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The Sensitivity of the Nipple-Areola Complex: An Anatomic Study Ingrid Schlenz, M.D., Rafic Kuzbari, M.D., Helmut Gruber, M.D., and Jürgen Holle, M.D. Vienna, Austria far, the 2nd, 3rd, 4th, and 5th1 or the 2nd, 3rd, 4th, 5th, and 6th2 or the 3rd, 4th, and 5th3–5 or the 4th, 5th, and 6th6,7 or only the 4th8 –12 intercostal nerves have been described as supplying nerves to the nipple and areola. The 4th lateral cutaneous branch is unanimously regarded as the most important nerve for the sensitivity of the nipple; however, its course from the point where it perforates the deep fascia in the midaxillary line to the nipple has been described controversially. Some authors describe it as “passing deeply through the breast tissue,”3,5,9,11 some describe a more superficial course close to the skin,1,2,4,8 and others do not give any details about its course at all.6,7,12 These controversial reports might be due to the difficulty in dissecting the thin nerves and to frequent anatomic variations that bias the results if the investigation is carried out only in a small number of cadavers. We undertook this anatomic study to clarify these controversial reports and to enable the preservation of the sensitivity of the nipple and areola during breast surgery. Although preservation of the sensitivity of the nipple and areola is an important goal in breast surgery, only scant and contradictory information about the course and distribution of the supplying nerves is found in the literature. The existing controversy might be due to the difficulty in dissecting the thin nerves and to frequent anatomic variations that bias the results if only a small number of cadavers are dissected. We dissected 28 female cadavers and found that the nipple and areola were always innervated by the lateral and anterior cutaneous branches of the 3rd, 4th, and 5th intercostal nerves. The most constant innervation pattern was by the 4th lateral cutaneous branch (79 percent) and by the 3rd and 4th anterior cutaneous branches (57 percent). The anterior cutaneous branches took a superficial course within the subcutaneous tissue and terminated at the medial areolar border in all dissected breasts. The lateral cutaneous branches took a deep course within the pectoral fascia and reached the nipple from its posterior surface in 93 percent of the dissected breasts. In 7 percent of the dissected breasts, the lateral cutaneous branches took a superficial course within the subcutaneous fat and reached the nipple from the lateral side. These findings suggest that the nerves innervating the nipple and areola are best protected if resections at the base of the breast and skin incisions at the medial areolar border are avoided. (Plast. Reconstr. Surg. 105: 905, 2000.) Preservation of the sensitivity of the nipple and areola is an important goal in breast surgery. Yet, only scant and contradictory information about the course and distribution of the supplying nerves is available in the literature. Although most authors agree that the nipple and areola are innervated by the lateral and anterior cutaneous branches of the intercostal nerves, there is a controversy about which intercostal nerves are involved and which course they take through the breast parenchyma. So MATERIALS AND METHODS Breast specimens of 28 female Caucasian cadavers were examined. Twenty-six cadavers had been embalmed with a mixture of 10% phenol/formaldehyde for 6 weeks before dissection; 2 cadavers were dissected 6 hours postmortem. As the course and distribution of the nerves innervating the nipple-areola complex seem to vary between different individuals1–12 From the Department of Plastic and Reconstructive Surgery at the Wilhelminenspital. Received for publication April 26, 1999; revised August 9, 1999. Presented at the 35th Annual Meeting of the Austrian Society of Plastic, Reconstructive and Aesthetic Surgery in Innsbruck-Igls, Austria, in October of 1997; at the 9th Annual Meeting of the European Association of Plastic Surgeons in Verona, Italy, in May of 1998; and at the 12th Congress of the International Confederation for Plastic, Reconstructive and Aesthetic Surgery, in San Francisco, California, in June of 1999. 905 906 PLASTIC AND RECONSTRUCTIVE SURGERY, and only rarely between the left and right side in the same individual,1 only one breast per cadaver was examined; the left breast was dissected in 24 cadavers, the right breast in 4 cadavers. The right breast was only used when a scar or a hematoma indicated prior surgery of the left breast. The skin was elevated in an area from the clavicle to 3 cm below the inframammary fold from the sternum to the medial rim of the areola and from the midaxillary line to the lateral rim of the areola. Then, the anterior and lateral cutaneous branches of the 2nd, 3rd, 4th, 5th, and 6th intercostal nerves were identified at the points where they perforated the chest wall in the parasternal and midaxillary lines, respectively. The nerves were dissected with magnifying loupes and traced until they entered the nipple or the areola or until they terminated on the surface of the subcutaneous tissue of the breast. In the two fresh cadavers, specimens of the nerves supplying the nipple or areola were taken 1 cm proximal to their entry into the skin of the nipple or areola. These specimens were preserved in 2.5% cacodylate buffer, embedded in epoxy resin, and cut with a microtome. Then, the specimens were examined microscopically; the fascicles were counted, and their diameters were measured. RESULTS We found that in all cadavers the nipple and areola were innervated by both the anterior and lateral cutaneous branches of the 3rd, 4th, or 5th intercostal nerves (Table I). The anterior and lateral cutaneous branches of the 2nd and 6th intercostal nerves innervated breast skin only. The diameter of the lateral cutaneous branches was always bigger than the diameter of the anterior cutaneous branches (m ⫽ 100 ⫾ 10 m versus m ⫽ 20 ⫾ 5 m). In 93 percent of the dissected breasts, the lateral cutaneous nerves pierced the deep fascia in the midaxillary line and took an inferomedial course within the pectoral fascia or the pectoral muscle (one breast). On reaching the midclavicular line, they turned for almost 90 degrees and continued through the glandular tissue toward the posterior surface of the nipple, which they entered with several tiny branches (Figs. 1 and 2). In 7 percent of the breasts, the lateral cutaneous nerves took a superficial course. They ran in the subcutaneous tissue close to the skin and reached the nipple from the lateral side. This course was March 2000 TABLE I Innervation of the Nipple and Areola ACB* Number of Cadavers Side III 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 L R R L L L L L L R L L L L L L R L L L L L L L L L L L xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA IV LCB V III xA xN xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xA xN xA xA xA IV xN xN xN xN xN xN xN xN xN xN xN xN xN xN xN xN* xN* xN xN xN xN xN xN xN xA V xN xN xN xN xN xN ACB, anterior cutaneous branch of the intercostal nerve III, IV, V. LCB, lateral cutaneous branch of the intercostal nerve III, IV, V. A, areola. N, nipple. * Superficial course of the nerve. similar to that of a constant cutaneous branch that terminated in the lateral breast skin after separating from the main stem of the 4th lateral cutaneous branch at the edge of the pectoral muscle (Figs. 1 and 2). The 4th lateral cutaneous branch supplied the nipple in 93 percent of the dissected breasts; in 79 percent it was the only lateral supply to the nipple. The 3rd and 5th lateral cutaneous branches were found to innervate the nipple alone in 3.6 percent and together with the 4th lateral cutaneous nerve in 7.1 percent of the dissected breasts (Table I). When multiple innervation was present, the diameter of the individual nerves was markedly smaller than in those cases where only one supplying nerve was present. In two breasts (7.1 percent), the two lateral cutaneous branches of the 3rd and 4th intercostal nerves formed an anastomosis lateral to the border of the pectoral muscle and supplied the nipple with the resulting single nerve branch. In one breast, the 4th lateral cutaneous branch separated into two smaller branches shortly after giving off the cutaneous branch to the skin. The two Vol. 105, No. 3 / SENSITIVITY OF THE NIPPLE-AREOLA COMPLEX FIG. 1. Lateral view of a left breast. Double arrow, lateral cutaneous branch of the 4th intercostal nerve reaching the posterior surface of the nipple; arrow, cutaneous branch of the lateral cutaneous branch terminating in the skin of the lower lateral quadrant. smaller branches took a parallel course and reached the posterior surface of the nipple within 5 mm of each other. The anterior cutaneous branches contributed to the medial innervation of the nippleareola complex. After piercing the fascia in the parasternal line, they divided into a lateral and a medial branch. Whereas the medial branch crossed the lateral border of the sternum, the lateral branch divided again into several smaller branches that took an inferolateral course through the subcutaneous tissue. They became progressively more superficial along their way and terminated in the breast skin or at the areolar edge. The branches that terminated at the areolar edge originated from the 3rd, 4th, or 5th intercostal nerves; they always reached the areolar edge between 8 and 11 o’clock in the left breast and between 1 and 4 o’clock in the right breast. Innervation by the 3rd and 4th anterior cutaneous branches was found in 57.1 percent and by the 4th and 5th anterior cutaneous branches in 10.7 percent 907 FIG. 2. Schematic drawing of the breast and the anterior (ACB) and lateral cutaneous branches (LCB) of the 4th intercostal nerve innervating the nipple and areola. Modified from Williams, P. L., Warwick, R., Dyson, M., and Bannister, L. H. (Eds.), The Course of a Typical Intercostal Nerve. In Gray’s Anatomy, 37th Ed. New York: Churchill Livingstone, 1989. P. 1138. Reprinted with permission. (Fig. 3). In 28.6 percent of the dissected breasts, only one nerve supplied the nippleareola complex from the medial side (the 3rd anterior cutaneous branch in 21.4 percent and the 4th anterior cutaneous branch in 7.1 percent). In one breast, the 3rd, 4th, and 5th anterior cutaneous branches contributed to the supply of the nipple-areola complex from the medial side (Table I). Again, there was a reciprocal relationship between the number and diameter of the supplying nerves: the more numerous the nerves, the smaller their diameter. DISCUSSION In the past, the innervation of the nipple and areola has received little attention in anatomic 908 PLASTIC AND RECONSTRUCTIVE SURGERY, FIG. 3. Anterior view of a left breast. Arrows, 3rd and 4th anterior cutaneous branch terminating at the medial border of the areola. space also contributed to the innervation of the nipple and areola. The number, distribution, and size of these nerves vary; the smaller the diameter of the nerves, the more numerous they are. We found that the lateral supply to the nipple and areola did not show as many variations as the medial supply (the 4th lateral cutaneous branch innervated the nipple in 93 percent). Because of its size and constancy, it has always been recognized as the most important nerve for the innervation of the nipple1–5,8,9 (its course, however, has been described controversially). We found that in 93 percent of the breasts it took a subglandular course within the pectoral fascia and reached the nipple from its posterior surface—a course that has been described by Craig and Sykes3 and Gonzalez et al.9 In 7 percent of the breasts, however, it took a superficial course close to the skin as described by Cooper,2 Farina et al.,8 and Sarhadi et al.1 Our dissections show that a superficial course of the lateral cutaneous branches is possible, but that a deep course is by far more common; the controversy in the existing literature is probably because of the small number of dissected female cadavers (three to seven).1,3,4,8,9 Montagna and McPherson13 showed in a histologic study that all neural elements are concentrated at the base of the nipple, only few at the side of the nipple, and practically none in the areola. They also found nerves along the major duct system but none in the smaller ducts and concluded that these could only be sensory, as there is no evidence of a motor neural mediation in the mechanism of mammary secretion; this supports the view that the nerves supplying the nipple pass through the gland to the posterior surface of the nipple and are therefore most likely to be injured by resections at the base of the breast. Two studies by Sandsmark et al.14 and Serletti et al.,15 which documented better preservation of the sensitivity of the nipple and areola after inferior pedicle techniques in comparison to superior pedicle techniques, are also in keeping with our findings. A detailed description of the course of the anterior cutaneous branches has been omitted in most of the papers on the innervation of the nipple and areola, and the two existing descriptions are controversial; Craig and Sykes3 describe a deep course and Sarhadi et al.1 a superficial course. We found that the anterior cutaneous descriptions of the breast.6,7 Recent investigations carried out in a small number of cadavers have yielded contradictory results and added to the controversy existing about nipple and areola innervation.1,3,4,8 –10 An exact knowledge of the course and distribution of the nerves innervating the nipple and areola is, however, essential to enable preservation of these nerves during surgery. The present investigation demonstrates that the innervation of the nipple and areola shows frequent variations of the course and distribution of the supplying nerves and helps to explain the previous controversial findings. Only when a large number of cadavers are dissected does it become clear that different types of innervation are possible; it is then that the most constant patterns can be found. The nipple and areola are always innervated by both the anterior and lateral cutaneous branches of the 3rd, 4th, or 5th intercostal nerves; this confirms the results of all other studies except Sarhadi et al.,1 who found that the anterior branch of the 2nd intercostal March 2000 Vol. 105, No. 3 / SENSITIVITY OF THE NIPPLE-AREOLA COMPLEX branches always took a superficial course in the subcutaneous tissue, becoming even more superficial as they approached the areola. Therefore, they are prone to be injured by surgical incisions near the medial areolar edge. In our study, the 3rd anterior cutaneous branch was found to be even more constant (82.1 percent) than the 4th anterior cutaneous branch (78.6 percent). Unlike our findings, Jaspers et al.4 described a medial supply by the 3rd anterior cutaneous branch in only 25 percent, Sarhadi et al.1 in 50 percent, and Craig and Sykes3 did not report any numbers. Because innervation by the 3rd and 4th anterior cutaneous branch seems to be the most common pattern, surgical incisions at the medial areolar edge between 8 and 11 o’clock in the left breast and between 1 and 4 o’clock in the right breast should be avoided whenever possible. In summary, our study shows that the innervation of the nipple and areola is very complex owing to frequent variations of the course and distribution of the supplying nerves. In the 28 cadavers we dissected, the most common pattern was a lateral innervation by the 4th lateral cutaneous branch, which took a “deep” course within the pectoral fascia and reached the nipple from its posterior surface, and a medial innervation by the 3rd and 4th anterior cutaneous branch, which took a “superficial” course within the subcutaneous tissue and reached the medial areolar edge. These nerves are best protected if surgical resections at the base of the breast and skin incisions at the medial edge of the areola are avoided. However, because variations are possible, breast surgery is still associated with the risk of impairing the sensitivity of the nipple and areola. Ingrid Schlenz, M.D. Department of Plastic and Reconstructive Surgery, Wilhelminenspital Montleartstasse 37 A-1171 Vienna, Austria [email protected] 909 REFERENCES 1. Sarhadi, N. S., Dunn, J. S., Lee, F. D., and Soutar, D. S. An anatomical study of the nerve supply of the breast, including the nipple and areola. Br. J. Plast. Surg. 49: 156, 1996. 2. Cooper, A. P. On the Anatomy of the Breast. London: Longman, Orme, Green, Brown and Longmans, 1840. 3. Craig, R. D., and Sykes, P. A. Nipple sensitivity following reduction mammaplasty. Br. J. Plast. Surg. 23: 165, 1970. 4. Jaspars, J. J., Posma, A. N., van Immerseel, A. A., and Gittenberger-de Groot, A. C. The cutaneous innervation of the female breast and nipple-areola complex: Implications for surgery. Br. J. Plast. Surg. 50: 249, 1997. 5. Corriveau, S., and Jacobs, J. S. 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