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Skandalakis' Surgical Anatomy > Chapter 27. Adrenal (Suprarenal) Glands >
HISTORY
The anatomic and surgical history of the adrenal glands is shown in Table 27-1.
Table 27-1. The History of Anatomy and Surgery of the Adrenal Glands
Eustachius
1522
Spigelius
1627
Riolan
1629
Valsalva (16661732)
Argued that the adrenal arteries were ducts running from the "glandula renalis" to the epididymis
Bartholinus
(Bartolin)
1656
Described the adrenals as "capsulae atrabilariae" because he observed that they were filled with black fluid.
This was later misconstrued to mean they were filled with black bile.
Diemerbroek
1694
Winslow
1732
Bordeau
1775
Reported his belief that the adrenals distribute substances into the blood
Schmidt
1785
Stated that the adrenals secreted substances that helped the action of the heart
Reported on the form, color, and weight of the adrenals in 30 species of animals
Cuvier
1805
Studied the adrenals of the human fetus, claiming that they were large during embryological growth
Henle
1843
Stated that the adrenals could be extirpated with impunity "without sensation or motion suffering in the
least"
Ecker
1846
Remak
1847
Addison
1849
&
1855
Described the effects of diseases of the adrenals, including primary adrenocortical insufficiency (Addison's
disease)
Vulpian
1856
Reported that the adrenal medulla developed a green color when in contact with ferric chloride
Brown-Squard
1856
Gerlach and
Welcher
1857
Harley
1858
Used carmine stain to provide a histological description of the adrenals. Stated that the removal of the
adrenals prolonged life in some species.
Henle
1865
Used chromium salts to develop a brown-yellow color in the medulla (thus the term pheochrome, or "dark
color")
Arnold
1866
Presented a classification of the adrenal cortex based on three zonae (glomerulosa, fasciculata, and
reticularis)
Leydig
1866
Claimed that the adrenal gland is part of the nervous system rather than a blood gland, with the medulla
functioning like a nervous ganglion
Frey
1875
Gottschau
1883
Grouped the zona reticularis and the medulla together as the zona consuptiva. Stated that the cells of the
cortex grew inward toward the medulla.
Frankel
1886
Tizzoni
1889
Showed that removing the adrenals caused changes in the brain and in the nervous system
Thorton
1889
Removed a tumor that "reminded the observer of the structure of an adrenal" when studied microscopically
Stilling
1890
Noted that accessory cortical bodies caused differing results after bilateral adrenalectomy
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Stilling
1890
Noted that accessory cortical bodies caused differing results after bilateral adrenalectomy
Oliver and
Schafer
1894- Found that a rise in blood pressure occurred after administration of an extract from the medulla, which they
1895 called adrenalin
Osler
1896
Abel
1897
Referred to Oliver and Schafer's extract called "adrenalin" (see above) as "epinephrine"
Takamine and
Aldrich
1901
Blum
1901
Kohn
1902
Demonstrated that the cells of the adrenal medulla, the carotid body, the abdominal paraganglia, and the
organ of Zuckerkandl contained cells positive to chromaffin; described the "chromaffin system"
Stolz
1904
Pick
1912
Cushing
1912- Described the syndrome of pituitary basophilism (Cushing's syndrome) and connected it with pituitary-adrenal
1932 hyperactivity
Elliot
1913
Described the association of the adrenal medulla with the sympathetic nervous system
Sargent
1914
Rogoff and
Stewart
1921
Vaquez and
Donzelot
1926
Roux
(Switzerland)
1926
Hartman, Dean
and McArthur
1928
Purified adrenocortical extracts and published a paper about this new isolate which prolonged life in
adrenalectomized animals
Pincoffs
1929
Rabin
Crile
1932
Broster
1933
Walters
1934
Kendall
1934
Isolated cortisone
Young
1936
Noted the importance of direct observation of both adrenals. Recommended bilateral subtotal adrenalectomy
to treat bilateral hyperplasia.
Mayo (U.S.)
Holtz, Credner
1945
and Kronenberg
Rediscovered norepinephrine
1945
Huggins and
Scott
1945
Von Euler
1946
Holtz
1947
Langino
1949
Thorn and
Forsham
1949
Wendlet
1950
Synthesized cortisol
Priestley
1951
With his colleagues at the Mayo Clinic, reported 29 patients who underwent subtotal adrenalectomy to treat
Cushing's disease, noting that perioperative cortisol treatment greatly decreased postoperative complications
Patio
1951
Successful transplantation of human fetal adrenal cortical tissue in patient with Addison's disease
Grundy and
Reichstein
1952
Isolated aldosterone
Conn
1955
Liddle
1961
Labeled hydrocortisone as the most important hormone in the adrenal cortex, noting its secretion after ACTH
stimulation
Bartter
1962
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Pearce
1968- Described APUD (amine precursor uptake decarboxylation) system, including cells that produced peptide
1978 hormones of neural crest or neuroectodermal origin
Vingerhoeds et
al.
1976
Viveros et al.
1979
Forest et al.
1982
Madrazo et al.
1987
Counts et al.
1987
Note to readers: We have used the term "adrenal" rather than "suprarenal" in this text because in spoken language such lengthy
terms as "suprarenalectomy" are so cumbersome they are not used.
EMBRYOGENESIS
Normal Development
The adrenal glands form from two separate primordia: the neuroectodermal component develops into the adrenal medulla, and
the mesodermal component becomes the adrenal cortex. The cells of the future medulla are identified by the 21st to the 22nd
day, and are among the wide variety of cells that migrate out of the neural crest (neuroectoderm) in the sixth and seventh
weeks2 (Fig. 27-1). These cells travel along the nerves of the 6th to 12th segments into the developing cortical primordia.
Fig. 27-1.
Formation of neural tube and origin of cells of neural crest from neuroectoderm. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr.
Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)
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Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)
Within the cortical tissue, the migrating cells proliferate and differentiate into chromaffin cells at around the third month of
gestation. This process is not complete until 12 to 18 months after birth. Some cells do not reach the adrenal organs, but
differentiate into chromaffin cells along the aorta. They form nodules of extraadrenal medullary tissue.
The mesodermal component of the cortex is visible as early as the fourth week. The first indication of the cortex is increased
division among the peritoneal epithelial cells of the posterior abdominal wall in the groove between the mesentery and the cranial
end of the mesonephric ridge (Fig. 27-2). From this epithelium, cords of cells invade the mesenchyme, while surface cells form a
cap over the region (Fig. 27-3A). This epithelial cap represents the future zona glomerulosa of the permanent cortex (Fig. 273B). Other derivatives of the neural crest cells such as chromaffin cells of the adrenal medulla and the aortic bodies are shown in
Fig. 27-4 and Table 27-2.
Table 27-2. Derivatives of the Neural Crest Cells
Dorsal root ganglion cells
Sympathetic trunk ganglia
Parasympathetic ganglia
Schwann cells
Ultimobranchial bodies
Epidermal pigment cells
Glial cells of peripheral ganglia (the satellite or capsule cells)
Leptomeninx
Parts of all the cranial nerve ganglia (except olfactory), connective tissue surrounding the eye and the ciliary muscle
All derivatives of the pharyngeal arches (except skeletal muscles), dermis, and hypodermis of the face and neck, and truncoconal
septum (heart outflow tracts)
Fig. 27-2.
Mesothelial cells from mesenteric root differentiate to form cortex. (Modified from Sadler TW. Langman's Medical Embryology (8th ed).
Baltimore: Lippincott, Williams & Wilkins, 2000; with permission.)
Fig. 27-3.
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Migration of neural crest cells into mesodermal components of adrenal gland during the sixth week (A) and seventh week (B).
(Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with
permission.)
Fig. 27-4.
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Derivatives of neural crest. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New
York: McGraw-Hill, 1983; with permission.)
Differentiation of cortical zones begins in the eighth week. The outer layer will become the adult zona glomerulosa. Beneath this
is the proportionally large "fetal cortex" (Fig. 27-5A), which will decrease in relative size and form the zona fasciculata and the
zona reticularis of the adult. These zones may be distinguished at birth (Fig. 27-5B), although they do not appear in the final
adult form until the fourth year of postnatal life (Fig. 27-5C).
Fig. 27-5.
Relative proportions of components of adrenal gland: A, fifth month of gestation; B, at birth; C, adult. (Modified from Skandalakis JE,
Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw Hill, 1983; with permission. Data from Sucheston
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ME, Cannon MS. Development of zonular patterns in the human adrenal gland. J Morphol 1968;126:477.)
In the words of Sucheston and Cannon,3 the adult zones appear to be established by "proliferation of the permanent cortex,
maturation of the fetal cortex and growth of the medulla," and are finally completed by 11 to 15 years of age. However, some
writers disagree with that view, and believe that shortly after birth, the fetal cortex degenerates and is replaced or reorganized,4
or that the fetal zone cells remodel and reduce in size.5
Due to the large size of the fetal cortex, the volume of the adrenal glands of the human fetus is 20 times larger than that of the
adult gland in relation to the weight of the body. The adrenal medulla, however, is small, and enlarges slightly after birth.
At birth, the volume of the adrenals is about 40 ml. Two months after birth, the volume has decreased to about 10 ml, owing to
regression and replacement of the fetal cortex (by whatever means). Growth begins again in the second year of postnatal life
and accelerates after puberty. Final adult size (40 ml) is reached by age 17.6
Bocian-Sobkowska7 studied the adrenal gland in the first postnatal year:
The postnatal decrease in adrenal volume was caused mainly by a rapid fall of fetal zone volume (from 70% to 3% of total
adrenal volume) that can be divided into two phases: rapid phase (from birth to the end of the second week) and a slow
phase from the 3rd week on. Involution was accompanied by increase of zona glomerulosa (from 10% to 25% of total
adrenal volume), zona fasciculata (from 10% to 38%) and zona reticularis volume (from 1% to 23%). During the whole
investigated period the volume of medulla remained constant. The volume fraction of stroma (connective tissue and blood
vessels) was highest at the beginning of the first postnatal week and then decreased rapidly at the end of the 2nd week,
with the most pronounced changes in the fetal zone and medulla.
The adrenal glands maintain their position in the abdomen, neither ascending with the kidney, nor descending with the testis.
Their arterial supply is from segmental mesonephric arteries, greatly altered in their arrangement.
Congenital Anomalies
Congenital anomalies of the adrenal glands are shown in Table 27-3 and Figure 27-6.
Table 27-3. Anomalies of the Adrenal Glands
Anomaly
Agenesis of
the adrenals
4th week
Fusion of the
adrenals
Hypoplasia of
the adrenals
Relative Frequency
Remarks
Uncommon
6th week
None
Male
Rare
Probably late in
gestation
At birth
Male
None
Uncommon
Accessory
4th-6th weeks
adrenal glands
None
Probably
equal
Common
Adrenal gland
hemorrhage
Hypovolemic shock or
corticosteroid
deficiency at birth
At birth
Sex Chiefly
Affected
Modified from Skandalakis JE, Gray SW. Embryology for Surgeons (2nd ed). Baltimore: Williams & Wilkins, 1994, p. 726. Used with
permission.
Fig. 27-6.
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Chief congenital anomalies of adrenal glands. (Modified from Skandalakis JE, Gray SW. Embryology for Surgeons (2nd ed). Baltimore:
Williams & Wilkins, 1994; with permission.)
Adrenal Heterotopia
Occasionally, the adrenal gland is in its normal location but is also beneath the capsule of the kidney (adrenorenal heterotopia) or
that of the liver (adrenohepatic heterotopia) (Fig. 27-7A). Renal tubules or bile ducts may be intermingled with adrenal cells in
the area of fusion of the organs. Such fusion renders adrenalectomy more difficult.
Fig. 27-7.
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Sites of heterotopic adrenal glands and nodules of cortical tissue (A), and chromaffin tissue (B). Masses (colored black) on and near
aorta are retroperitoneal extraadrenal paraganglia. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in
General Surgery. New York: McGraw-Hill, 1983; with permission.)
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Reported locations of adrenocortical and medullary tissue. (Modified from Fonkalsrud EW. The adrenal glands. In: O'Neill JA, Rowe MI,
Grosfeld JL, Fonkalsrud EW, Coran AG (eds). Pediatric Surgery, 5th ed. St. Louis: Mosby, 1998, pp. 1155-1574; with permission.)
Fig. 27-9.
Most frequent location of accessory gland (shaded area) on aorta between celiac and superior mesenteric arteries. (Modified from
Graham LS. Celiac accessory suprarenal glands. Cancer 1953;6:149-152.)
Accessory cortical tissue alone is not rare. Most such cortical nodules are under the renal capsule, in the broad ligament in the
female or in the spermatic cord of the male.12,13 These sites have surgical significance when the suspected lesion is not found
within the substance of the normally situated adrenal glands. All these cortical structures are as susceptible to adenomas as is
the normal adrenal gland (Fig. 27-7A).
Chromaffin tissue distributed around the aorta near the origin of the inferior mesenteric artery, in the lumbar sympathetic chain,
and in and about the celiac plexus is normal (Fig. 27-7B). Such tissue represents chromaffin cells from the neural crest that were
not incorporated into the adrenal medulla. The largest of these are the paraaortic bodies (organs of Zuckerkandl); they regress
in size with age.14
These structures may be sites of pheochromocytomas in childhood. They may also be sites of "nonfunctioning" paragangliomas
with no clinical evidence of hormonal activity.15 Medullary (chromaffin) tissue outside the normal adrenal gland is much more
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Print: Chapter 27. Adrenal (Suprarenal) Glands
with no clinical evidence of hormonal activity.15 Medullary (chromaffin) tissue outside the normal adrenal gland is much more
frequently found than is cortical tissue, and is more frequently associated with hyperfunction than is cortical tissue. O'Riordain et
al.16 studied extraadrenal functional paragangliomas and their locations (Fig. 27-10).
Fig. 27-10.
Anatomic location of extraadrenal tumors. Numbers indicate number of patients with tumors in particular location. (Note: patients with
multiple tumors are counted more than once if they had tumors at different locations.) (Modified from O'Riordain DS, Young WF Jr, Grant
CS, Carney JA, van Heerden JA. Clinical spectrum and outcome of functional extraadrenal paraganglioma. World J Surg 1996;20:916922.)
Pheochromocytoma
Pheochromocytoma is a benign or malignant medullary tumor. "Functioning" tumors produce catecholamines, either epinephrine,
norepinephrine, or both. Hypertension, tachycardia, sudoresis, and anxiety reaction result from the hormonal excess.17
Lo et al.18 stated that "[a]drenal pheochromocytoma is potentially lethal if undetected and is associated with long-term
morbidity." They cited the results of studies in which pheochromocytoma was diagnosed in 4 of 8486 autopsies (0.05%); in 3 of
these cases, it was the immediate cause of death.
Ito et al.19 stated that parenchymal degeneration of pheochromocytomas produces paroxysmal hypertension in most cases.
Pheochromocytoma is a rare tumor that is found in only 0.1% of patients with diastolic hypertension, according to Favia et al.20
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Pheochromocytoma is a rare tumor that is found in only 0.1% of patients with diastolic hypertension, according to Favia et al.20
They presented 55 patients with pheochromocytoma as a rare cause of hypertension.
Neuroblastoma
Neuroblastoma is the second most common tumor of infancy, and the most common abdominal tumor of infancy. Fifty percent of
the tumors originate in the adrenal gland; the remainder originate in the sympathetic chain. Genetic basis, autosomal dominance,
autosomal recessive inheritance patterns, and chromosomal abnormalities are probably all responsible for the genesis of
neuroblastoma.
We quote Alexander22:
Neuroblastoma is a malignant tumor of neural crest origin that may arise anywhere along the sympathetic ganglia or within
the adrenal medulla. The median age of diagnosis is 2 years; however occurrence is skewed toward younger children, with
nearly 35% of cases occurring under 1 year of age and the remainder under 10 years of age. Seventy-five percent of
neuroblastomas originate within the abdomen or pelvis, and half of these occur within the adrenal medulla, whereas 20%
originate within the posterior mediastinum and 5% within the neck.
Adrenal Cyst
Dermoid cyst of the adrenal gland has been reported.23
SURGICAL ANATOMY
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reported in the literature. A knowledge of these variations is very important in diagnosis of abnormalities of the [adrenal] gland,
of which tumoral enlargement is rather common."
Relations
Each adrenal gland has only an anterior and posterior surface. Their relationships to other structures are as follows: (Figs. 27-11
and 27-12)
Right adrenal gland:
Anterior surface:
Superior: "bare area" of the liver
Medial: inferior vena cava
Lateral: "bare area" of the right lobe of the liver
Inferior: peritoneum (very rarely, if ever) and first part of the duodenum (occasionally)
Posterior surface:
Superior: diaphragm
Inferior: anteromedial aspect of the right kidney
Left adrenal gland:
Anterior surface:
Superior: peritoneum (posterior wall of the omental bursa) and the stomach
Inferior: body of the pancreas
Posterior surface:
Medial: left crus of the diaphragm
Lateral: medial aspect of the left kidney
Fig. 27-11
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. Relations of adrenal glands from anterior approach. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in
General Surgery. New York: McGraw-Hill, 1983; with permission.)
Fig. 27-12.
Anatomy of adrenal glands. Ao, Aorta (Modified from Hughes S, Lynn J. Surgical anatomy and surgery of the suprarenal glands. In:
Lynn J, Bloom SR (eds). Surgical Endocrinology. Oxford: Butterworth Heinemann, 1993, pp. 458-467; with permission.)
The medial borders of the right and left adrenal glands are about 4.5 cm apart. In this space, from right to left, are the inferior
vena cava, the right crus of the diaphragm, part of the celiac ganglion, the celiac trunk, the superior mesenteric artery, the
other part of the celiac ganglion, and the left crus of the diaphragm.
Remember
The right adrenal gland is located posterior to the duodenum and the right lobe of the liver.
In many cases, the medial part of the right adrenal gland is related to the inferior vena cava.
The right adrenal gland may be closely related to the right hepatic vein as it passes to drain into the inferior vena cava.
The right adrenal vein is short, and is difficult to ligate.
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The right adrenal gland is anterior to the diaphragmatic and pleural reflections.
The left adrenal gland is located posterior to the stomach and pancreas and medial to the splenic porta.
The left adrenal gland is located in front of the reflections of the diaphragm and the pleura.
The left adrenal gland is related to the medial aspect of the upper pole of the left kidney, occasionally extending to the left renal
porta.
Adrenal Zones
The outer portion of the adrenal gland, the adrenal cortex, is composed of three zonae: glomerulosa, fasciculata, and reticularis.
The innermost region of the adrenal gland is the medulla. Figs. 27-4 and 27-7 demonstrate chromaffin cells of the adrenal medulla
and of heterotopic adrenal glands.
To help the student remember the layers of the adrenal gland, every year in our clinical and surgical anatomy classes we repeat
the mnemonic "Good For Reason Mother" (Fig. 27-13). Another mnemonic device which is currently popular with medical students
relates the architecture of the cortical region of the adrenal gland and its regulatory functions: Great fat rats: salt, sugar, sex.
Fig. 27-13.
Summary of embryology, anatomy, physiology, and pathology of adrenal glands. (Modified from Skandalakis JE, Gray SW. Embryology
for Surgeons (2nd ed). Baltimore: Williams & Wilkins, 1994.)
Vascular Supply
Arterial Supply
The adrenal glands and the thyroid gland are the viscera having the greatest blood supply per gram of tissue. As many as 60
arterial twigs may enter the adrenal gland. The arterial supply of the adrenal glands arises, in most cases, from three sources
(Fig. 27-14):
The superior adrenal arteries. A group of six to eight arteries arises separately from the inferior phrenic arteries. One artery may be
larger than the others, or all may be of similar size.
The middle adrenal artery arises from the aorta just proximal to the origin of the renal artery. It can be single, multiple, or absent. It
supplies the perirenal fat only.
One or more inferior adrenal arteries arise from the renal artery, an accessory renal artery, or a superior polar artery. Small twigs may
arise from the upper ureteric artery.
Fig. 27-14.
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Fig. 27-14.
Arterial supply and venous drainage of adrenal glands. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in
General Surgery. New York: McGraw-Hill, 1983; with permission.)
All these arteries branch freely before entering the adrenal gland, so 50-60 arteries penetrate the capsule over the entire
surface.28 It is possible that this branching of arteries before entering the adult adrenal gland indicates the outline of the surface
of the much larger gland of the embryonic period, when the fetal cortex was present.
The sources of arterial supply to the adrenal gland are subject to variation.29-31 In 61 percent of individuals, the supply by
middle or inferior adrenal arteries may be lacking; the superior adrenals are absent in only about 2 percent of cases. In about 5
percent of individuals, the arterial supply is derived wholly from one source a singular vessel supplying the superior, middle,
and inferior branches.
Venous Drainage
The adrenal venous drainage does not accompany the arterial supply, and is much simpler (Fig. 27-14). A single vein drains the
adrenal gland, emerging at the hilum. The left vein passes downward over the anterior surface of the gland. This vein is joined by
the left inferior phrenic vein before entering the left renal vein.
The right vein is typically very short; it may be 0.5 cm long, or even less. The right adrenal vein passes obliquely to open into
the posterior side of the inferior vena cava. The right adrenal vein does not usually have any tributaries other than from the
adrenal gland. If the adrenal gland must be mobilized or removed, it is wise to ligate the right adrenal vein first, then divide and
ligate the arteries later, because the right vein is so easily torn from the inferior vena cava.
The right adrenal vein may drain into the right hepatic vein, close to the junction of the hepatic vein with the inferior vena
cava.32 Occasionally there are two veins: one having a normal course, and an accessory vein entering the inferior phrenic
vein.33 In his 40 years in the dissecting room, the senior author of this chapter (JES) has encountered accessory veins several
times. Some variations of the venous drainage are shown in Fig. 27-15.
Fig. 27-15.
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Venous drainage of adrenals. HV, hepatic vein; Rt. RV, right renal vein; Inf. VC, inferior vena cava; TV, testicular vein; Lt. RV, left renal
vein; OV, ovarian vein; Sp. V, suprarenal vein. (Modified from Johnstone FRC. The surgical anatomy of the suprarenal glands with
particular reference to the suprarenal vein. Surg Clin North Am 1964;44: 1315-1385; with permission.)
When using the posterior approach to the adrenal gland, the left adrenal vein is found on the anterior surface of the gland. The
right adrenal vein is found between the inferior vena cava and the gland. Careful mobilization of the gland is necessary for good
ligation of the vein.
In the early studies of Dobbie and Symington,34 it was observed that the adrenal gland appeared to be divisible into three
regions: the head, the body, and the tail. The head region, in which the medullary tissue was most prominent, was that part
closest to the emergence of the adrenal vein from the gland. The tail, where medulla was almost absent, was the most lateral
part. The ventral surface of the gland was characterized by an anterior groove. The dorsal surface possessed a ridgelike
elevation, the crest, which increased in prominence near the lateral tip of the gland. The crest is flanked by two alar parts.
The central adrenal vein carries with it a cuff of cortical tissue into the substance of the gland. The vein is characterized by
unique longitudinal muscle fibers, especially thick on its dorsal surface, which may be related to effective closure of its tributaries
upon contraction. Shortly after entering the adrenal gland, the central vein receives a large muscular branch which curves
backwards and drains the head of the gland. Several other main tributaries enter the main vein from the body and tail region.
In the studies of Monkhouse and Khalique,35 in almost all cases venous interconnections were found between the adrenal venous
system and the azygos, hemiazygos, and lumbar veins, in addition to accessory connections with the renal veins. The study was
initiated by the finding (in a patient with a left-sided pheochromocytoma) of high levels of catecholamines in the superior vena
cava and right atrium, rather than in the inferior vena cava, as one would normally expect.
Lymphatic Drainage
The lymphatics of the adrenal gland are usually said to consist of a profuse subcapsular plexus that drains with the arteries and
a medullary plexus that drains with the adrenal veins. Merklin36 could find no evidence of lymphatic vessels within the
parenchyma of the adrenal glands.
Drainage is to renal hilar nodes, lateral aortic nodes, and to nodes of the posterior mediastinum above the diaphragm by way of
the diaphragmatic orifices for the splanchnic nerves (Fig. 27-16). Rouvire37 stated that lymphatics from the upper pole of the
right adrenal gland may enter the liver. The majority of capsular lymphatic vessels pass directly to the thoracic duct without the
intervention of lymph nodes.36
Fig. 27-16.
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Lymphatics of adrenal glands. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New
York: McGraw-Hill, 1983; with permission.)
Innervation
The adrenal cortex appears to have only vasomotor innervation. Most of the fibers reaching the gland from the splanchnic
nerves, the lumbar sympathetic chain, the celiac ganglion, and the celiac plexus enter the medulla (Fig. 27-17). These fibers are
preganglionic 38 and end on the medullary chromaffin cells. This arrangement is not as anomalous as it might appear; chromaffin
cells arise from the same embryonic source as do the postganglionic neurons elsewhere. Most of these preganglionic fibers in
humans are nonmyelinated.39
Fig. 27-17.
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Nerve supply to adrenal glands. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New
York: McGraw-Hill, 1983; with permission.)
HISTOLOGY
Adrenal Cortex
The vascularity of the adrenal cortex is among the greatest in the entire body. The adrenal cortex is composed of three zones:
the zona glomerulosa, the zona fasciculata, and the zona reticularis. In all three zones, all cells produce steroids.
In the zona glomerulosa (the outermost layer), small cells are arranged in roughly spherical groups. This zone secretes the
mineralocorticoid aldosterone.
In the zona fasciculata, larger cells are arranged in columns which are oriented radially. The carbohydrate-active steroid,
cortisol, and the adrenal sex steroids are produced here. Vitamin C is abundant in these cells.
In the third layer, the zona reticularis, small cells are arranged in strands forming an irregular network. These cells secrete
cortisol, androgens, and estrogens. Cholesterol is present as a precursor to the genesis of the steroids.
Adrenal Medulla
The cells in the adrenal medulla are large and pale. They secrete epinephrine and have a chromaffin reaction. These cells are
called chromaffin cells, or pheochromocytes. Distributed throughout the medulla, but few in number, are postganglionic
sympathetic neurons.
Most medullary cells secrete epinephrine, but some secrete norepinephrine instead.
An abundance of round or oval secretory granules is located within the cellular cytoplasm of the adrenal medulla.
PHYSIOLOGY
As mentioned above, the following corticosteroid hormones are secreted by the adrenal cortex:40
aldosterone (in the zona glomerulosa)
cortisol
carbohydrate-active cortisol and androgens (in the zonae fasciculata and reticularis)
Secretion of aldosterone is controlled by angiotensin II, serum potassium, and the adrenocorticotropic hormone (ACTH) (Fig. 2718).
Fig. 27-18.
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Relations of renin, angiotensin I, angiotensin II, and their anatomic sites of production and enzymatic conversion. ACTH,
adrenocorticotropic hormone. (Modified from Newsome HH. Suprarenal glands. In: Greenfield LJ (ed). Surgery: Scientific Principles and
Practice. Philadelphia: JB Lippincott, 1993, pp. 1209-1223; with permission.)
Cortisol secretion is controlled by ACTH from the anterior pituitary gland (Fig. 27-19).
Fig. 27-19.
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Feedback relations between adrenal gland, hypothalamus, and anterior pituitary. CRH, corticotropin-releasing hormone; ACTH,
adrenocorticotropic hormone. (Modified from Newsome HH. Suprarenal glands. In: Greenfield LJ (ed). Surgery: Scientific Principles and
Practice. Philadelphia: JB Lippincott, 1993, pp. 1209-1223; with permission.)
An excess of androgenic sex steroids almost always arises from carcinoma. Enzymatic defects (Fig. 27-20) are responsible for
congenital adrenal hyperplasia with sexual ambiguity.41 By blocking the adrenal production of cortisol, the defects result in the
loss of negative feedback to the hypothalamus. There is continued stimulation and excess production of androgens and possibly
mineralocorticoids. The result is congenital adrenal hyperplasia syndrome. The most common enzymatic deficiencies are 21hydroxylase, 11- -hydroxylase and 3- -hydroxysteroid dehydrogenase.
Fig. 27-20.
Adrenal production of cortisol blocked by heritable enzymatic defects. CRH, corticotropin-releasing hormone; ACTH, adrenocorticotropic
hormone. (Modified from Newsome HH. Suprarenal glands. In: Greenfield LJ (ed). Surgery: Scientific Principles and Practice.
Philadelphia: JB Lippincott, 1993, pp. 1209-1223; with permission.)
In the adrenal medulla, sympathetic stimulation is responsible for the secretion of epinephrine and norepinephrine.
An excellent paper by Hiatt and Hiatt 42 presents the triumphal conquest of Addison's disease. It includes the discovery of the
glands, identification of their hormonal products, use of the hormones for therapy, and biosynthesis for pharmacologic
applications. We recommend it to all our readers.
Ito et al.43 reported that the assay for urine metanephrine and normetanephrine is an effective test for the diagnosis of
pheochromocytoma and management of incidentaloma.
We present Del Rio44 verbatim:
The sympathoadrenal system (SAS) represents a major contributor to body homeostasis, regulating blood pressure, heart
rate, energy balance and inter-mediary metabolism. Thus, it is not unexpected that in the last decades a consistent
literature has been focused on the possible role of the sympathoadrenal system in the pathogenesis of human obesity.
There are, however, many factors confounding a compar-ison of sympathoadrenal system activity between lean and
obese subjects. Among these, one should be aware that SAS should be functionally separated into sympathetic nervous
system (SNS) and adrenal medulla (AM), and that each of these two systems can be activated independently from the
other by distinct physiological stimuli; this phenomenon in fact underlies the discordant pattern of findings for
adrenomedullary and sympathetic activity in human obesity. While, in fact, obese subjects often display an increased
basal SNS activity, there are numerous reports of blunted AM function in the obese. Recent evidence suggests that this
reduced adrenaline secretion is an acquired feature of human obesity, a finding that fits in well with the hypothesis that
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reduced adrenaline secretion is an acquired feature of human obesity, a finding that fits in well with the hypothesis that
the hormonal milieu, particularly sex steroids and cortisol, plays a role in the determination of blunted AM activity.
Catecholamines have been recently demonstrated to play a role also in the regulation of the whole energy balance.
Adrenaline in fact acutely reduces both leptin mRNA as well as circulating leptin in human obese subjects, suggesting that
catecholamines may influence the cross-talk between energy stores and the centrally mediated modulation of food intake.
SURGICAL APPLICATIONS
...it should be recognized that the surgical approach and exposure to the suprarenal gland will be tailored to the underlying
disease process...Richard Bihrie and John P. Donahue45
Surgery is the treatment of choice for all benign functioning or malignant adrenal tumors. Stratakis and Chrousos46 summarized
several studies of adrenal cancer, which showed these neoplasias accounting for 0.05-0.2% of all cancers and occurring at
every age:
A bimodal age distribution has been reported, with the first peak occurring before the age of 5 years and the second in
the fourth to fifth decade. In all published series, females predominate, accounting for 65% to 90% of the reported cases.
Several studies have shown a left-sided prevalence in adrenal cancer, whereas others have reported a right-sided
preponderance. In approximately 2% to 10% of patients, adrenal cancer is found bilaterally.
Khorram-Manesh et al.47 reported the rarity of adrenocortical carcinoma and the need for better treatment alternatives. Though
surgery is the treatment of choice, its role in advanced disease has been questioned.
Cook and Christie48 reminded us that a unilateral adrenal mass may be secondary to Mycobacterium kansasii in patients with
AIDS. The only conservative treatment applies to congenital adrenal hyperplasia with adrenal hyperfunction syndromes.
The adrenal glands may be approached by three open methods. These are: anterior, posterior, and lateral (transthoracic).
Harrison et al.49 reported that the prognosis of adrenocortical carcinomas after curative resection depends on tumor size,
hemorrhage, and mitotic count.
Paul et al.50 advocated adrenalectomy for isolated adrenal metastases for selected patients presenting with long disease-free
intervals and favorable tumor biology. Tsui et al.51 provided a thoughtful analysis of the role of adrenalectomy in radical
nephrectomy:
With a low incidence of 0.6%, adrenal involvement is not likely in patients with localized, early stage renal cancer cell
carcinoma and adrenalectomy is unnecessary, particularly when CT is negative. In contrast, the 8.1% incidence of adrenal
involvement with advanced renal cell carcinoma supports the need for adrenalectomy. Careful review of preoperative
imaging is required to determine the need for adrenalectomy in patients at increased risk with high stage lesions, renal vein
thrombus and upper pole or multifocal intrarenal tumors. With a negative predictive value of 99.4%, negative CT should
decrease the need for adrenalectomy. In contrast, positive findings are less reliable...[and] may not necessarily indicate
adrenalectomy....
The anterior approach has the advantage of enabling the surgeon to inspect, palpate, and biopsy both glands. The incision
chosen for an anterior approach may be vertical, midline or paramedian, transverse, or chevron. The chevron transabdominal
incision provides bilateral exposure (Fig. 27-21).
Fig. 27-21.
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Incisions for anterior exposure of adrenal glands. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in
General Surgery. New York: McGraw-Hill, 1983; with permission.)
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Incision of parietal peritoneum lateral to left colon. Incision divides splenorenal ligament. (Modified from Skandalakis JE, Gray SW, Rowe
JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)
Another approach to the left adrenal gland is by opening the lesser sac through the gastrocolic omentum, which may be incised
longitudinally outside the gastroepiploic arcade (Fig. 27-23). In this approach, care must be taken to avoid traction on the
spleen or the splenocolic ligament. The ligament may contain tortuous or aberrant inferior polar renal vessels or a left
gastroepiploic artery.
Fig. 27-23.
Approach to the left adrenal through the gastrocolic omentum by opening the lesser sac. (Modified from Skandalakis JE, Gray SW,
Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)
Following either approach, the peritoneum under the lower border of the pancreas should be incised halfway along the tail; the
incision should be extended laterally for about 10 cm. The pancreas can be gently retracted upward, avoiding injury. This
maneuver will expose the left adrenal gland on the superior pole of the left kidney; both the gland and the kidney are covered
with renal fascia (of Gerota). The adrenal gland will be lateral to the aorta, about 2 cm cranial to the left renal vein. Incision of
the renal fascia exposes the adrenal gland completely, and permits access to the adrenal vein. If the operation is for
pheochromocytoma, the adrenal vein should be ligated at once to prevent the release of catecholamines into the circulation
during subsequent manipulation of the gland.
A retractor must be placed gently to avoid tearing the inferior mesenteric vein from the splenic vein. Although the inferior
mesenteric vein may be ligated without sequelae, it is prudent to refrain from the use of retractors in this area if possible.
A third approach, useful in patients whose left adrenal lesion is anterior, is exposure of the gland by an oblique incision of the left
mesocolon (Fig. 27-24). The arcuate vessels can be divided and the marginal artery can be sectioned, but the major branches of
the middle and left colic arteries must be preserved. Care to avoid excessive retraction will prevent injury to the wall of the left
colon.
Fig. 27-24.
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Approach to the adrenal by incision of the left mesocolon near the splenic flexure. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr.
Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)
In some lesions, such as primary aldosteronism, the adrenal gland is hypervascular and friable; meticulous attention to
hemostasis is essential. Adenoma can be disguised or mimicked by hematomas from operative trauma.53 The surgeon can use a
part of the adjacent periadrenal fascia to handle the gland. Manipulation should be with fine forceps only. Hemostasis from the
numerous arteries can be maintained by clips, ligatures, or by electrocoagulation.
Dissection should start at the inferolateral aspect of the left adrenal gland and should proceed superiorly (Fig. 27-25). The
surgeon should keep in mind the possible presence of a superior renal polar artery. The gland can be retracted superiorly.
Remember that the left adrenal gland extends downward, close to the left renal artery and vein.
Fig. 27-25.
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The left adrenal gland exposed by an upward dissection. Note position of left adrenal vein. (Modified from Skandalakis JE, Gray SW,
Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)
After removal of the adrenal gland, its bed should be inspected for bleeding points. Surrounding organs, especially the spleen,
should be inspected for injury. Splenic injury can be repaired with sutures over a piece of retroperitoneal fat, Gelfoam, or
Avitene. More severe injury may require partial or even total splenectomy.
Right adrenal gland and upper pole of right kidney are exposed following Kocher maneuver. Note position of right adrenal vein.
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Right adrenal gland and upper pole of right kidney are exposed following Kocher maneuver. Note position of right adrenal vein.
(Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw- Hill, 1983; with
permission.)
Unlike the left adrenal gland, the right gland rarely extends downward to the renal pedicle. The right adrenal vein usually leaves
the gland on its anterior surface close to the cranial margin, and enters the vena cava on its posterior surface (Fig. 27-26). To
prevent the release of catecholamines and to avoid stretching the vein, hemostatic clips should be placed as soon as both
borders of the vein are visible. Stretching the vein invites hemorrhage from the vena cava.
Tominaga et al.54 advised resection of pheochromocytoma by completely isolating the IVC and using extracorporeal charcoal
hemoperfusion, thereby preventing systemic distribution of catecholamines during manipulation of the tumor.
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Incisions for posterior approach to adrenal glands. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in
General Surgery. New York: McGraw- Hill, 1983; with permission.)
The erector spinae muscle attachments to the dorsal aspect of the 12th rib should be detached, exposing the rib. The rib must
be removed subperiosteally to avoid damaging the underlying pleura. Periosteum should be stripped on the superior surface from
medial to lateral and on the inferior surface from lateral to medial. Avoid injury to the 12th intercostal nerve bundle at the inferior
angle of the rib. The nerve is separate from, but parallel with, the blood vessels. The vessels can be ligated if necessary.
The pleura must be separated from the upper surface of the diaphragm, and the diaphragm should be incised from lateral to
medial. The fascia can be opened, and the upper pole of the kidney identified. Inferior retraction of the kidney will usually bring
the adrenal gland into the field. Care must be taken to avoid tearing the renal capsule or stretching a possible superior polar
artery.
Dissection of the left adrenal gland should begin on the medial aspect, with clips for the arteries encountered. Remember that
the pancreas lies just beneath the gland; it is easily injured. In this approach, the last step is to identify the left adrenal vein,
which usually emerges from the medial aspect of the gland and courses obliquely downward to enter the left renal vein. Undue
traction on the gland can tear the renal vein.
The right adrenal gland is approached by retracting the superior pole of the right kidney inferiorly; the posterior surface of the
adrenal gland can then be dissected free from fatty tissue. The liver must be retracted upward as the apex of the gland is
reached. The lateral borders are freed up, leaving only the medial margins attached.
The right adrenal gland should be retracted laterally. Branches from the inferior phrenic artery, aorta, and right renal artery to
the gland should be ligated. The right adrenal vein, also, should be ligated (Fig. 27-26). We recommend freeing the vena cava far
enough to ensure room for an angle clamp should hemorrhage from the vena cava or the adrenal vein require it. After removing
the gland, carefully inspect for air leaks and bleeding before closing the incision.
Incision for thoracoabdominal approach to adrenal gland. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications
in General Surgery. New York: McGraw- Hill, 1983; with permission.)
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LAPAROSCOPIC ADRENALECTOMY
Laparoscopic adrenalectomy may be performed by a lateral transabdominal or a posterior retroperitoneal approach. Duh et al.60
reported that both methods are safe. They used the posterior approach for bilateral tumors; for tumors of more than 6 cm, the
lateral approach was preferable. Walz et al.61 supported the posterior retroperitoneoscopic approach for adrenalectomy.
Imai et al.62 stated that laparoscopic transperitoneal lateral adrenalectomy is the technique of choice for removing functioning
adenomas and adrenal masses less than 6 cm in diameter. They reported that patients undergoing the laparoscopic procedure
experience greater comfort, less blood loss, and shorter hospital stays with no increase in cost.
Thompson et al.63 found transabdominal laparoscopic adrenalectomy preferable to open posterior adrenalectomy, despite its
greater expense. They reported improved patient comfort and satisfaction, and "dramatically" fewer complications. Rutherford et
al.64 presented 67 successful adrenalectomies employing the unilateral transabdominal approach; postoperative bleeding
occurred in 1.5% of cases, as did port site herniation.
Basso et al.65 advised that laparoscopic supragastric approach for left adrenalectomy gives a good visualization of the left
adrenal, avoiding anatomic complications during mobilization of the spleen, pancreatic tail, and splenic flexure of the colon. Good
visualization of the left adrenal vein is also accomplished.
Horgan et al.66 found laparoscopic adrenalectomy safe and effective for benign adrenal tumors. Jossart et al.67 stated
"Laparoscopic adrenalectomy can now be considered the standard of care for most adrenal neoplasms." Using data on
pheochromocytoma surgery, Fernndez-Cruz et al.68 reached the same conclusion. Walther et al.69 reported the following:
"Laparoscopic partial adrenalectomy is technically feasible in patients with a hereditary form of pheochromocytoma, and may
preserve adrenocortical function. Laparoscopic ultrasound was necessary to identify 2 of the seven pheochromocytomas
removed."
Shen et al.70 advised laparoscopic adrenalectomy for patients with primary hyperaldosteronism. The authors report that this
laparoscopic procedure yields similar results with respect to blood pressure and hypokalemia and is accompanied by lower
morbidity than the open procedure. Patients with less severe hypertension and hypokalemia are now undergoing this procedure.
A seven-year study of laparoscopic adrenalectomies by Brunt et al.71 concluded the following:
Laparoscopic adrenalectomy is a safe and effective procedure and has several advantages over open adrenalectomy.
Laparoscopic adrenalectomy should become the preferred operative approach for the treatment of patients with small,
benign adrenal neoplasms.
In commentary on the Washington University findings, Prinz72 wisely stated that adrenal glands should be removed in toto with
their capsule intact. Prinz agreed with Brunt and colleagues that increased tumor size greatly decreased the advisability of
laparoscopy. Siperstein et al.73 stated that laparoscopic posterior adrenalectomy should be considered in patients with tumors
less than 6 cm. Staren and Prinz74 concluded that more than 60 percent of surgically treatable adrenal disease may be
approached laparoscopically.
Walz et al.75 stated that in selected cases subtotal adrenalectomy via posterior approach retroperitoneoscopically is a safe
procedure.
Kollmorgen et al.76 compared acute-phase response and wound healing in laparoscopic and open posterior adrenalectomy in 40
pigs. They concluded that laparoscopic adrenalectomy compared favorably enough that study of its use should continue. Ting et
al.77 stated that laparoscopic adrenalectomy is replacing posterior adrenalectomy.
Barry et al.78 stated that for small incidentalomas considered benign or nonfunctioning the appropriate treatment is conservative
management, rather than laparoscopic removal.
Barresi and Prinz79 stated the following:
Conventional surgical approaches, particularly the transabdominal and thoracoabdominal approaches, will undoubtedly be
required to treat certain lesions of the adrenal gland. This is especially true when dealing with larger tumors, and those
suspicious for malignancy. Surgeons with an interest in treating patients with adrenal disorders must become proficient in
the technique of lapraroscopic adrenalectomy. This will allow them to offer their patients the most appropriate means of
operative therapy suitable for their individual problems.
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operative therapy suitable for their individual problems.
Gill et al.80 provided cautious support for outpatient adrenalectomy, "Ambulatory adrenalectomy is feasible and safe, and results
in high patient satisfaction. However, ambulatory adrenalectomy should be restricted to highly select patients and performed by
minimally invasive surgeons who have considerable experience with laparoscopic surgery."
Smith et al.81 have written that "laparoscopic adrenalectomy has become the gold standard for adrenalectomy."
ANATOMIC COMPLICATIONS
Organ Injury
SPLENIC CAPSULE AND SPLEEN
Excessive traction on the spleen with tearing of the capsule is the greatest single operative risk in anterior left adrenalectomy.
Nash and Robbins83 reported splenic injury requiring splenectomy in up to 20 percent of adrenalectomy patients. We believe that
partial splenectomy should be performed whenever possible.
PANCREAS
The pancreatic parenchyma can be injured during upward reflection of the organ; this may result in clinical pancreatitis with the
formation of a pseudocyst in some cases. Injury to the tail of the pancreas requires resection and drainage. If injury to the
inferior border is minor, drain; if major, repair and drain, or resect the entire distal pancreas and drain.
RENAL CAPSULE
Sharp dissection of the inferior medial margin of the left adrenal gland can injure the capsule of the left kidney. Such injury
should be repaired.
LEFT COLON
Incision of the left mesocolon or excessive retraction of the colon could injure the colon wall, or even perforate it. The colon
should be prepared with enemas and antibiotics before surgery, in case inadvertent perforation occurs and repair is necessary.
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Remember that the medial posterior attachments of the liver contain the hepatic veins. Retract with care. A right hepatic vein
can be ligated.84 Hepatic resection after major hepatic vein ligation is necessary in some animals, but not in humans.
INFERIOR VENA CAVA
Avoid aggressive lateral retraction of the adrenal gland. Traction on the right adrenal vein may rupture the vena cava;
hemorrhage here is difficult to control, and immediate repair is necessary.
SUPERIOR RENAL POLAR ARTERY
As on the left, the occasional polar artery lies close to the operative field and can be injured. If injured, it can be ligated.
GASTRODUODENAL ARTERY
The gastroduodenal artery should be identified and avoided during the Kocher maneuver. If it is injured, ligation is necessary.
Organ Injury
LIVER
Injury to the liver can result from excessive retraction. Pressure, cautery, Gelfoam, or Avitene can be used in repair.
DUODENUM
Mobilization and reflection can injure the duodenum and may result in a catastrophic postoperative duodenal fistula. Avoid sharp
dissection, and be prepared to repair the defect.
Organ Injury
PLEURA
The pleura at the 12th rib must be identified and pushed out of the way. Flint and Bartels58 found 4 cases of perforated pleura
among 29 exposures of the adrenal glands.
If perforation occurs, it is necessary to evacuate air from the pleural cavity by catheter, with pulmonary inflation. Repair the
pleural defect if possible.
TWELFTH SUBCOSTAL NERVE
The 12th subcostal nerve should be protected. Its injury will result in hyperesthesia or dysesthesia in the groin.
RENAL CAPSULE
Excessive retraction can tear the renal capsule. Repair it if necessary. The adrenal gland, in some cases, receives inferior adrenal
arterial supply from capsular branches of the renal arteries.
PANCREAS
Remember that in the posterior approach, the pancreas lies just beneath the left adrenal gland. See details in the "Anterior
Approach for Left Adrenalectomy" section.
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Vascular Injury
These injuries are the same as in anterior approaches.
Organ Injury
In the thoracoabdominal approach, the lung and phrenic nerve are at risk in addition to the organs that are subject to injury in
an anterior approach to the adrenal glands (splenic capsule and spleen, pancreas, left renal capsule, left colon, liver, duodenum).
If the pleura is entered, there is a possibility of injury to the lung; such injury must be repaired.
Incision of the diaphragm must be planned to avoid sectioning major branches of the phrenic nerve. Fig. 27-29 shows permissible
incisions of the diaphragm from above.85
Fig. 27-29.
Schematization showing chief branches of phrenic nerves on cranial surface of diaphragm. Dashed lines indicate location of incisions
that will avoid phrenic nerves. A, The diaphragmatic component of a combined abdominothoracic incision extending down into the
esophageal hiatus. B, Circumferential incision. C, D, Incisions extending from lateral (midaxillary) and posterior costal areas into the
central tendon (from above). (Modified from Merendino KA. The intradiaphragmatic distribution of the phrenic nerve. Surg Clin North Am
1964;44:1217; with permission.)
In a select group of patients with Cushing's syndrome, bilateral adrenalectomy is necessary and effective. However, this surgery
is associated with occasional morbidity and mortality. According to O'Riordain et al.,86 long-term sequelae are not well known.
NOTE: For further reading about the adrenal glands, the authors highly recommend Surgery of the Suprarenal Glands, edited by H.
REFERENCES
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2. Crowder RE. The development of the adrenal gland in man, with special reference to origin and ultimate location of cell types
and evidence in favor of the "cell migration" theory. Contrib Embryol Carnegie Inst Wash 1957;36:193.
3. Sucheston ME, Cannon MS. Development of zonular patterns in the human adrenal gland. J Morphol 1968;126:477. [PubMed:
5716437]
4. Yeasting RA. Selected morphological aspects of human suprarenal glands. In: Mulrow PJ (ed). The Adrenal Gland. New York:
Elsevier, 1986, pp. 45-63.
5. Winter JSD. Fetal and neonatal adrenocortical development: embryogenesis and morphology. In: James VHT (ed). The Adrenal
Gland (2nd ed). New York: Raven Press, 1992. pp. 88-89.
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Gland (2nd ed). New York: Raven Press, 1992. pp. 88-89.
6. Swinyard CA. Volume and corticomedullary ratio of the adult human suprarenal gland. Anat Rec 1940:76:69.
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