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Advances in Anatomic Pathology:
doi: 10.1097/PAP.0b013e3181bb6c09
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Cystic Lymphangioma-like Adenomatoid Tumor of the Adrenal Gland: Case Presentation and Review of the Literature

Bisceglia, Michele MD*; Carosi, Illuminato MD*; Scillitani, Alfredo MD; Pasquinelli, Gianandrea MD‡ §

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Author Information

Departments of *Pathology

Endocrinology, IRCCS, “Casa Sollievo della Sofferenza” Hospital, V.le Cappuccini, I-71013 San Giovanni Rotondo (FG)

Department of Clinical, Radiological, and Cytohistopathological Sciences, University of Bologna, Bologna

§Istituto Nazionale Biostrutture e Biosistemi, INBB, Roma, Italy

Reprints: Michele Bisceglia, MD, Department of Pathology, IRCCS, “Casa Sollievo della Sofferenza” Hospital, V.le Cappuccini, I-71013 San Giovanni Rotondo (FG), Italy (e-mail: m.bisceglia@operapadrepio.it).

All figures can be viewed online in colour at http://www.anatomicpathology.com.

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Abstract

Adenomatoid tumors (AT) are usually found in the genital tract of both sexes. They are very rarely located in extragenital sites, and are exceedingly rare in the adrenal. AT of the adrenal gland (AT-AG) are nonfunctioning, usually discovered incidentally and confused on imaging with other more common adrenal neoplasms. The overwhelming majority occur in males. Thirty-four cases have been reported so far, more often presenting grossly as solid tumors, rarely as solid with cystic areas, and 5 cases were almost entirely cystic. At histology they can be either circumscribed or locally infiltrative, and may pose diagnostic difficulties when the pathologist relies on morphology alone or is challenged on frozen section. On light microscopy the diagnosis may be very difficult if the tumor is rich in vacuolated cells, mimicking metastatic signet ring-cell adenocarcinoma. Immunophenotyping and/or electron microscopy are paramount in helping to ascertain their mesothelial lineage. Lymphangioma is the main histologic mimic of solid-cystic and cystic AT-AG, but lymphangioma is immunopositive for endothelial markers and negative for cytokeratins and mesothelial markers. Ultrastructural analysis has been performed in 10 published cases of AT-AG, in all of which the classical microvilli of coelomic type were always observed. In brief we report herein the sixth case of cystic lymphangioma-like AT, which was incidentally discovered during clinical follow-up in a 39-year-old man undergoing cancer staging and surveillance after surgery. The adrenal tumor was 5.5 cm in size and was fully investigated immunohistochemically and ultrastructurally. A complete review of the literature is also presented.

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OVERVIEW

Diagnosis: Cystic lymphangioma-like adenomatoid tumor  of the adrenal gland (AG).

Referral sources: AMR seminar n. 36-case 4 (slides labeled  96188-9618899), contributed by M. Bisceglia, MD, San  Giovanni Rotondo, Italy

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CLINICAL HISTORY

A 39-year-old male patient was being followed for previously diagnosed cancer of the left colon (Dukes B stage), which had been surgically removed 4 years before. Two years after that operation, the patient was found to have an expansile hypodense, well-defined, nodular lesion 3 cm in size in his right AG on a computed tomography abdominal scan (Fig. 1). The suspected diagnosis was nonfunctioning cortical adenoma, as the patient did not show any clinical features either of hypercortisolism, or sex steroid, or mineral-corticoid production and had normal arterial blood pressure, and follow-up was continued. Two years later the lesion increased in size to 5 cm, and surgical right adrenalectomy was performed. Imaging studies of all other internal organs were unremarkable. The preoperative blood chemical assays for adrenocortical hormones were all normal. Following the Synacten test, 17-OH progesterone blood level was elevated to twice the maximum normal value, a finding considered a common occurrence with incidentally discovered adrenocortical tumors. Serum analyses and urinalyses for catecholamines as well as urinary 5-OH-indolacetic acid also were normal.

Figure 1
Figure 1
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HISTOLOGIC FINDINGS

The adrenalectomy specimen grossly showed a well-circumscribed lesion of 5.5 cm within the AG, which on sectioning was cystic and gray-to-pale yellowish in color (Fig. 2). The lining of the cyst on the cut surface was mostly smooth. However, small areas of slight mural thickening with a spongy appearance and short endoluminal papillations were seen (Fig. 3).

Figure 2
Figure 2
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Figure 3
Figure 3
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Microscopic examination of the latter areas showed a lymphangioma-like tumor, composed of variably sized, anastomosing tubules, channels, and small cystic spaces lined by flat endothelial-like cells, replacing and infiltrating the normal cortical and medullary adrenal parenchyma (Figs. 4A–F). A few small-scattered lymphoid aggregates were also seen at the periphery of the lesion. Immunohistochemically the flattened cell layer lining the lumen of the major cyst and the thin walls of the microcystic and tubular spaces of the lesion failed to react with any of the endothelial markers used (ie, CD34, FVIII-RAg, and CD31), whereas it strongly reacted with cytokeratins (pankeratins, cytokeratin 5/6), and calretinin (Figs. 5A–F). Ultrastructural analysis was also performed on small fragments recovered from the paraffin-embedded tumor tissue, which showed numerous slender microvilli (coelomic or mesothelial type) on the surface of tumor cells (Figs. 6A, B).

Figure 4
Figure 4
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Figure 5
Figure 5
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Figure 6
Figure 6
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FINAL DIAGNOSIS

Cystic lymphangioma-like adenomatoid tumor of the AG.

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AUTHORS' COMMENT

Adenomatoid tumors (AT) are uncommon tumors, usually found in the genital tract of both sexes, mostly in the epididymis and other paratesticular structures in males1 as well as in the uterus,2 fallopian tubes, and ovary3 in females, respectively. They are much more rarely located in extragenital sites, such as the omentum, intestinal mesentery, retroperitoneum, heart, pleura, and mediastinal lymph nodes(Ref. 4 and references therein). A case of multiple intra-abdominal AT involving the omentum and mesocolon has also been reported.5 Primary AT of the AG (AT-AG) are exceedingly rare, their histogenesis being related either to the entrapment of primitive mesenchymal cells associated with the müllerian tract in the adrenal, a plausible occurrence in view of the embryologic relationship between the developing AGs and the gonads(Ref. 4 and references therein, 6) or to the dislodgement therein of mesothelial inclusions(Ref. 4 and references therein), both of which are of coelomic epithelium derivation(Ref. 4 and references therein).

AT-AG are nonfunctioning tumors, which are usually discovered incidentally on imaging. So far 34 cases of AT-AG have been described (Table 1),7–30 including the periadrenal case of Evans et al8 and 2 of the 4 cases reported by Alfred Plaut from the AFIP (Washington, D.C.) in 1962 as locally invasive lymphangioma of the AG,7 which according to other authors really seem to be adenomatoid tumors.31 AT-AG have been reported in both sexes, the overwhelming majority of them in males (male-to-female sex ratio 10 to 1). Of the 31 cases in which the side was stated, in 18 cases the tumor was on the right side and in 13 cases on the left. The age range spanned from 24 to 73 years. Twenty-five cases, out of the 33 in which the patient age was stated, were discovered in the third to fifth decades, with the peak incidence in the fourth decade (12 cases) (Table 1). AT-AG has been incorporated into the last World Health Organization classification of tumors of endocrine organs.32

Table 1
Table 1
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In 7 out of the 34 cases, the tumor was incidentally diagnosed on post-mortem.7,11,12,15 In the majority of the remaining cases the tumor was found incidentally during investigation either of completely unrelated symptoms (pneumonia, bronchiectasias, cholecystitis, epigastric pain, dyspepsia, etc), concurrent but unrelated symptoms referable to the ipsilateral kidney (renal pain or colic due to kidney lithiasis), or for suspected related systemic symptoms (arterial hypertension), which were later found to be associated with the adrenal lesion in 2 cases.10,16 In these latter 2 cases either an elevation of urinary homovanillic acid or hyperaldosteronism was documented in each of the cases, such endocrinopathies are likely caused by stimulation of the normal adrenal parenchyma by AT. In 1 other case gross hematuria was directly attributable to the adrenal AT.8 Clinico-radiologic preoperative and intraoperative diagnosis is challenging if not impossible, because of the rarity of these lesions in this specific location, their usual hormonal inactivity, and the lack of specific radiologic features.13 As a consequence of that, AT-AG is often confused with other more common adrenal tumors and mostly diagnosed clinically as benign nonfunctioning adrenocortical tumors, lymphangioma, myelolipoma, and cysts of various types (Table 1). Malignant primary13 and metastatic tumors9,30 are included among the diagnostic considerations, and functioning adrenocortical tumors and pheochromocytomas are also suspected on rare occasions, on the basis of the elevation of some hormonal levels.10,16,20 The awareness of the possible occurrence of this type of tumor in this unusual site is crucial to avoid misinterpretation, especially when dealing with patients who are undergoing clinical cancer staging or are being followed for previously resected cancer, as of several internal organs, both abdominal and thoracic, adrenal is 1 of the most favoured locations for metastatic seeding. In 4 cases the adrenal AT was incidentally discovered during clinical cancer staging/surveillance (cases 4, 9, and 34 in Table 1, in addition to this present case).

Tumor size varied from less than 1 cm to 15 cm (Table 1). Grossly the majority of AT-AG were similar to their genital counterparts and presented as solid tumors, firm or soft in consistency, whereas some have been described as solid with cystic areas, and only 5 were described as entirely or almost entirely cystic9,15,21,29 (Table 1). On histology AT-AG are described both as circumscribed with well-defined capsule walls and as infiltrative,7,10,11,15,16,18,21,28 occasionally penetrating into the periadrenal adipose tissue.7,9,11,14,15,21 In 2 cases (case 1 in Ref. 7, and case 5 in Ref. 15) the tumor was seen infiltrating the walls of large (intra-)adrenal veins. Microscopically the following growth patterns have been seen: adenoid (adenomatoid), solid (packing of tubules and vacuolated cells), lymphangiomatoid, microcystic-cavernous, and papillary (Table 1). As expected, intracellular or extracellular epithelial mucin was not seen using Diastase-periodic acid-Schiff or mucicarmin histochemical stains, but stromal mucin (alcian blue positive) has been demonstrated. Lymphoid infiltrates similar to those in the genital cases are a common finding in AG-AT,7,10,11,13–15,17,21,26 which in a lymphangiomatoid, microcystic or cavernous variant of AT may reinforce the misleading diagnostic alternative of lymphangioma. Intratumoral adipose tissue has also occasionally been seen.21,27 Dystrophic calcifications.11,15,20,24,25,29, sometimes already noted on preoperative imaging studies,20,29 and metaplastic ossification20 have been described as well. Immunohistochemistry has been performed in 29 cases, always showing the usual immunohistochemical profile of mesothelial cells, including strong immunoreactivity for cytokeratin (pankeratin, high-molecular weight cytokeratin 5/6) and calretinin. Ultrastructural analysis has been used in 10 cases,8,9,11,14,16,18,21,30 in all of which the classical microvilli of coelomic type were always observed, these being the substrate of the “brush” border some people were able to observe and depict even on hematoxylin and eosin stained slides in mesothelial derived tumors, including AT-AG.10 In all cases the AT-AG was totally resected (either by laparoscopic or open surgery), except for 1 (case 34, Table 1) where the diagnosis was made on core biopsy and the lesion was left for follow-up.30

Metastatic adenocarcinoma, lymphangioma, angiosarcoma, cysts, and pseudocysts of various origin, including the mesothelial cyst and the so-called true epithelial cyst of the adrenal, and cystic mesothelioma, may enter the differential histologic diagnosis. Classic-type adenoid tumors or those rich in vacuolated cells can mimic adenocarcinoma not otherwise stated or signet ring-cell carcinoma, respectively, presenting a difficult challenge if the pathologist is confronted with a frozen section4,15 or relies on morphology alone. Immunophenotyping and or electron microscopy are paramount, helping to confirm the mesothelial lineage of AT as opposed to metastatic carcinoma, as with other analogous tumors of mesothelial-cell derivation.33,34 Lymphangioma, which is a well-known entity possibly involving the adrenal,31,35–37 is the main histologic mimic of AT as attested to not only by the unrecognized cases of Plaut from the preimmunohistochemical era, but also by some remarks made by other club members (see below). However, this issue is easily resolved, as lymphangioma is immunopositive for endothelial and negative for both epithelial and mesothelial markers. Angiosarcoma exhibits at least some cytologic atypia, mitotic activity, and the same immunohistochemical profile as lymphangioma. Primary cystically degenerated adrenocortical tumors (cystic adenoma and carcinoma) are still recognizable by the presence of residual nests of neoplastic cortical cells. Ancient schwannoma is another unusual cystic tumor, which may occur in the adrenal, but it shows different diagnostic clues. Adrenal hemorrhagic pseudocyst and parasitic cyst (echinococcus) have totally different appearances and no epithelial or endothelial or mesothelial lining layer. “True” epithelial cysts of the adrenal,38 likely of mesothelial origin,9 and mesothelial cysts primary of the adrenal(Ref. 9 and Ref. 6 therein)32, are unilocular simple cysts, histogenetically linked to the entity under discussion, with a thin capsule and noninfiltrative borders, which some authors believe may give rise to AT-AG.9,10,32 Multicystic mesothelioma occurring in the pelvic peritoneum of young-to-middle-aged women, may have areas identical to AT(Ref. 39 and references therein), and in some respects may be related to the case we report here. Finally, the AT-AG variant with papillary features14 needs to be differentiated from well-differentiated papillary mesothelioma, a solitary or multifocal, usually benign tumor, located in the peritoneum (omentum, mesentery, pelvis) and also derived from mesothelial cells, a case of which with the features of AT39 also having been reported.

AT-AG has occasionally been reported as a composite tumor in association with myelolipoma (2 cases),27 which in our opinion may represent a possible coincidental occurrence, as AG is the most common location for myelolipoma. Ipsilateral, intratumoral or adjacent adrenocortical micronodular hyperplasia has also been observed in 3 cases7(case 1),9,16 a likely causal relationship since, as previously mentioned, the AT may probably interfere with the normal physiology of the adrenal cortex, leading to hyperplasia. The latter circumstance can be analogous with other situations, such metastatic carcinoma to the ovaries causing stromal hyperplasia with its attendant endocrine symptoms. In a singular case a microscopic (not evident on gross examination) AT was incidentally found at histology as an intramural nodule located in the wall of a concurrent hemorrhagic vascular cyst21 (case 1).

Similarly to their genital counterpart, AT-AG of the adrenal are benign tumors. Surgery alone (complete resection) is the treatment of choice with no adjunctive therapy needed. No case of recurrence or metastasis has ever been described. In conclusion, we report herein the sixth case of a cystic lymphangioma-like adenomatoid tumor of the adrenal, incidentally discovered in the course of clinical follow-up for cancer staging and surveillance, and fully investigated by preoperative imaging and pathologic studies, in a surgically operated patient.

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CLUB'S OPINIONS AND COMMENTS

* I had never heard of the entity until after seeing the answer, but that is what it looks like to me. It is not exactly the same histologically as a usual adenomatoid tumor but it is an unequivocally benign mesothelial proliferation.

* I would have predicted a lymphangioma, as I saw 1 such adrenal lesion a few years ago; that one showed a much greater degree of lymphoid tissue than this one. It is uncanny how AT can mimic vascular proliferations.

* Beautiful example of a rare tumor.

* Agree. Wow! Thanks for sharing this most unusual example of adenomatoid tumor of AG.

* Agree with diagnosis; my differential was mesothelial (i.e, adenomatoid tumor) versus vascular and the immunostains readily solved it.

* What a great case. I have never heard of such an entity and yet my differential diagnosis included lymphangioma and adenomatoid tumor!

* Very nice case. Agree.

* Agree. Adenomatoid tumor.

* I have never seen this before, but the histology is convincing.

* I have not seen before a case of adenomatoid tumor of the AG, thank you.

* Agree, benign mesothelioma. The link with cystic variant is very strong.

* Now I understand what the club meant when they said that you work in a pathologist's treasure land. I cannot remember any such incredible case: I also asked my mentor who has done about 30,000 autopsies during the last 50 years and despite his thorough search he cannot recall anything like this.

* Remarkable case which I never seen before.

* An amazing but entirely convincing case, I had not previously been aware that one could encounter adenomatoid tumor at this location.

* A classic appearance in a very unusual location.

* I agree with you.

* This is the first time I see this tumor in this location.

* Most unusual case, which shows the importance of electron microscopy in diagnostic pathology.

* This is a remarkable case of a lesion I have never seen before (at least in this organ), excellently documented.

* I did not know that adenomatoid tumor could also occur in the adrenal.

* Thank you for this rarity.

* Great and unusual case. Thanks a lot for sharing this extraordinary neoplasm.

* It is the first case of adenomatoid tumor in the AG I have ever seen. Interestingly even this case has nodules of lymphoid tissue, which is a feature never missing in the gonadal examples. Lack of myoid proliferation in this case, nearly always present in the gonadal examples, shows that this latter proliferation is a reactive phenomenon of tubal and epidydimal myomatous tissues.

* Agree on adenomatoid tumor, periadrenal, or intra-adrenal tumor.

* The picture is fairly typical of adenomatoid tumor, but I would not have imagined it could supervene in adrenal!

* Looks great for adenomatoid tumor. Never seen an example in the adrenal!

* Wonderful example of this rare entity of adenomatoid tumor of the adrenal. The glycosaminoglycans and microvilli lining the spaces are beautifully evident on the hematoxylin and eosin stain.

* Adenomatoid tumor of the adrenal mimicking cystic lymphangioma.

* This is the first time I see this condition in this location!

* Great case. I have seen a few of these (including, I think, the one published by Simpson). The situation is similar to the spleen, in which cases previously reported as lymphangioma were found to have a keratin-positive lining and actually represent mesothelial cysts.

* Beautiful case. This is histologically similar to a case I saw 8 months ago which I considered to be a vascular (endothelial) lesion; having been primed by having seen that earlier case I was more inclined to consider this one as an adenomatoid tumor. Thanks.

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ACKNOWLEDGMENT

The authors wish to thank D. Ben Dor, M.D, Department of Pathology, Barzilai Medical Center, Ashkelon, Israel, for his helpful suggestions and critical review of the article.

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Cited By:

This article has been cited 1 time(s).

International Journal of Clinical and Experimental Pathology
Cystic lymphangioma-like adenomatoid tumor of the adrenal gland: report of a rare case and review of the literature
Zhao, M; Li, CS; Zheng, JJ; Yan, MH; Sun, K; Wang, ZM
International Journal of Clinical and Experimental Pathology, 6(5): 943-950.

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Keywords:

adrenal gland; adenomatoid tumor; lymphangioma; cystic mesothelioma; adrenal cyst

© 2009 Lippincott Williams & Wilkins, Inc.

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