is the smallest group of the axillary nodes. The pectoralis major must be removed to access these nodes. Group 5: Axillary vein nodes (10.7 nodes). These extend on the cau-
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dal and ventral surfaces of the lateral part of the axillary vein. This is the second largest of the axillary lymph nodes. Group 6: Subclavian nodes (3.5 nodes). These lie on the caudal and ventral exterior of the medial portion of the axillary vein. They are inaccessible without removal of the pectoralis minor, according to Haagensen et al. 12 However classified by the surgeon, the axillary lymph nodes are defined in three levels according to their location in relation to the pectoralis minor muscle (Fig. 11): Level I: Lymph nodes that are located at the vicinity of the lower border of the pectoralis minor muscle. This level is formed by three groups: exterior mammary lymph nodes, axillary vein lymph nodes, and scapular lymph nodes. Level II: Lymph nodes located deep to (under) the pectoralis minor muscle. This level is formed by central lymph nodes and some subclavian nodes. Level III: Lymph nodes located at the medial bonier of the pectoralis minor. These are the sub clavicular group.
Internal Thoracic (Mammary) Drainage (8.5 Nodes)
Lymphatic vessels arise on the pectoralis fascia on the medial edge of the breast. They accompany the perforating blood vessels and, at the end of the intercostal space, pierce the pectoralis major and intercostal muscles to reach the internal thoracic nodes. Usually located within the
Figure 11. Levels of axillary lymph nodes identified in relation to the pectoralis minor muscle: I = lateral; II = behind; III = medial. (From Wood WC: Definitive surgery for stages I and II breast cancer. In Kennedy BJ (ed): Breast Cancer. New York, Alan R. Liss, Inc., 1989, p 98, copyright © 1989 Wiley-Liss; reprinted by permission of Wiley-Liss, a Division of John Wiley and Sons, Inc.)
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fat and connective tissue of the intercostal spaces, there are usually four to five of these small nodes on each side. Lymphatic trunks to these nodes arise from the liver, diaphragm, rectus sheath, and the upper portion of the rectus abdorninis. 12 The internal thoracic trunks drain into the right lymphatic duct or the thoracic duct. Overall, this is a shorter route than the axillary route to the venous system. Other Nodes
The student of breast anatomy should also remember that there are a few other lymph nodes associated in an indirect way with the breast, such as intercostal lymph nodes, diaphragmatic nodes, and mediastinal nodes. ANATOMIC COMPLICATIONS OF MASTECTOMY
We include the anatomic complications of breast surgery in this presentation to emphasize the anatomic entities with which the surgeon must be familiar during surgery of the breast. Although radical mastectomy rarely is performed, Bland and Copeland l correctly state that radical mastectomy is occasionally necessary to achieve local and regional control of malignancy in the breast, axilla, and chest wall. Skin
The most frequent complication of mastectomy is skin necrosis. To avoid recurrence of malignant disease, all fat and glandular tissue must be removed. Vascular Injury
Sources of bleeding during mastectomy are (1) perforating arteries and veins, especially those of the first and second intercostal vessels, (2) the axillary vein and its tributaries, and (3) the axillary artery and its branches. Coller et a1 5 estimate the average blood loss during radical mastectomy to be 732 mL. The perforating vessels should be ligated, because the first three are too large for cautery. If torn, the axillary vein must also be ligated. Although rare,22 an injury to the axillary artery should be repaired, if necessary, between bulldog clamps. Postoperative edema of the arm frequently follows mastectomy, but functional impairment is less cornmon. Although obstruction to the axillary vein once was considered to be an important factor in edema formation, this has been disproved by subsequent studies. 15,21 Lymphatic
THE BREAST AND ITS RELATED ANATOMIC STRUCTURES
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destruction appears to be the sole cause of edema, which occurs in approximately 50% of patients undergoing radical mastectomy. Organ Injury
Pneumothorax is a danger during ligation of perforating vessels. The surgeon should use curved hemostats and avoid use at right angles. Although the pneumothorax is easily repaired, any contamination of the pleural cavity with malignant cells can prove a delayed disaster. Zintel and Nay22 reported one pneumothorax among 249 consecutive radical mastectomies. Nerve Injury Thoracodorsal Nerve
The thoracodorsal (middle subscapular) nerve arises from the posterior cord of the brachial plexus and innervates the latissimus dorsi muscle (Fig. 12). Although there will be no deformity, internal rotation and adduction of the arm will be weakened if the nerve is cut. The nerve and its associated vessels can best be located near the medial border of the latissimus dorsi about 5 em above a plane passing through the third sternochondral junction. The neurovascular bundle, when found, should be marked with an umbilical tape. Obvious involvement of lymph nodes around the nerve will necessitate the nerve's removal. Long Thoracic Nerve
The long thoracic nerve innervates and lies upon the serratus anterior muscle in the midaxillary line. Section of the nerve results in the "winged scapula" deformity. This nerve should, therefore, be spared unless actually invaded by cancer. The point at which the axillary vein passes over the second rib identifies the nerve's location. Careful dissection of this area will reveal it descending on the second rib posterior to the axillary vein. 8 Anterior Thoracic Nerves
Several authors l6-18 have emphasized the importance of the medial and lateral pectoral nerves. The medial pectoral nerve arises from the medial cord of the brachial plexus, deep to the pectoralis minor. After it receives ~ communication from the lateral pectoral nerve, the medial pectoral nerve passes through the pectoralis minor, supplying it, and then ends within the sternal part of the pectoralis major. The lateral pectoral nerve arises from the lateral cord of the brachial plexus. One branch of this nerve passes directly to the clavicular head of the pecto-
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Upper subscapular n.
Long thoracic
n.
Pectoralis major & minor (cut)
Thoracodorsal n.
Serratus anterior
Subscapularis m.
m.
Medial border of latissimus dorsi m.
A
Retracted axillary margin (pectoralis major minor)
a
B Figure 12. A, The triangular bed of a radical mastectomy. B, The triangular bed of a modified radical mastectomy. The pectoralis muscles are retracted rather than removed. The triangle is slightly smaller than that shown in A. (From Skandalakis LJ, Vohman MD, Skandalakis JE, et al: The axillary lymph nodes in radical and modified radical mastectomy. Am Surg 45:552, 1979; with permission.)
ralis major, which it supplies solely. The remaining part of the lateral pectoral nerve communicates with the medial pectoral nerve. Injury to the lateral pectoral nerve will result in atrophy of the clavicular head of the pectoralis major, with an accompanying severe cosmetic deformity just inferior to the clavicle. Injury to the medial pectoral nerve branches will result in atrophy of the sternal and costal parts of the pectoralis major and the pectoralis minor muscles. The nerves should be removed if the few lymph nodes of the interpectoral group are involved and are fixed with these nerves.
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It is of some importance to plastic surgeons, especially, to know that the nerve supply to the areola and nipple is attributable to the anterior ramus of the lateral cutaneous branch of the fourth thoracic (T4) or intercostal nerve. This branch, which provides sensation for the nipple and areola and motor supply to the smooth muscle of the nipple, passes medially after turning about the lateral border of the pectoralis major muscle, within the superficial fascia. It can be spared in reconstructive procedures, thereby leaving the patient with a sensate and responsive nipple. Brachial Plexus
Most injury to the plexus is the result of stretching the nerves during surgery, although direct injury is possible. Zintel and Nay22 had one patient in a series of 249 mastectomies suffer transient injury to the plexus. THE MALE BREAST
The male breast remains rudimentary in its prepubertal stage, up to which time it is identical with the female breast. It comprises small ducts or cords of cells with scanty supporting fibrous tissues and a variable amount of periductal fat. It is generally stated that the male breast does not extend beyond the areola, although it is well known that male breast tumors may occur from areas outside the diameter of the areola. Carcinoma of the male breast constitutes about 1% of all breast cancers, less than 1.5% of all malignant tumors in men. 3 In a study of 40 cadaveric male breasts, we have shown that the glandular epithelium radiates from the central fibrous nodule to a highly variable extent. 4 In one third of normal specimens, the glandular tissue extended beyond the confines of the pigmented areola. CONCLUSION
This article provides the general and plastic surgeon with knowledge of the surgical embryology and surgical anatomy of the breast and its associated anatomic entities. Careful anatomic technique for the simplest and more radical breast operations will avoid complications and will benefit both the patient and the surgeon. References 1. Bland KI, Copeland EM III (eds): The Breast. Philadelphia, WB Saunders, 1991, p 587 2. Blevins PK: Subcutaneous mastectomy and breast replacement: Its role in the treatment of benign, premalignant, and malignant breast disease. Am Surg 47:281,1981 3. Crichlow RW, Galt SW: Male breast cancer. Surg Clin North Am 70:1165-1177, 1990
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4. Cochrane R, Gee A, Ellis H: Microscopic topography of the male breast. The Breast 1:25-27, 1992 5. Coller FA, Crook CE, lob V: Blood loss in surgical operations. JAMA 126:1, 1944 6. DeCosse JJ: Is the demise of radical mastectomy premature? Surgery 89:398, 1981 7. Donegan WL: General considerations. In Operative Surgery: Principles and Techniques, ed 2. Philadelphia, Lea & Febiger, 1980 8. Feller I, Woodburne RT: The long thoracic and thoracodorsal nerves in radical mastectomy. Surg Gynecol Obstet 107:798, 1958 9. Fisher BN, Wolmark, Bauer M, et al: The accuracy of clinical nodal staging and of limited axillary dissection as a determinant of histologic nodal status in carcinoma of the breast. Surg Gynecol Obstet 152:765, 1981 10. Goldman LD, Goldwyn RM: Some anatomical considerations for subcutaneous mastectomy. Plast Reconstr Surg, 51:501, 1973 11. Gray SW, Skandalakis JE: Embryology for Surgeons, ed 2. Baltimore, Williams & Wilkins, 1993 12. Haagensen CD: Lymphatics of the breast. In Haagensen CD, et al (eds): The Lymphatics in Cancer. Philadelphia, WB Saunders, 1972 13. Hultborn AL, Hulten B, Roos M, et al: Effectiveness of axillary lymph node dissection in modified radical mastectomy with preservation of pectoral muscles. Ann Surg 179:269,1974 14. Kowlessar M, Orti E: Complete breast absence in Siblings. Am J Dis Child 115:91, 1968 15. MacDonald I: Resection of the axillary vein in radical mastectomy: Its relation to the mechanism of lymphedema, Cancer 1:618, 1948 16. Moosman DA: Anatomy of the pectoral nerves and their preservation in modified mastectomy. Am J Surg 139:883,1980 17. Scanlon EF: The importance of the anterior thoracic nerves in modified radical mastectomy. Surg Gynecol Obstet 152:789,1981 18. Scanlon EF, Caprini JA: Modified radical mastectomy. Cancer 35:710, 1975 19. Skandalakis LJ, Vohman MD, Skandalakis JE, et al: The axillary lymph nodes in radical and modified radical mastectomy. Am Surg 45:552,1979 20. Stone MD, Cady B: Techniques of lumpectomy and axillary dissection. Surg Clin North Am 70:885, 1990 21. Watson TA, Bond AF, Phillips AJ: Swelling and dysfunction of the upper limb following radical mastectomy. Surg Gynecol Obstet 116:99, 1963 22. Zintel HA, Nay HR: Postoperative complications of radical mastectomy. Surg Clin North Am 44:313,1964
Address reprint requests to John E. Skandalakis, MD, PhD, FACS Centers for Surgical Anatomy and Technique Emory University School of Medicine 1462 Clifton Road, NE Suite 303 Atlanta, GA 30322
0039-6109/93 $0.00 + .20
SURGICAL EMBRYOLOGY AND ANATOMY OF THE BREAST AND ITS RELATED ANATOMIC STRUCTURES Harold Ellis, CBE, FRCS, FACS (Hon), Gene L. Colborn, PhD, and John E. Skandalakis, MD, PhD, FACS
In man (for to explain man is my present task) the mammae are properly placed upon the breast, first, because this is the most suitable location for them if there is nothing else to prevent; second, because the breasts, placed one on each side of the part called the sternum, afford additional protection to the heart lying beneath it; and third, because it is possible in man's case for a residue of useful nutriment to accumulate very abundantly in this location. GALEN, 175 A.D.
De usu partium
The mammary gland is one of the characteristic features of the mammal. Indeed, the term "mammal" derives from the Latin mamma, the breast. It should be noted that the terms "mammary gland" and "breast" are not exactly synonymous, although they will be used in this way for convenience in the following discussion. The word "breast" refers to the mammary gland, plus the additional connective tissue elements and fat that surround and support the gland. Although present in both sexes, the breast is rudimentary in the male. In the female it is undeveloped until puberty but then undergoes considerable growth and differentiation, which is particularly marked during pregnancy and lactation. From the University of Cambridge, Cambridge, United Kingdom (HE); The Medical College of Georgia, Augusta, Georgia (GLC, JES); Emory University School of Medicine, Atlanta, Georgia (JES); and Piedmont Hospital, Atlanta, Georgia (JES)
SURGICAL CLINICS OF NORTH AMERICA VOLUME 73' NUMBER 4· AUGUST 1993
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ELLIS et al
This article describes the embryology of the breast, its histologic appearances during the various phases of life, the gross anatomy of the breast, and the anatomy of the male breast. The surgical significance of each of these aspects will be considered.
EMBRYOLOGY The breasts develop as downgrowths of the skin. The first evidence of this takes place in the 5-week human fetus when a bilateral thickening develops along the ventral body wall from the axillae to the medial aspect of the proximal part of the thigh. These are termed the mammary ridges or milk lines, which represent potential mammary gland tissue (Fig. 1). In many mammals, a series of paired mammary glands develop along this ridge. In humans, however, most of the ridges disappear apart from the area of the chest wall at the definitive site of the adult nipple. Here, cords of epithelium extend into the underlying mesoderm as solid epithelial columns, comprising some 15 to 20 branches. The epithelial system becomes surrounded by invading mesenchyme, which develops into the supporting connective tissue and fat of the breast. During the last 8 weeks of fetal life, the solid ducts become canalized, and the epidermis at the point of origin of the gland forms a depression, the mammary pit, into which the lactiferous tubules open. At about the time of birth, this pit evaginates to form the definitive nipple. Not infrequently, this process fails, resulting in a congenitally inverted nipple, which may be unilateral or bilateral (Fig. 2). Other congenital abnormalities can be readily explained embryologically.
Figure 1. The milk line. Mammary glands normally develop in humans from the pectoral portion of the line. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 38; with permission.)
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,...,..,....;;~. Epidermis
.. Mesenchyme
A
B
C
D --. Nipple
. Lactiferous ducts
E Figure 2. Development of the breast. A-D, Stages in the development of the duct system and potential glandular tissue from the epidermis. Connective tissue septa form from the epidermis. E, Eversion of the nipple near giving birth. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, P 38; with permission.)
Amastia
Amastia is congenital absence of the breast. It is a rare condition that can be unilateral or bilateral and can occur in either sex. There can be a familial tendency, and there can be an associated hypoplasia of the underlying pectoralis major. A number of cases, all in males, have been reported in which absence of the breast was associated with a thin, dry skin, absence of hair and sweat glands, saddle nose, atrophic nasal mucosa, and underdeveloped or missing teeth. These patients seem to have a generalized defect of ectodermal tissues. Kowlessar and Ortp4 reported complete breast absence in siblings.
Amazia
Amazia is a more commonly seen condition in which the breast tissue fails to form but the nipple is present. More common still than this is hypoplasia of one or both breasts in the presence of a normal nipple.
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Athelia
Athelia is the absence of the nipple in the presence of underlying breast tissue. This is rare at the normal site but is not infrequent in accessory breasts. Accessory Breasts
Accessory breasts (supernumerary breasts or polymastia) usually are found along the embryonic milk line and are nearly always either axillary or thoracic. Accessory breasts below the thorax are rare, occasionally being found on the abdominal wall, groin, or inner side of the thigh. Breast tissue found outside of the milk line is said to be "ectopic." Rare examples have been found on the face, buttock, shoulder, and back. These rare cases are explicable only on the basis that mammary glands are related to sweat glands and apocrine glands. In addition to these, a few cases of midline thoracic or abdominal breast tissue have been described, which may represent displacement of the milk line or may be truly ectopic. About 65% of these supernumerary organs are single, 30% are double, and occasionally three or more supernumerary breasts may occur in the same subject. Polythelia, the presence of accessory nipples, is most commonly observed just inferior and medial to the position of the normal breast. Polymastia and polythelia are not usually accompanied by other congenital anomalies. Gray and Skandalakisl l stated that among whites supernumerary breasts are 90% thoracic, 5% axillary, and 5% abdominal. The condition of polymastia is far from unusual and has been reported to occur, in various series, in between 1% and 5% of subjects. There does not appear to be a sex difference. Subhuman primates appear to be equally subject to polymastia. If no glandular tissue exists, enlargement may occur at puberty or, more often, in late pregnancy. Indeed, if a nipple is present, milk may be secreted. Occasionally the mass may become tender and more painful before each period. Congenital Inversion of the Nipple
The embryologic contribution to the formation of congenital inversion of the nipple has been noted previously. A history showing that the condition was present from birth enables differentiation from the more sinister symptom of recent inversion of the nipple, which so often denotes an underlying carcinoma.
STRUCTURE The breast is made up of lactiferous ducts but no alveoli at birth; it possesses no alveoli until puberty. Prior to puberty, little branching of
THE BREAST AND ITS RELATED ANATOMIC STRUCTURES
615
the ducts occurs. At puberty, however, which commences about the age of 10 to 12 in the western world, the ducts proliferate and their terminal branches form solid masses of polythelial cells, the future alveoli. At this time, the nipple becomes more prominent, and the breast, which hitherto has been flat, becomes enlarged. Most of the increase in size is due to accumulation of fat in the connective tissue between the breast lobules. These changes continue during the next 4 or 5 years of adolescent development. The adult breast comprises a collection of tuboalveolar glandular tissue of a firm pinkish-red appearance. This tissue is arranged in 15 to 20 lobes, each of which contains many lobules, which terminate in clusters of rounded alveoli. Histologically, the duct walls are generally composed of two layers of epithelial cells with pale cytoplasm and a pale-staining oval nucleus. The epithelial cells rest on a basement membrane. Each duct is surrounded by cellular intralobular connective tissue, and the lobules themselves are surrounded by relatively noncellular interlobular connective tissue that contains lobules of fat, which make up the bulk of the breast tissue. This stroma of connective tissue contains the supplying blood vessels, lymphatics, and nerves of the breast. Although textbook diagrams show lobules clearly differentiated from their encasing connective tissue, a section of a fresh operative mastectomy specimen will show that the epithelial elements and the connective tissue are closely bound with each other and do not allow a plane of dissection one from the other. Moreover, although the mammary gland is functionally segregated into lobes, dissection of the breast from the premenopausal female demonstrates that the parenchyma forms a continuous and rather dense mass of secretory tissue, not separable into visible "lobes." The 15 to 20 lactiferous ducts converge under the areola of the nipple. Here they expand into lactiferous sinuses, which are lined by a stratified squamous epithelium. Each of these sinuses then constricts into a terminal duct, which runs vertically upward to end at the papilla of the nipple at a visible but narrow orifice. It is probable that the so-called lactiferous sinuses exist only when the lumen of the lactiferous duct just proximal to the base of the nipple is enlarged by the presence of secretions or epithelial cells that have been sloughed from the lining of the duct. The nipple is pink in color in the nulliparous breast but becomes pigmented to a dark brown color in early pregnancy. Some of this pigmentation persists post-partus. The nipple is covered by a stratified squamous keratinized epithelium. Its stroma is composed of dense connective tissue, which contains smooth muscle around the lactiferous ducts. The skin that surrounds the nipple is the areola. The areola undergoes the same pigment changes as does the nipple during pregnancy. Beneath the areola and opening onto its surface are the large areolar glands of Montgomery, which are often visible to the naked eye. Not infrequently, one of these glands becomes obstructed, distended, and infected, forming an abscess.
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Marked changes occur during the early weeks of pregnancy. Ductal sprouting and lobular proliferation occur, and by the eighth week of pregnancy, breast enlargement is clinically obvious, with dilatation of superficial veins over the breast and with increased pigmentation of the areola and nipple. Most epithelial growth in the breast occurs before the end of the sixth month, by which time the lobules are greatly expanded with alveoli, which are composed of a single layer of columnar cells. After the sixth month, the breast continues to enlarge owing to the alveoli becoming distended with colostrum. This contains fat globules and corpuscles that may represent shed lining cells of the alveoli or macrophages. True milk secretion does not commence until a few days after parturition. At this stage, the alveolar cells are distended with large secretory vacuoles, which discharge into the alveolar lumen by apocrine secretion. After lactation ceases, the glandular tissue returns to its resting state, and the alveoli in most cases lose their lumen. After menopause, the glandular tissue of the breast atrophies, and the connective tissue stroma becomes less cellular. In some subjects marked fatty infiltration of the breast occurs at this stage, whereas in others considerable shrinkage of the breast tissue takes place.
TOPOGRAPHY The adult female breast extends from the second rib or upper border of the third rib superiorly to the sixth rib below. Its medial border extends to the lateral edge of the sternum or, in some cases, close to the mid sternal plane, and its lateral border reaches the mid-axillary line. Superolaterally, the breast tissue extends as a projection into the axilla around the lateral, or inferior, border of pectoralis major (the axillary tail of Spence). This may form a palpable or even visible swelling, and its apex may reach as far as the pectoral group of axillary lymph nodes. A tumor in this location may not infrequently be mistaken for an enlarged lymph node and vice versa. The main bulk of the tissue of the breast is concentrated in its upper outer quadrant, which is thus the most usual site for both breast cancer and most benign breast pathologies. The nipple is usually situated at the level of the fourth intercostal space in men and nulliparous females, but its position is inconstant when the breasts are pendulous. About two thirds of the breast lies on the pectoralis major muscle. Inferiorly it extends onto the upper part of the rectus sheath, and laterally it overlaps onto the serratus anterior. 5 The breast is contained within a pocket of superficial fascia (Fig. 3). The subcutaneous layer of this lies immediately deep to the dermis. It is in this plane that cutaneous flaps of skin are raised in the operation of mastectomy. It is relatively avascular. Fibrous processes and irregular strands, the retinacula cutis, extend deeply from the dermis into the underlying tissues of the breast. Such connective tissue bands (the suspen-
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Cenllcal !ascia
Intercostal m.-------;,;u
Aetinaculae cutiS . Cooper's ligament (superficial fascia)
Pectoralis , _ _--+ majorm .
Submammary
space
Superficial fascia
Figure 3. Sagittal cross section of the non lactating female breast and anterior thoracic wall. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 39; with permission.)
,
sory ligaments of Cooper) attach the skin of the breast, the areola, and the nipple to the underlying elements, including the breast parenchyma. The so-called suspensory ligaments of the breast are more developed over the upper part of the breast. Contraction of this fascia by infiltration with malignant cells produces the characteristic dimpling of the skin over a carcinoma of the breast. The deep layer, or membranous layer, of superficial fascia covers the deep aspect of the breast and is separated by a layer of filmy areolar tissue from the underlying fascial covering of pectoralis major and serratus anterior. This areolar layer forms the retromammary or submammary space and enables the normal breast to move freely over the underlying muscles. Deep infiltration of a carcinoma through this space into the
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ELLIS et al
underlying pectoralis fascia or muscle produces deep tethering of the tumor. The retromammary space enables rapid and relatively avascular dissection of the deep aspect of the breast in simple mastectomy.
Deep Fascia-Related Muscles and Nerves
The deep pectoral fascia encases the pectoralis major muscle and is continuous caudally with the deep fascia of the anterior abdominal wall. Deep to the pectoralis major, the pectoralis minor is ensheathed with a layer of fascia that begins cranially at the clavicle, the clavipectoral fascia. Inferior to the clavicle, this fascial layer envelops the subclavius muscle, and after crossing the region of the infraclavicular fossa, it reaches and covers the pectoralis minor. Between the subclavius and the pectoralis minor, the clavipectoral fascia is pierced by the cephalic vein, the thoracoacromial artery, and the nerve supply to the clavicular head of the pectoralis major. Below the lower border of the pectoralis minor, this fascial layer joins that of the pectoralis major, forming the so-called suspensory ligament of the axilla, by continuity with the fascia of the latissimus dorsi muscle. In some cases, the fascial connection between the pectoral muscles and the latissimus dorsi may contain a more or less distinct band of muscle, in which case it is called the suspensory muscle of
the axilla. The axillary fascia resting at the base of the axillary pyramidal space is an extension of the pectoralis major fascia. It continues as the fascia of latissimus dorsi. The axillary fascia forms the axilla's dome (Fig. 6A). The prevertebral fascia produces a sheet that covers the floor of the posterior triangle of the neck. Where the axillary vessels and the nerves to the arm pass through it, they carry a tubular fascial sleeve, the axillary sheath. The clavipectoral fascia is thus composed of four parts (see Fig. 6A): (1) the attachment to the clavicle and the envelope of the subclavius muscle; (2) the costocoracoid ligament, a thickening of the lateral portion of the clavipectoral fascia between the subclavius and pectoralis minor muscle; (3) the pectoralis minor envelope; and (4) caudally, the clavipectoral fascia joins the muscle fascia of the pectoralis major. The resulting fascial layer passes posteriorly to become continuous with the fascia of the latissimus dorsi, thereby forming the suspensory ligament of the axilla.
MUSCLES
The muscles and nerves of the breast with which the surgeon must be familiar are listed in Table 1.
Table 1. MUSCLES AND NERVES INVOLVED IN MASTECTOMY Muscle
Origin
Insertion
Nerve Supply
Comments
Pectoralis major
Medial half of clavicle, lateral half of sternum, 2nd to 6th costal cartilages, aponeurosis of external oblique muscle
Greater tubercle of humerus
Lateral anterior thoracic nerve
Pectoralis minor
2nd to 5th ribs
Coracoid process of scapula
Medial anterior thoracic nerve
Deltoid
Lateral half of clavicle, lateral border of acromion process, spine of scapula
Deltoid tuberosity of humerus
Axillary nerve
Serratus anterior (3 parts)
1. 1st and 2nd ribs
Costal surface of scapula at superior angle Vertebral border of scapula Costal surface of scapula at inferior angle
Long thoracic nerve
Injury produces "winged scapula."
The anterior border forms the lateral extent of radical mastectomy; injury results in weakness of rotation and abduction of arm.
2. 2nd to 4th ribs 3. 4th to 8th ribs Latissimus dorsi
Back, to crest of ilium
Crest of lesser tubercle and intertubercular groove of humerus
Thoracodorsal nerve
Subclavius
Junction of 1st rib and its cartilage
Groove of lower surface of clavicle
Subclavian nerve
Subscapularis
Costal surface of scapula
Lesser tubercle of humerus
Subscapular nerve
External oblique aponeurosis
External oblique muscle
Rectus sheath and linea alba, crest of ilium
Rectus abdominis
Ventral surface of 5th to 7th costal cartilages and xiphoid process
Crest and superior ramus of pubis
Clavicular portion of pectoralis forms upper extent of radical mastectomy; lateral border forms medial boundary of modified radical mastectomy; both nerves should be preserved in modified radical procedure.
Subscapular nerve should be spared. Remember the interdigitation with serratus anterior and pectoralis muscles.
Branches of 12th thoracic nerve
The rectus sheath is the lower limit of radical mastectomy.
From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili, 1983, p 42; with permission.
a-
.... ~
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ELLIS et al
BLOOD SUPPLY
The arterial supply of the breast forms a rich anastomotic plexus derived from the internal thoracic, axillary, and intercostal arteries (Fig. 4). The largest vessels supplying the breast arise from the internal thoracic artery via its perforating branches, which pierce the thoracic wall adjacent to the sternal edge in the first to the fourth intercostal spaces. The vessel in the second space is usually the largest of these. A secondary perforating branch is usually found about 2 cm lateral to the main perforating vessel. Thus, the principal vascular supply, both arterial and venous, passes inferiorly and laterally from the upper intercostal spaces, to reach the parenchyma and surrounding tissues superior to a horizontal plane through the nipple. Branches from the axillary artery to the breast include the small supreme thoracic artery, the pectoral branches of the thoracoacromial artery, the lateral thoracic artery, and the subscapular artery, which gives twigs of supply to the lateral aspect of the breast. Small branches of the intercostal arteries in the second, third, and fourth spaces pass to the overlying breast tissue. Venous drainage corresponds to the arteries listed previously, although as with veins everywhere in the body, there are marked anatomic variations. Surgeons who perform a radical mastectomy are well aware
A
B
I c.
Figure 4. Blood supply to the breast. A, The breast may be supplied with blood from the internal thoracic, the axillary, and the intercostal arteries in 18% of individuals. B, The contribution from the axillary artery is negli· gible in 30% of individuals. C, The intercostal arteries contribute little or no blood to the breast in 50% of individuals. Other variations may be found in the remaining 2%. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 43; with permission.)
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of the variable distribution of the tributaries that drain into the axillary vein (Fig. 5). AXILLA
The axilla (Figs. 6 and 7) is a pyramidal space having an apex, a base, and four walls. Its apex is at the junction of the clavicle, the upper border of the scapula, and the first rib. The base is formed by axillary fascia beneath the skin of the axillary fossa. The anterior wall consists of three muscles-the pectoralis major, the pectoralis minor, and the subclavius-together with the fasciae that envelop these muscles and fill the spaces between them. The posterior wall is composed of the scapula and
Sternum
A In!. thoracic v. to right heart . &lungs
Figure 5. Frontal section through the right breast showing pathways of venous drainage. A, Medial drainage through the thoracic vein to the right heart. B, Posterior drainage to vertebral veins. C, Lateral drainage to intercostal vein, superior epigastric veins, and liver. D, Lateral superior drainage through axillary vein to the right heart. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGrawHill Book Company, 1983, p 44; with permission.)
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_Clavi pectoral fascia .... ,.."..,--Axillary a.
Pectoralis major m.
\~hn---
Pectoralis minor m.
Subscapularis
~~--Suspensory
ligament (clavi pectoral fascia) - Teres major
Deep fascia of armpit (axillary) ~~~---
Latissimus dorsi
B .
Serratus anterior
Humerus --4-...f,I~~
Serratus anterior
o
major m.
c Figure 6. The walls of the axilla. A. Anterior wall. B, Posterior wall. C, Medial wall. D, Lateral wall. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili, 1983, P 40; with permission.)
three muscles: the subscapularis, the latissimus dorsi, and the teres major. The medial wall is formed by the lateral chest wall, which includes the second to sixth ribs and the serratus anterior muscle. The lateral wall, the narrowest wall, is formed by the bicipital groove of the humerus. The axilla contains lymph nodes, the axillary sheath, and its contained elements of the brachial plexus of nerves, the tendon of the long head of the biceps brachii, the short head of the biceps, and the coracobrachialis muscles.
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Pectoralis " minor Pectoralis . major
Medial
~~~~~~I-- pectoral n.
Lateral thoracic a.
Th'lrl"'nrlnr~.,,1
n.
Long thoracic n.
Figure 7. Anterior view of the topography of the axilla. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw·Hili Book Company, 1983, p 41; with permission.)
LYMPHATIC DRAINAGE
A plexus of lymphatic vessels lies in the interlobular connective tissue and communicates with a subareolar plexus around the nipple (the subareolar plexus of Sappey). Efferent vessels pass from the breast tissue around the anterior axillary fold to the pectoral (anterior) group of axillary nodes, which lie along the lateral thoracic artery and vein at about the level of attachment of the pectoralis minor to the fifth rib. Some channels pass directly to the subscapular (posterior) group. Efferent vessels drain from the superior aspect of the breast directly to the apical axillary nodes deep to the clavipectoral fascia, just inferior to the clavicle, sometimes interrupted by small interpectoral and infraclavicular nodes. From the medial part of the breast, lymphatics drain along the perforat-
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ing vessels to the internal thoracic chain of nodes. Some drainage occurs along the lateral cutaneous branches of the posterior intercostal veins to the intercostal chain of nodes near the rib heads. About three quarters of all lymphatic drainage of the breast passes to the axillary nodes; the remainder drains principally to the internal thoracic group. Any part of the breast may drain to either group, although there is a greater tendency for tumors in the medial part of the breast to disseminate to the internal thoracic nodes than for growths in the lateral part of the breast. Involvement of the supraclavicular nodes in the spread of breast cancer usually represents retrograde spread along blocked lymphatic channels when the apical nodes are heavily involved. However, efferent channels do pass directly from these nodes to the inferior deep cervical chain, so that involvement of the cervical nodes may occur via this route. Lymphatic do not normally drain to lymphatics across the opposite side of the body. However, in very advanced tumors, extensive blockage of lymphatic channels allows subcutaneous lymphatic permeation to occur to the opposite side. Lymphatic drainage of the breast typically accompanies the blood supply. Drainage from any quadrant of the breast passes to axillary nodes (75%) or to the internal mammary chain (25%), according to Hultborn et al.13 The lymph flow was traced upward and laterally through the tail of the breast to the central lymph nodes by HaagensenP Metastases are most frequently found at this location. Another drainage route follows lymphatics that pierce the pectoralis major and pass upward between the pectoralis major and minor to reach the axillary vein group or the sub clavicular group of nodes. A few interpectoral nodes (of Rotter) may be encountered between the two muscles. The subclavicular group of nodes is important, because Haagensen believes metastasis to these nodes renders surgical cure impossible (Fig. 8). The mortality rates from lesions in different locations in the breast vary greatly despite anatomic evidence. The inner lower quadrant was the least frequently affected, but it had the highest relative mortality in a series of 142 patients recorded by Gray and Skandalakisl l (Fig. 9). Fisher et a19 stated that regional lymph nodes are primary indicators and not instigators of distal disease. They assert that lower axillary dissection is more than adequate to fulfill the aims of axillary node dissection. The qualitative axillary nodal status (positive or negative) can be accurately determined with the removal of a few lymph nodes according to the same authors. Re-examination of surgical specimens taken from 24 radical mastectomies by Skandalakis et aP9 revealed that 19.5% of the lymph nodes removed during surgery escaped examination by the pathologist. In a second group of 20 modified radical mastectomies, re-examination found that 7.7% were not initially removed. In one patient, a malignant node was sectioned only during re-examination. With this in mind, we agree with Stone and Cady,2° who stated that the goals of axillary dissection may be diagnostic or therapeutic. Lymph nodes appear in inconstant groups of varying numbers. This
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Subclavicular (apical) nodes Axillary nodes
/
Central nodes
I
Scapular nodes
\
Ext. mammary (pectoral) nodes
Figure 8. Lymphatic drainage of the breast. (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 45; with permission.)
inconstancy is reflected and perhaps magnified by the inconsistency of the terminology for the lymph nodes as used by various authors. We recommend the terminology of Haagensen et al,l2 Because lymph nodes vary in occurrence and many are very small (Fig. 10), only acute examination will reveal all those present. 19 The major groups of lymph nodes, as described by Haagensen et al/ 2 with the average number of nodes in each, are as follows.
37 ~
A
/ /
//~
13
La!.
Med.
28.6
B
~/
/
1
32.0/
71.5
"-
~"-
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Figure 9. A, Localization of breast tumors in 328 patients. B, Five-year mortality from breast tumors by location (percentage dying < 5 years; 142 patients, all ages). (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 46; with permission.)
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Internal mammary nodes
Axillary vein nodes
Central nodes
External . mammary nodes
Figure 10. Lymph nodes of the breast and axilla. Classification is that of Haagensen et al.'2 (From Skandalakis JE, Gray SW, Rowe JS Jr: Anatomical Complications in General Surgery. New York, McGraw-Hili Book Company, 1983, p 45; with permission.)
Axillary Drainage (35_3 Nodes) Group 1: External mammary nodes (1.7 nodes). These lie under the lateral edge of the pectoralis major, along the medial side of the axilla. They follow the course of the lateral thoracic artery on the chest wall from the second to the sixth rib. Group 2: Scapular nodes (5.8 nodes). These rest on the subscapular vessels and their thoracodorsal branches. Group 3: Central nodes (12.1 nodes). Embedded in fat in the axilla's center, these form the largest group of lymph nodes and are the most easily palpated in the axilla. Group 4: Interpectoral nodes (Rotter's nodes) (1.4 nodes). These are located between the pectoralis major and minor muscles. Often occurring singularly, this is the smallest group of the axillary nodes. The pectoralis major must be removed to access these nodes. Group 5: Axillary vein nodes (10.7 nodes). These extend on the cau-
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dal and ventral surfaces of the lateral part of the axillary vein. This is the second largest of the axillary lymph nodes. Group 6: Subclavian nodes (3.5 nodes). These lie on the caudal and ventral exterior of the medial portion of the axillary vein. They are inaccessible without removal of the pectoralis minor, according to Haagensen et al. 12 However classified by the surgeon, the axillary lymph nodes are defined in three levels according to their location in relation to the pectoralis minor muscle (Fig. 11): Level I: Lymph nodes that are located at the vicinity of the lower border of the pectoralis minor muscle. This level is formed by three groups: exterior mammary lymph nodes, axillary vein lymph nodes, and scapular lymph nodes. Level II: Lymph nodes located deep to (under) the pectoralis minor muscle. This level is formed by central lymph nodes and some subclavian nodes. Level III: Lymph nodes located at the medial bonier of the pectoralis minor. These are the sub clavicular group.
Internal Thoracic (Mammary) Drainage (8.5 Nodes)
Lymphatic vessels arise on the pectoralis fascia on the medial edge of the breast. They accompany the perforating blood vessels and, at the end of the intercostal space, pierce the pectoralis major and intercostal muscles to reach the internal thoracic nodes. Usually located within the
Figure 11. Levels of axillary lymph nodes identified in relation to the pectoralis minor muscle: I = lateral; II = behind; III = medial. (From Wood WC: Definitive surgery for stages I and II breast cancer. In Kennedy BJ (ed): Breast Cancer. New York, Alan R. Liss, Inc., 1989, p 98, copyright © 1989 Wiley-Liss; reprinted by permission of Wiley-Liss, a Division of John Wiley and Sons, Inc.)
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fat and connective tissue of the intercostal spaces, there are usually four to five of these small nodes on each side. Lymphatic trunks to these nodes arise from the liver, diaphragm, rectus sheath, and the upper portion of the rectus abdorninis. 12 The internal thoracic trunks drain into the right lymphatic duct or the thoracic duct. Overall, this is a shorter route than the axillary route to the venous system. Other Nodes
The student of breast anatomy should also remember that there are a few other lymph nodes associated in an indirect way with the breast, such as intercostal lymph nodes, diaphragmatic nodes, and mediastinal nodes. ANATOMIC COMPLICATIONS OF MASTECTOMY
We include the anatomic complications of breast surgery in this presentation to emphasize the anatomic entities with which the surgeon must be familiar during surgery of the breast. Although radical mastectomy rarely is performed, Bland and Copeland l correctly state that radical mastectomy is occasionally necessary to achieve local and regional control of malignancy in the breast, axilla, and chest wall. Skin
The most frequent complication of mastectomy is skin necrosis. To avoid recurrence of malignant disease, all fat and glandular tissue must be removed. Vascular Injury
Sources of bleeding during mastectomy are (1) perforating arteries and veins, especially those of the first and second intercostal vessels, (2) the axillary vein and its tributaries, and (3) the axillary artery and its branches. Coller et a1 5 estimate the average blood loss during radical mastectomy to be 732 mL. The perforating vessels should be ligated, because the first three are too large for cautery. If torn, the axillary vein must also be ligated. Although rare,22 an injury to the axillary artery should be repaired, if necessary, between bulldog clamps. Postoperative edema of the arm frequently follows mastectomy, but functional impairment is less cornmon. Although obstruction to the axillary vein once was considered to be an important factor in edema formation, this has been disproved by subsequent studies. 15,21 Lymphatic
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destruction appears to be the sole cause of edema, which occurs in approximately 50% of patients undergoing radical mastectomy. Organ Injury
Pneumothorax is a danger during ligation of perforating vessels. The surgeon should use curved hemostats and avoid use at right angles. Although the pneumothorax is easily repaired, any contamination of the pleural cavity with malignant cells can prove a delayed disaster. Zintel and Nay22 reported one pneumothorax among 249 consecutive radical mastectomies. Nerve Injury Thoracodorsal Nerve
The thoracodorsal (middle subscapular) nerve arises from the posterior cord of the brachial plexus and innervates the latissimus dorsi muscle (Fig. 12). Although there will be no deformity, internal rotation and adduction of the arm will be weakened if the nerve is cut. The nerve and its associated vessels can best be located near the medial border of the latissimus dorsi about 5 em above a plane passing through the third sternochondral junction. The neurovascular bundle, when found, should be marked with an umbilical tape. Obvious involvement of lymph nodes around the nerve will necessitate the nerve's removal. Long Thoracic Nerve
The long thoracic nerve innervates and lies upon the serratus anterior muscle in the midaxillary line. Section of the nerve results in the "winged scapula" deformity. This nerve should, therefore, be spared unless actually invaded by cancer. The point at which the axillary vein passes over the second rib identifies the nerve's location. Careful dissection of this area will reveal it descending on the second rib posterior to the axillary vein. 8 Anterior Thoracic Nerves
Several authors l6-18 have emphasized the importance of the medial and lateral pectoral nerves. The medial pectoral nerve arises from the medial cord of the brachial plexus, deep to the pectoralis minor. After it receives ~ communication from the lateral pectoral nerve, the medial pectoral nerve passes through the pectoralis minor, supplying it, and then ends within the sternal part of the pectoralis major. The lateral pectoral nerve arises from the lateral cord of the brachial plexus. One branch of this nerve passes directly to the clavicular head of the pecto-
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Upper subscapular n.
Long thoracic
n.
Pectoralis major & minor (cut)
Thoracodorsal n.
Serratus anterior
Subscapularis m.
m.
Medial border of latissimus dorsi m.
A
Retracted axillary margin (pectoralis major minor)
a
B Figure 12. A, The triangular bed of a radical mastectomy. B, The triangular bed of a modified radical mastectomy. The pectoralis muscles are retracted rather than removed. The triangle is slightly smaller than that shown in A. (From Skandalakis LJ, Vohman MD, Skandalakis JE, et al: The axillary lymph nodes in radical and modified radical mastectomy. Am Surg 45:552, 1979; with permission.)
ralis major, which it supplies solely. The remaining part of the lateral pectoral nerve communicates with the medial pectoral nerve. Injury to the lateral pectoral nerve will result in atrophy of the clavicular head of the pectoralis major, with an accompanying severe cosmetic deformity just inferior to the clavicle. Injury to the medial pectoral nerve branches will result in atrophy of the sternal and costal parts of the pectoralis major and the pectoralis minor muscles. The nerves should be removed if the few lymph nodes of the interpectoral group are involved and are fixed with these nerves.
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It is of some importance to plastic surgeons, especially, to know that the nerve supply to the areola and nipple is attributable to the anterior ramus of the lateral cutaneous branch of the fourth thoracic (T4) or intercostal nerve. This branch, which provides sensation for the nipple and areola and motor supply to the smooth muscle of the nipple, passes medially after turning about the lateral border of the pectoralis major muscle, within the superficial fascia. It can be spared in reconstructive procedures, thereby leaving the patient with a sensate and responsive nipple. Brachial Plexus
Most injury to the plexus is the result of stretching the nerves during surgery, although direct injury is possible. Zintel and Nay22 had one patient in a series of 249 mastectomies suffer transient injury to the plexus. THE MALE BREAST
The male breast remains rudimentary in its prepubertal stage, up to which time it is identical with the female breast. It comprises small ducts or cords of cells with scanty supporting fibrous tissues and a variable amount of periductal fat. It is generally stated that the male breast does not extend beyond the areola, although it is well known that male breast tumors may occur from areas outside the diameter of the areola. Carcinoma of the male breast constitutes about 1% of all breast cancers, less than 1.5% of all malignant tumors in men. 3 In a study of 40 cadaveric male breasts, we have shown that the glandular epithelium radiates from the central fibrous nodule to a highly variable extent. 4 In one third of normal specimens, the glandular tissue extended beyond the confines of the pigmented areola. CONCLUSION
This article provides the general and plastic surgeon with knowledge of the surgical embryology and surgical anatomy of the breast and its associated anatomic entities. Careful anatomic technique for the simplest and more radical breast operations will avoid complications and will benefit both the patient and the surgeon. References 1. Bland KI, Copeland EM III (eds): The Breast. Philadelphia, WB Saunders, 1991, p 587 2. Blevins PK: Subcutaneous mastectomy and breast replacement: Its role in the treatment of benign, premalignant, and malignant breast disease. Am Surg 47:281,1981 3. Crichlow RW, Galt SW: Male breast cancer. Surg Clin North Am 70:1165-1177, 1990
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4. Cochrane R, Gee A, Ellis H: Microscopic topography of the male breast. The Breast 1:25-27, 1992 5. Coller FA, Crook CE, lob V: Blood loss in surgical operations. JAMA 126:1, 1944 6. DeCosse JJ: Is the demise of radical mastectomy premature? Surgery 89:398, 1981 7. Donegan WL: General considerations. In Operative Surgery: Principles and Techniques, ed 2. Philadelphia, Lea & Febiger, 1980 8. Feller I, Woodburne RT: The long thoracic and thoracodorsal nerves in radical mastectomy. Surg Gynecol Obstet 107:798, 1958 9. Fisher BN, Wolmark, Bauer M, et al: The accuracy of clinical nodal staging and of limited axillary dissection as a determinant of histologic nodal status in carcinoma of the breast. Surg Gynecol Obstet 152:765, 1981 10. Goldman LD, Goldwyn RM: Some anatomical considerations for subcutaneous mastectomy. Plast Reconstr Surg, 51:501, 1973 11. Gray SW, Skandalakis JE: Embryology for Surgeons, ed 2. Baltimore, Williams & Wilkins, 1993 12. Haagensen CD: Lymphatics of the breast. In Haagensen CD, et al (eds): The Lymphatics in Cancer. Philadelphia, WB Saunders, 1972 13. Hultborn AL, Hulten B, Roos M, et al: Effectiveness of axillary lymph node dissection in modified radical mastectomy with preservation of pectoral muscles. Ann Surg 179:269,1974 14. Kowlessar M, Orti E: Complete breast absence in Siblings. Am J Dis Child 115:91, 1968 15. MacDonald I: Resection of the axillary vein in radical mastectomy: Its relation to the mechanism of lymphedema, Cancer 1:618, 1948 16. Moosman DA: Anatomy of the pectoral nerves and their preservation in modified mastectomy. Am J Surg 139:883,1980 17. Scanlon EF: The importance of the anterior thoracic nerves in modified radical mastectomy. Surg Gynecol Obstet 152:789,1981 18. Scanlon EF, Caprini JA: Modified radical mastectomy. Cancer 35:710, 1975 19. Skandalakis LJ, Vohman MD, Skandalakis JE, et al: The axillary lymph nodes in radical and modified radical mastectomy. Am Surg 45:552,1979 20. Stone MD, Cady B: Techniques of lumpectomy and axillary dissection. Surg Clin North Am 70:885, 1990 21. Watson TA, Bond AF, Phillips AJ: Swelling and dysfunction of the upper limb following radical mastectomy. Surg Gynecol Obstet 116:99, 1963 22. Zintel HA, Nay HR: Postoperative complications of radical mastectomy. Surg Clin North Am 44:313,1964
Address reprint requests to John E. Skandalakis, MD, PhD, FACS Centers for Surgical Anatomy and Technique Emory University School of Medicine 1462 Clifton Road, NE Suite 303 Atlanta, GA 30322