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The Journal of Clinical Endocrinology & Metabolism Vol. 83, No. 11 3786-3789
Copyright © 1998 by The Endocrine Society

Special Articles

Recurrent Cushing’s Syndrome Due to Recurrent Adrenocortical Tumor—Fragmentation or Tumor in Ectopic Adrenal Tissue?

J. Leibowitz, D. Pertsemlidis and J. L. Gabrilove

Division of Endocrinology, Bronfman Department of Medicine, Mount Sinai Hospital and Mount Sinai School of Medicine of the City University of New York, New York, New York 10029

Address all correspondence and requests for reprints to: Dr. J. Lester Gabrilove, Division of Endocrinology, Mount Sinai School of Medicine, 5th Avenue and 100th Street, New York, New York 10029.


   Abstract
Top
 Abstract
Introduction
 Case Report
 Discussion
 References
 
A 33-yr-old woman was found to have Cushing’s syndrome due to a left adrenal cortical tumor. The tumor and the surrounding adrenal gland were removed intact and in toto. Four years later, she noticed recurrent symptoms of Cushing’s syndrome, and 6 yr postoperatively, an adrenal tumor was demonstrable on computed tomography. Fourteen years after the initial procedure, a left adrenal tumor, presumably arising in ectopic adrenal tissue, was removed with relief of her symptoms of Cushing’s syndrome. The site and functional capacity of ectopic adrenal tissues are reviewed.


   Introduction
Top
 Abstract
 Introduction
Case Report
 Discussion
 References
 
TUMORS originating from ectopic adrenal tissue are very rare, as is secretion of aldosterone, cortisol, or androgens from such tissue. Adrenocortical adenomas and carcinomas associated with Cushing’s syndrome usually occur as solitary neoplasms, and instances of multiple neoplasms of the adrenal in association with this disease are uncommon. We have observed a case of tumor arising in presumed ectopic adrenal tissue causing Cushing’s syndrome in a patient who previously had had complete intact surgical removal of a cortisol-producing adrenal adenoma together with the entire surrounding adrenal gland. In this light we review the location and possible clinical manifestations of ectopic or aberrant adrenocortical tissue.


   Case Report
Top
 Abstract
 Introduction
 Case Report
Discussion
 References
 
A 33-yr-old woman was admitted to another hospital with a diagnosis of Cushing’s syndrome. She was well until 5 yr before the admission. She began to markedly gain weight of a central character, and a dorsal-cervical fat pad appeared. Approximately 2 yr before that admission she had noted the onset of irregular menses, and 1 yr later amenorrhea. During that interval, she complained of muscle weakness and fatigue, inability to climb stairs, easy bruisability, and bluish stretch marks on the abdomen. She also noted facial hirsutism, lower back pain, nocturia, some decrease in height, and hypertension. The urinary free cortisol level was 361.2 µg/24 h, and a late afternoon plasma cortisol was 21.1 µg/dL. After the administration of 1.5 mg dexamethasone in the late evening, the plasma cortisol level was 22.3 µg/dL the following morning. After the administration of 2 mg dexamethasone/day for 2 consecutive days, the urinary free cortisol level was 40.8 µg/24 h, the urinary neutral 17-ketosteroid level was 6.9 mg/24 h, and the plasma cortisol level was 25.5 µg/dL. After administration of 8 mg dexamethasone/day for 2 days, urinary free cortisol was 55.6 µg/24 h, urinary neutral 17-ketosteroids were 12.1 mg/24 h, and plasma cortisol was 22.5 µg/dL. There was no increase in the plasma concentration of testosterone, dehydroepiandrosterone sulfate, or androstenedione. Computed tomography revealed a left adrenal mass.

Physical examination at that time revealed a white woman with moon facies and marked central obesity. The blood pressure was 150/100 mm Hg. Mild facial hirsutism was present, and the abdomen was obese, exhibiting bluish striae. There were scattered ecchymoses and a dorsal-cervical fat pad.

A diagnosis of Cushing’s syndrome due to a left adrenal cortical tumor was made. She underwent left adrenalectomy, with removal of a 4 x 5-cm mass. The intact left adrenal and enclosed adrenal tumor were totally excised. Postoperatively, she was maintained on cortisone acetate. The pathological diagnosis was adrenocortical adenoma in an atrophic adrenal gland.

Two years after the left adrenalectomy she had an uneventful pregnancy. Four years later, she was found to have mild hypertension. The menses were regular. Urinary free cortisol was 115 µg and 101 µg/24 h. The morning plasma cortisol was 18.1 µg/dL, with an ACTH level of less than 20 pg/mL. An overnight 1-mg dexamethasone suppression test revealed a plasma cortisol level of 6.9 µg/dL. After the administration of 2 mg dexamethasone/day for 2 days, the plasma cortisol was 7.6 µg/dL, and the 24-h urinary free cortisol was 47 µg. After the administration of 8 mg dexamethasone for 2 days, plasma cortisol was 8.6 µg/dL and 24-h urinary free cortisol was 51 µg. Computed tomography of the abdomen revealed a 2-cm tumor in the left adrenal bed. The right adrenal gland was interpreted as normal or slightly reduced in size. Surgery was deferred, with close follow-up recommended.

When seen at the Mount Sinai Medical Center 8 yr later, she complained of recurrence of facial hair, fatigue, joint aches, impaired memory, and diminished libido. On physical examination, she weighed 227 lb. The blood pressure was 150/90 mm Hg. There were prominent cervical-dorsal and supraclavicular fat pads. Minimal nonviolaceous abdominal striae were present. The skin was of good texture, and there was equivocal thigh weakness. The remainder of the examination was essentially negative. The urinary free cortisol was 92.4 µg in 24 h. Morning serum cortisol was 13.9 µg/dL, and ACTH was 6.1 pg/mL. On another occasion the urinary free cortisol level was 78 µg in 24 h. Urinary excretions of vanillyl mandelic acid, homovanillic acid, and metanephrines were normal. Serum 17-hydroxyprogesterone, 17-hydroxypreg-nenalone, total testosterone, androstenedione, dehydroepiandrosterone sulfate, blood chemistries, complete blood count, and urinalysis were within the normal range. An iodocholesterol scan revealed uptake only in the area of the left adrenal gland. Magnetic resonance imaging of the abdomen revealed a 2.4 x 2-cm mass in the vicinity of the left adrenal. The right gland was atrophic.

At laparotomy, the surgeon removed a 2.5 x 3-cm adrenal tumor surrounded by adrenal cortical tissue. The pathological report was "adrenal cortical adenoma in the remnant of the adrenal gland and fat containing adrenal gland." The pathologist was unaware of the previous operative totally intact removal of the left adrenal gland. Postoperatively, the patient did well on reducing dosages of glucocorticoids, and her symptoms gradually improved.


   Discussion
Top
 Abstract
 Introduction
 Case Report
 Discussion
References
 
In 1740, Morgagni noticed yellowish nodules with the characteristics of adrenal tissue near the adrenal gland (1). Subsequently, nodules were noted at various anatomical locations. Before 1900 and in the early 20th century, several researchers noted accessory adrenal tissue in the kidney, broad ligament of the ovary, spermatic or ovarian vein, testes, and spermatic cord (2).

According to Jaffe (3), accessory adrenal tissue may be found in at least 50% of neonates and infants if searched for carefully. With advancing age, this accessory tissue atrophies because it is physiologically unnecessary in the presence of normal adrenal glands. In 1939, in 630 autopsies, Nelson reported 19 cases of accessory adrenal cortical tissue, of which 11 were found in proximity to the testes, 5 near the renal capsule, and 3 on the spermatic cord or broad ligament (2). He cited the work of Lubarsch, who found adrenal cortical tissue in 8 kidneys of 300 autopsies, of Brites who found accessory adrenal tissue in 10 kidneys of 376 examinations, and Glynn who found no accessory adrenal tissue in 1500 kidneys (2). In 1943, Mitchell and Angrist (4) encountered 23 instances of accessory adrenal tissue in the kidney in 2896 autopsies at the Queens General Hospital. They postulated that if the renal capsule is stripped carefully and examined carefully, the incidence of accessory adrenal tissue increases markedly. That same year, 8 cases of adrenal tissue beneath the capsule of the kidneys with no adrenal tissue in the normal position (adrenal-renal heterotopia) were reported in 5000 routine autopsies (5).

Graham (6) examined the celiac region in 100 consecutive autopsies at Memorial Hospital. Thirty-two cases of some form of accessory adrenal tissue were found; 16 contained cortical tissue only, and 16 contained both cortex and medulla. Similarly, Falls reported 11 cases of adrenal cortical nodules in the broad ligament of adults during a 14-month period (7). Mares et al. (8) documented 12 cases of ectopic adrenal cortical tissue along the spermatic cord in 386 surgical specimens. One report described 9 cases of ectopic adrenal tissue in 304 operations in the inguinal region of children (9). Thus, it appears that accessory adrenal tissue occurs fairly commonly in the celiac region, the genitourinary region, and in the vicinity of the adrenals.

The cortex develops from a collection of mesenchymal cells on each side between the root of the dorsal mesentery and the developing gonad (the urogenital ridge). The cells that form the medulla are derived from sympathetic ganglia (10). As the elements that form the medulla migrate to the region of the fetal cortex, fragments of tissue, particularly cortex, can be split off, forming accessory adrenals (3). Most accessories remain near the vicinity of the adrenal gland, but some become more closely related to the sex organs, which migrate during development.

Ectopic adrenal tissue has also appeared in other multiple areas of the body. There have been two reports of ectopic adrenal tissue in the lung of newborns (11, 12) and one report of an ectopic virilizing tumor attached to the posterior pericardium in a young woman (13). There are several reports of intracranial (14, 15) or intraspinal ectopic adrenal tissue (16). Ectopic adrenal tissue has also been described in the liver (17, 18, 19), pancreas (20), gallbladder (21), placenta (22), appendix (23), and transverse colon (24). Bozic suggests that the unusual location of ectopic tissue may be related to misplaced mesothelial cells or autonomous differentiation of mesodermal elements (11).

Ectopic tissue may undergo malignant transformation and/or become hormonally functional. Jaffe performed bilateral adrenalectomy in several hundred rats and found functioning gross accessories in nearly 25% of the animals (3). Chaffee et al. (25) described a patient who showed continued classical Cushing’s syndrome after bilateral total adrenalectomy. A 7 x 2 x 1-cm mass near the inferior pole of the left kidney was encountered. Histological examination revealed medullary and cortical adrenal tissue with hyperplasia of the cortical element. Postoperative improvement in Cushing’s syndrome occurred. Several years later three cases of persistent Cushing’s syndrome after bilateral adrenalectomy were described (26). However, the researchers were unable to localize the persistent functioning ectopic adrenal tissue that they assumed existed. Other reports demonstrated persistent Cushing’s syndrome after bilateral adrenalectomy, with the right adrenal remnant (27) and a parovarian nodule (28) as the source of ectopic functioning adrenal tissue. Thus, it is assumed that under the influence of corticotropin, accessory adrenal cortical tissue is capable of being stimulated to the point of producing Cushing’s syndrome. In all such instances, it is necessary to exclude fragmentation of the adrenal during the actual operative procedure.

Hyperfunctioning ectopic tissue can result in Conn’s syndrome, extreme virilization, as well as Cushing’s syndrome. Arnold and Mitchell described a woman with an ectopic aldosteronoma located posteromedial to the stomach and above the left adrenal (29). Other reports described ectopic aldosteronomas in the retrocaval region (30) and in the right kidney (31, 32). Two reports demonstrated an adrenogenital syndrome caused by hyperfunctioning ectopic adrenal tissue located in the ovary and the solar plexus (33, 34). Virilizing ectopic adrenal tissue in the parovarian region has been activated by Nelson’s syndrome in three separately described cases (35, 36, 37). Additionally, a virilizing adrenocortical neoplasm has been described attached to the posterior pericardium (13), and a 23-yr-old female who presented with elevated androgen levels and a mild degree of Cushing’s syndrome was found to have a functional adrenal rest tumor of the liver (19). Precocious puberty has been described in males with testicular tumors of probable adrenal origin (38, 39). Testicular tumors (presumably adrenal cells) are encountered in untreated or inadequately treated instances of male congenital adrenocortical hyperplasia.

Very few cases of neoplasms, usually malignant, of ectopic adrenal tissue causing Cushing’s syndrome have been reported. A 26-yr-old woman was found to have a fully encapsulated 15-cm adrenal carcinoma resting above a normal left adrenal gland (40). A 59-yr-old male who continued to have Cushing’s syndrome had an adrenal carcinoma in a 7-cm mass that rested 8 cm above the upper pole of the right kidney (41). A 26-yr-old woman was found to have a 2.5-cm adrenal carcinoma in the tail of the pancreas (20). Surgical exploration revealed a right-sided 4 x 5-cm adenoma near a normal right adrenal gland (42), and in an infant a neuroblastoma in ectopic adrenal tissue was found close to but distinct from a normal right adrenal gland (43). A large nonfunctioning ectopic adrenal mass in the hilum of the right kidney with benign histology was classified as carcinoma because of its weight (44), and a large nonfunctioning histologically proven adrenal carcinoma in the omentum adherent to the transverse colon has also been described (24). Tumors such as myelolipomas (45, 5) and oncocytomas (47) have originated from ectopic adrenal tissue.

Multiple functional adrenocortical adenomas in Cushing’s syndrome are a very rate entity, as only 18 cases have been reported, 14 bilaterally and 4 unilaterally (48, 49). This is the first report to describe sequential development of adrenocortical adenomas causing Cushing’s syndrome, the second adenoma in ectopic adrenocortical tissue. In this instance, the chronology was readily demonstrable. However, in ordinary instances of bilateral adenoma, differentiation must be made from bilateral macronodular hyperplasia. In both, serum ACTH may be suppressed, and the roentgen examination may be unable to differentiate them. However, in the presence of adenomas, the nonadenomatous tissue is likely to be more atrophic than in macronodular hyperplasia, where a distorted thick cortex may be seen. In addition, the morphological, enzyme histochemical, and ultrastructural features of the compact and clear cells seen in adenoma are seen in the bilateral adenomas (50). The differential characteristics of adenoma from macronodular hyperplasia are detailed by Aiba et al. (51) and include in the latter many yellow macronodules distorting the entire architecture and even responsiveness to ACTH.

The original surgical and pathological reports of the patient reported deny the likelihood of fragmentation at the initial procedure. The possibility of carcinoma is rendered extremely unlikely by 1) the long history of 16 yr without metastases, 2) the normal adrenal steroid precursor levels, and 3) the benign histology of both tumors, although we recognized that this can be deceiving. In addition, there was absolutely no indication of erosion of the capsule in either lesion, and a tumor plus normal adrenal tissue were found at the second operation. If the original lesion were a carcinoma, normal adherent adrenal tissue would not be present. In addition, if spillage were to occur at the time of the original procedure, it also is unlikely that both tumor and normal adrenal tissue would be found.

In summary, we have described a patient with Cushing’s syndrome due to a left adrenal adenoma who was cured by a left total (intact) adrenalectomy. Several years later, Cushing’s syndrome recurred, and an adenoma was found in the vicinity of the previously removed left adrenal gland. We believe that this patient’s recurrence was due to a second tumor in ectopic adrenal tissue, that it was not due to fragmentation nor spillage, and that the original lesion was not a carcinoma. The concurrence of ectopic adrenal tissue and the hyperfunctioning syndromes associated with it are described.



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  		Figure 1. MRI of the abdomen demonstrating a tumor in adrenal tissue after the normally located adrenal had previously been excised 15 yr previously.

 


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  		Figure 2. Pathology specimen of adrenal tumor removed in 1995 and depicted in MRI in Fig. 1Go. a, Gross specimen; b, Microscopic.

 


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  		Figure 3. CAT scan of the abdomen postoperatively demonstrates the site of the previously removed mass seen in Fig. 1Go.

 
Received February 9, 1998.

Revised June 3, 1998.

Revised July 14, 1998.

Accepted July 21, 1998.


   References
Top
 Abstract
 Introduction
 Case Report
 Discussion
 References
 

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