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SURGICAL ANATOMY AND EMBRYOLOGY OF THE ADRENAL GLANDS Claude Avisse, MD, Claude Marcus, MD, Martine Patey, MD, Viviane Ladam-Marcus, MD, Jean-Franqois Delattre, MD, and Jean-Bernard Flament, MD

Each of the two adrenal glands in the body is an anatomic entity. They are suprarenal endocrine viscera, located in the lateral retroperitoneal area and surrounded by perirenal fascia with their corresponding kidneys. Their morphologies are similar from a practical point of view, allowing for macroscopic surgical and radiologic recognition. Their dorsal and lateral anatomic relationships are similar, with a common posterior and lateral approach to adrenalectomy, but the adrenal glands have anatomic duality. Their ventral and medial relationships are different and explain the various anterior approaches to laparotomy and celioscopy. Their blood supplies are different, with some technical differences in vascular exclusion. Each adrenal gland comprises two embryologically and physiologically distinct parts: (1)the cortex, essential to the maintenance of life and producing three steroid hormones, and (2) the medulla, synthesizing catecholamines. Consequently, the adrenal glands may develop two types of disease: (1) tumors of the cortex, which may produce excess hormones, and (2) pheochromocytomas. MORPHOLOGY

Each adrenal gland-triangular on the right, crescent-shaped on the leftcaps the superomedial pole of each kidney. In the lateral retroperitoneal areas, the adrenal glands are located in front of the 12th rib on the right, in front

From the University of Reims (CA, CM, ME VL-M, J-FD, J-BF) and HBpital Robert Debre (CA, CM, VL-M, J-FD, J-BF), Reims, France






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of the 11th and 12th ribs on the left, and on the lateral edge of the vertebral column. The adrenal glands are located in the middle of the abdominal cavity (Fig. 1A). This medial location is true if the various sizes and depths of adipose subcutaneous tissue are not taken into consideration. These factors are important for the choice of surgical approach (Fig. 1B) to adrenalectomy. The cortex is the visible part of the adrenal gland and is distinguished from perirenal fat by its dark-yellow color, finely granular surface, and firm consistency. These macroscopic characteristics are found in cases of small-sized tumors, allowing for visual and tactile identification and prudent traction during adrenalectomy. The medulla is of a dark-red color and friable mass. Sometimes, anatomic sections (Fig. 2) of the medulla on CT scanning show an inverted Y

Figure 1. CT scans of normal adrenal glands (arrows), kidney (K), liver (L), vena cava (V), aorta (A), spleen (S), and pancreas (P). A, Note that the adrenal glands are located in the middle of the abdominal cavity, approximately 10 cm from the anterior and posterior abdominal walls. €IIn , heavy and obese patients, the adrenal gland is nearer the posterior (- 10 cm) rather than the anterior abdominal wall (- 15 cm).



Figure 2. Section of adrenals glands (with their aspect like an inverted Y) and main adrenal vein (arrows). (Courtesy of the Armed Forces Institute of Pathology, Washington, DC.)

(see Fig. 1) orientation. Minimal modifications of this aspect allow for the diagnosis of a small-sized tumor or incidentaloma. Each adrenal gland weighs approximately 6 g, and its average dimensions in adults are approximately 5.0 x 3.0 x 0.6 cm. All of these morphologic data apply to healthy adrenal glands and are sometimes modified by disease, so the surgical and radiologic anatomy of large adrenal tumors is better described by the anatomic relationships visualized on CT scanning or MR imaging.24,12, l 3 RELATIONSHIP OF THE ADRENAL GLANDS WITH THE KIDNEYS

The adrenal glands are embedded in the perirenal fat and enclosed by the renal fascia. The ventral and dorsal layers of the renal fascia extend upward, surround the adrenal glands, and are attached to the diaphragm. A transverse fibrous lamella joins the ventral layer with the dorsal layer of the renal fascia and separates the kidneys and adrenal glands (Fig. 3). This lamella can be divided, which allows for the separate removal of the kidney or adrenalectomy. Some investigators*2believe that the renal fascia is not closed below the kidney, which could explain cases of mobile or ectopic kidneys, although the adrenal gland may be normally located in these cases. In the retroperitoneal area, the adrenal glands are mobile, but they are fixed to the abdominal wall because they are attached to the diaphragm. They move with the diaphragm during the respiration, which explains the occasional diffi-


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Figure 3. Sagittal cross-section of relations with the kidney and dorsal relations of the adrenal gland. Perirenal fascia (1) and its diaphragmatic fixation (2). Latissimus dorsi muscle (3). Posterior and inferior serratus muscle (4). Lumbocostal arch (5). Twelfth subcostal nerve (6). Aponeurosis of the transverse muscle (7).Quadratus lumborum muscle (8).

culty encountered during hemostasis and location of the adrenal glands on CT scanning. They are held in position by the renal fascia, which is attached to the diaphragm, and by large renal veins and DORSAL AND LATERAL RELATIONSHIPS For each adrenal gland, the dorsal and lateral 'relationships are almost identical, so the posterior and lateral approaches (Figs. 3 and 4) to adrenalectomy do not differ significantly. Through the pararenal fat and the perirenal fascia, the adrenal glands are in contact with the superior part of the posterior abdominal wall (Fig. 5). Each gland lies in close proximity to the diaphragmatic crus and to the lateral arcuate ligament (i.e., the lateral lumbocostal arch). These structures separate the adrenal glands from the reflection of the pleura; from the 11th and 12th ribs; and from the subcostal, sacrospinalis, and latissimus dorsi muscles. From the surface to the depth, a posterolateral approach along the 11th or 12th rib includes several steps. First is the incision of the latissimus dorsi muscle on the lateral border of the sacrospinalis muscle and (2) removal of the




Figure 4. Posterior and posterolateral approaches for adrenalectomy.





Figure 5. Transversal cross-section of dorsal relations of the adrenals at the superior part of the abdominal wall. Sacrospinalis ( l ) , subcostal (2),posterior and inferior serratus (3), latissirnus dorsi (4), and transverse (5) muscles. Diaphragmatic crus (6). Posterolateral approach (arrows).


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rib. The incision is extended ventrally by incision of the large muscles. The peritoneum is pushed aside. The lateral border of the diaphragm is divided, and the pleura is freed from the diaphragm, which allows for a direct approach to the adrenal gland by its lateral aspect (see Fig. 5).1,*,4 The adrenal glands are distant from the middle part of the posterior abdominal wall. This muscular part (Fig. 6) is divided during the posterior approach, as popularized by Y o ~ n g . 'The ~ aponeurosis of the latissimus dorsi muscle is vertically incised along the lateral border of the sacrospinalis muscle. Then the aponeurosis of the transverse muscle is opened in the same way along the lateral border of the quadratus lumborum. At the upper part of the incision, the 12th rib is removed, and the pleura is freed from the diaphragm, which can be divided. The 12th subcostal nerve may be preserved to avoid postoperative neuralgia. The kidney may be retracted downward, and the perirenal fascia is opened to bring into view the adrenal gland by its posterior aspect.', 2, 9, lo VENTRAL RELATIONSHIPS

The ventral relationships of the adrenal glands explain the anterior transabdominal approaches by laparotomy or celioscopy.2, The surgical approach on the right side seems easier than that on the left. The ventral aspect of the adrenal glands includes two distinct parts: (1) the ventral and lateral part and (2) the ventral and medial part. The ventral and lateral part is overlapped by the peritoneum between the liver, kidney, and hepatic flexure of the colon. An adequate exposure of the adrenal gland is provided by opening the peritoneum after mobilization of the viscera. The right lobe of the liver (bare area, eighth segment) and the gallbladder are retracted upward, and the hepatic flexure of the colon is retracted downward. The ventral and medial part (Fig. 7) is behind the inferior vena cava, which separates the gland from the epiploic foramen (i.e., Winslow's foramen) at the \




Figure 6. Transverse cross-section of dorsal relations of the adrenals at the middle part of the abdominal wall. Sacrospinalis ( l ) , quadratus lumborum (2),latissimus dorsi (3),and transverse (4) muscles. Posterior approach (arrows).



Figure 7. Sagittal cross-section of ventral relations of the right adrenal gland. Liver (L). Inferior vena cava (IVC). Duodenal loop (D). Pancreatic head (P). Hepatic flexure of the colon (C). Foramen of Winslow (W). Anterior approach (arrows) with Kocher maneuver (arrowheads).

top and from the duodenal loop and pancreatic head further down. The right adrenal vein emerges from here before emptying directly into the inferior vena cava. A descending duodenum with a pancreatic head may be separated from the retroperitoneal structures posteriorly (i.e., Kocher's maneuver), which exposes the underlying vena cava and adrenal vessel^.^," On the right side, when an adrenal tumor is large, a planned thoracoabdominal approach can be used' for vascular control. On the left side (Fig. B), the surgical approach is more difficult. The ventral aspect of the adrenal gland is attached to the viscera of the dorsal mesogastrium3, by the medial border of the spleen and by the body of the pancreas, with the splenic vein behind it and the splenic artery on its superior border. The avascular attachment of the dorsal mesogastrium (Fig. 8A) can be divided, and the spleen, body of the pancreas, and associated vessels are moved from left to right. This is a common approach to the left adrenal gland, especially in cases of large tumors. The body of the pancreas separates the adrenal gland from the lesser sac (i.e., the omental bursa) and from the stomach. A second approach is direct access by the lesser sac after dissection of the gastrocolic ligament. The adrenal gland can be exposed by a peritoneal incision along the inferior or superior border of the pancreatic body, which may be mobilized (see Fig. 8A).


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A Figure 8. A, Transverse cross-section of ventral relations of the left adrenal gland. Stomach (S). Spleen (Sp). Body of the pancreas (P). Omental bursa (B). Anterior approaches by way of the ornental bursa (arrows) by dividing the dorsal rnesogastriurn (arrowheads). lllustration continued on opposite page

The last important relationship is the implantation of the transverse mesocolon along the inferior pancreatic border. Dissection of the transverse mesocolon gives direct access to the posterior side of the pancreas and to the adrenal gland (see Fig. 8B). MEDIAL RELATIONSHIPS

The medial relationships of the adrenal glands are different on each side. The medial borders of the adrenal glands correspond to the inferior vena cava or the abdominal aorta (Fig. 9). On the right side, the adrenal gland is behind the inferior vena cava, and its anterior side (- 3 mm in length) is in close proximity to the lateral border of the cava. By its suprarenal location, the gland keeps aloof from the right renal vein and artery. On the left side, the adrenal gland is located in front of the origin of the celiac trunk but is separated from the aorta by a space of approximately 7 mm. By its prerenal location, the gland is near to the left renal vessels, in the sinus of the kidney.2,4,13 BLOOD SUPPLY, LYMPHATIC DRAINAGE, AND INNERVATION

All of the vessels and nerves form a thick arborization at the periphery of the adrenal glands, fastened in close proximity to the medial retroperitoneal structures (see Fig. 9). The adrenal glands receive their arterial blood from three source^^^^: (1) a superior source, which arises from the inferior phrenic artery;



B Figure 8 (Continued). 6, Sagittal cross-section of ventral relations of the left adrenal gland. Stomach (S). Spleen (Sp). Body of the pancreas (P). Transverse colon (TC). Omental bursa (B). Anterior approaches by way of the omental bursa (arrows) by section of the transverse mesocolon (arrowheads).

( 2 ) a medial source, by the adrenal artery from the abdominal aorta; and (3) an inferior source, by some branches from the renal artery. The cortex and medulla are irrigated by arterial and venous capillaries. Consequently, blood containing steroid hormones passes through the medulla, which could be favorable to the transformation of norepinephrine into epinephrine. The venous return is important physiologically. The arrangement of the adrenal veins is much simpler than that of the arteries. During adrenalectomy for the treatment of tumor with excess hormonal production, especially in cases of pheochromocytomas, the flow of the main adrenal vein can be controlled. On the left side, vascular control of the adrenal vein is easy because the adrenal vein is long (30 mm), empties into the left inferior phrenic vein, and takes an oblique course downward to enter the left renal vein. On the right side, vascular control of the adrenal vein is more difficult. The adrenal vein is much shorter on this side (6 mm) before emptying directly into the posterior part of the inferior vena cava, which presents the risk for injury of the vena cava with disastrous hemorrhage. On each side, numerous accessory adrenal veins, following the arteries, empty into the inferior phrenic, renal vein, or anastomotic exorenal venous arc, in connection with the azygos system and posterior gastric


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Figure 9. A, Blood supply of the right adrenal gland. Inferior phrenic (l), adrenal (2),and renal (3) arteries. Inferior vena cava (IVC). Inferior phrenic (IPV), main adrenal (AV), and right renal (RV) veins. Illustration continued on opposite page

veins.5, These collateral vessels are a caval or portal shunt, and their significant development can occur in cases of large tumors. The adrenal glands are the origin of numerous collecting lymphatic vessels8 that accompany large blood vessels and follow three pathways. On the right side, a first pathway ends in the right lateral aortic nodes, in front of the right crus of the diaphragm and proximal to the celiac trunk. A second pathway also ends in the right lateral aortic nodes, proximal to the junction between the left renal vein and the vena cava. A third pathway ends in the thoracic duct or in the posterior mediastinal nodes after the lymphatic vessels pierce the crura of the diaphragm, which explains the arrival of distant and early metastases of cortical malignant tumors. On the left side, the first two pathways end in the left lateral aortic nodes proximal to the celiac trunk and left renal vein. The third pathway is through the diaphragm, as on the right side. 'This lymphatic drainage is an image of physiologic and embryologic duality. Lymphatic vessels drain the cortex, not the medulla; corticoids can be found in the thoracic duct. The innervation of the adrenal gland^^,^ is of more interest from an anatomic and physiologic standpoint than from a surgical standpoint. During adrenalectomy, nerves and vessels are ligated simultaneously. The nerves are numerous and are derived from the sympathetic visceral nervous system. The visceral afferent fibers arise from the celiac ganglia (semilunar ganglia), which are in connection with the posterior vagus nerve and greater and lesser splanchnic nerves. They traverse the cortex and could give it direct secretory or indirect vasomotor innervation. They end around the cells of the medulla and are



Figure 9 (Continued). 6,Blood supply of the left adrenal gland. Aorta (Ao). Inferior phrenic ( l ) , adrenal (2),and left renal (3) arteries. Left renal (LRV), inferior phrenic (4), main adrenal (5), and gonadic (6) veins.

sympathetic preganglionic fibers. The medulla is a presynaptic sympathetic nerve and belongs to the nervous system, which is well explained by the development of the adrenal glands. DEVELOPMENT The suprarenal glands embryologically comprise two distinct parts4,6-H: (1) the cortex and (2) the medulla (Fig. 10). The cortex is derived from mesoderm and is a groove in the coelom between the base of the mesentery medially and the mesonephros and undifferentiated gonad laterally. This close proximity explains why ectopic cortical tissue has been described to be located below the 6, kidneys and associated with the testes or ~varies.~, The medulla is derived from the ectoderm and is developed from migrating cells of the neural crest. This migration of nervous cells forms the ganglia of the sympathetic trunk and of the sympathetic plexuses. It also forms the paraganglia, which secrete catecholamines (i.e., the chromaffin tissue). The medulla is the most important site of chromaffin tissue and tumors, which arise from adrenal medullary cells and are known as pkeockromocytornas. Usually, the other sites of chromaffin tissue involute progressively but are possible sites of extraadrenal and multiple pheochromocytomas. Zuckerkandl’s organ is a common location for extra-adrenal pheochromocytomas, near the ventral side of the aortic bifurcation. In primitive vertebrates, the cortex and the medulla remain independent. They are fused only in mammals. In humans, the two parts are fused together


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Figure 10. Transverse cross-section of development of the adrenals. Neural tube (1). Chorda (2). Aorta (3).Base of the mesentery (4). Digestive tube (5). Cortex of adrenal gland (6). Undifferentiated gonad (7).Mesonephros (8). From the neural crest (9),a migration of nervous cells (arrows) form the ganglia of sympathetic trunk (A) and sympathetic plexuses (B) and the medulla and paraganglia (C).

but remain distinct, with the macroscopic aspect of ectodermal tissue enclosed by mesoblastic tissue. SUMMARY

Gross anatomy explains the different surgical approaches to adrenalectomy and the difficulties encountered by surgeons during this procedure. Development of the adrenal glands explains the location of the ectopic sites and excess hormone production by adrenal tumors. The choice of a surgical approach is sometimes difficult and is dependent on (1)the morphology of the body; (2) the volume of the tumor, which necessitates immediate vascular control; and (3) the type of disease, which may necessitate a complete exploration of the abdominal cavity. References 1. Chapuis Y Adrenal surgery in 1990. AM Chir 45:5, 1991 2. Chapuis Y, Peix JL: Chirurgie des glandes surrknales. In Arnette (ed): Rapport de I'Association Francaise de Chimrgie. Paris, 1994, pp 1-9



3. Couinaud C: Anatomie de l’abdomen. In Tome 2. Paris, G. Doin, 1963 4. Duclos JM: Chirurgie de la glande surrenale. In Encyclopedic Medico Chirurgicale. Paris, 1992, Techniques Chirurgicales Uro-Gynecologie 41495 5. Gillot C: La veine renale gauche. Etude anatomique, aspects angiographiques, abord chirurgical. Anatomica Clinica 1:135, 1978 6. Giroud A, Lelievre A: In Elements d’Embryologie. Paris, Librairie le Francais, 1971, pp 159-164 7. Hoang C: Anatomie, embryologie et histologie de la surrenale. In Encyclopedic Medico Chirurgicale. Paris, 1996, Endocrinologie-Nutrition 10-014-A-10 8. Hureau J, Hidden G, Ta Thanh Minh A: Vascularisation des glandes surrbnales. Anatomica Clinica 2127, 1979 9. Proye C: La chirurgie des surrknales en 1990. Ann Chir 45:259, 1991 10. Proye C, Huart JY, Cuvilier XD, et al: Safety of the posterior approach in adrenal surgery: Experience in 105 cases. Surgery 114:6, 1993 11. Richelme H, Dor V, Guerinel G: Recherches d’anatomie chirurgicale sur les glandes surrknales. In Puget (ed): Travaux de l’Institut d’Anatomie de la Facult6 Medecine de Marseille. Marseille, 1960 12. Rouviere H: Anatomie descriptive et topographiques. In Abdomen. Paris, Masson, 1974 13. Senecail B, Menanteau B: Anatomical basis for tomographic exploration of the suprarenal glands. Anatomica Clinica 4:93, 1982 14. Young HH: A technique for simultaneous exposure and operation on the adrenals. Surgery, Gynecology, and Obstetrics 62179, 1936

Address reprint requests to Jean-Bernard Flament, MD Department of Digestive Surgery HBpital Robert Debrk Rue du General Koenig 51092 Reims Cedex France