534465
research-article2014
IJSXXX10.1177/1066896914534465International Journal of Surgical PathologySopha et al
Case Report
Hepatic Uterus-Like Mass Misdiagnosed as Hepatic Abscess
International Journal of Surgical Pathology 2015, Vol. 23(2) 134–139 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1066896914534465 ijs.sagepub.com
Sabrina C. Sopha, MD1, Flavia G. N. Rosado, MD2, J. J. Smith, MD, PhD3, Nipun B. Merchant, MD4, and Chanjuan Shi, MD, PhD4
Abstract Background. Hepatic endometriosis/uterus-like mass is rare and may be overlooked during hepatic cyst workups. We report a case of uterus-like mass, misdiagnosed as hepatic abscess. Case Report: A 47-year-old woman developed abdominal pain and vomiting. Infectious colitis with hepatic abscess was diagnosed, and remained antibiotic-refractory. Fine-needle aspiration and core biopsies showed benign contents. The patient presented to our institution with symptoms and normal blood work. Laparoscopic excision demonstrated a 1.4-cm cyst composed of endometrial glands (estrogen receptor+ and progesterone receptor+) and stroma (CD10+) with smooth muscle actin (SMA+), arranged in an organoid fashion. The patient, status-post hysterectomy, had no history or symptoms of endometriosis. Conclusion. This rare case illustrates the merit of considering uterus-like mass/endometriosis in the differential diagnosis of antibiotic-refractory hepatic cysts. Cyst heterogeneity may confound needle biopsy. We report the first instance of a hepatic uterus-like mass, with a review of related entities, postulated histogenesis, and important clinical associations. Keywords uterus-like mass, endometriosis, hepatic cyst
Introduction (Case Report) A 47-year-old Caucasian woman with a long history of diarrhea presented to an outside hospital with acute right upper quadrant and back pain with nausea and vomiting. Other pertinent medical history includes right salpingoophorectomy at age 18 years for teratoma, and Caesarian section at age 26 years, wherein a second teratoma was incidentally encountered and resected. There was a remote laparoscopic procedure for possible malrotation, and the patient underwent a supracervical hysterectomy at age 40 years for unclear reasons. She had taken estrogen for 7 years. She had no previous history of endometriosis or pelvic pain. At the time of this presentation, an abdominal computed tomography (CT) scan showed an area of abnormal enhancement, diagnosed as a liver abscess. Stool culture and serum tests were positive for Aeromonas sp and Entamoeba histolytica, respectively. She was diagnosed with infectious enterocolitis and completed 5 days of intravenous piperacilin/tazobactam, 10 days of ertapenem, and 2 weeks of levofloxacin. The patient had several recurrent episodes of right abdominal pain and right chest pain with effusion and was treated with oral and intravenous antibiotics. During this period, a repeat abdominal CT demonstrated a 13-mm fluid collection in segment VII in the perirenal retrohepatic space, with no abnormalities of the genitourinary system
(Figure 1, arrow). A CT-guided fine-needle aspiration of the lesion revealed necrotic debris, histiocytes, and inflammatory cells consistent with an abscess. A CT-guided liver biopsy revealed smooth muscle, interpreted as incidental diaphragmatic sampling. On the fourth episode of symptoms, the patient presented to Vanderbilt University Medical Center. Blood laboratory tests, including liver function tests and electrolytes, were normal, except for mild leukocytosis (11.5 × 103/mL) with a normal differential. The patient’s symptoms and white blood cell count normalized after three days of analgesic treatment. She was referred to surgical oncology for further evaluation. Because of debilitating symptoms, a laparoscopic segment VII excisional biopsy was performed. An intraoperative frozen section showed endometriosis. Formal pathologic evaluation revealed a 1.4-cm hepatic nodule 1
The Johns Hopkins Hospital, Baltimore, MD, USA The Mayo Clinic, Rochester, MN, USA 3 Memorial Sloan-Kettering Cancer Center, New York, NY, USA 4 Vanderbilt University Medical Center, Nashville, TN, USA 2
Corresponding Author: Sabrina C. Sopha, Department of Pathology, The Johns Hopkins Hospital, Weinberg 2267, 201 N. Broadway, Baltimore, MD 21231, USA. Email: [email protected]
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with epitope retrieval solution 1 for 5 minutes and the antibody incubation was 15 minutes. CD10 antigen retrieval was with epitope retrieval solution 2 for 10 minutes and the antibody incubation was 15 minutes.
Discussion
Figure 1. Noncontrast abdominal computed tomography imaging demonstrating a segment VII, peripherally and posteriorly located cystic lesion.
composed of endometrial-type glands and stroma with associated smooth muscle proliferation in layers recapitulating endometrium and myometrium, arranged around a cystic cavity (Figure 2A and B). Estrogen receptor (ER) and progesterone receptor (PR) immunohistochemical stains confirmed the diagnosis (Figure 2C and D). CD10 and smooth muscle actin (SMA) immunohistochemical stains highlighted endometrial stroma and smooth muscle, respectively, with CD10+ endometrial stromal cells “feathering out” into myometrium (Figure 2E and F). The patient has been asymptomatic on follow-up evaluation.
Materials and Methods Fresh liver tissue was fixed in 10% formalin and processed in the standard fashion. Five micrometers thick sections of paraffin-embedded tissue were stained with hematoxylin and eosin according to standard protocol. Immunohistochemical staining was performed as follows: estrogen receptor (ER, clone SP1 rabbit monoclonal, product code 790-4325 from Ventana Medical Systems, Tucson, AZ) and progesterone receptor (PR, clone 1E2 rabbit monoclonal, product code 790-2223 from Ventana Medical Systems, Tucson, AZ) were run on the Ventana Benchmark XT (Ventana Medical Systems, Tucson, AZ) using the Ultraview DAB Detection kit. Antigen retrieval was with cell conditioning 1 for 30 minutes and the antibody incubations were 4 and 8 minutes, respectively. Smooth muscle actin (SMA, clone asm-1 mouse monoclonal, diluted 1:5, product code PA0943, Leica Microsystems, Bannockburn, IL) and CD10 (clone 56C6 mouse monoclonal, predilute, product code PA0270, Leica Microsystems, Bannockburn, IL) were run on the Leica Bondmax (Leica Microsystems, Bannockburn, IL) using the Refine DAB Detection kit. SMA antigen retrieval was
Endometriosis is defined as a “heterotopic island of endometrial mucosa represented with both its glandular and stromal components.”1 The exact “discoverer” of endometriosis is not clear because the designation is complicated by continuing subtleties in terminology, the recognition (or lack thereof) of endometriosis as a pathologic finding, and the inability to recover all scientific and medical literature on the subject. Benagiano and Brosens2,3 discuss these issues and the contributions of Schrön, Rokitansky, von Recklinghausen, Iwanoff, Russel, Mayer, Orloff, Schroeder, Lockyer, Cullen, and Sampson to the field. Involvement of nearly every organ except the spleen has been described,4 and endometriosis has been reported in males.5-7 The first case of hepatic endometriosis was reported separately in 1986 by Finkel et al8 and Grabb et al9. In total, there are 22 reports of 24 cases of hepatic endometriosis in the English literature.8-29 Most of these lesions are cystic or solid-cystic, with intrahepatic, perihepatic, and hepatic capsular surface locations. One case demonstrated continuity with the biliary system,13 while another developed a bronchobiliary fistula.25 A subset of hepatic endometriosis cases are described with secondary tumors, including endometrioid adenosquamous carcinoma,14 adenosarcoma,15 and endometrial stromal sarcoma.19 One case had a coexisting hemangioma.21 Secondary tumors in endometriosis were first reported by Sampson in 1925.30 The ovary is the primary site in 78.7% of cases, and extragonadal sites compose the remaining 21.3%. Tumor subtypes include endometrioid adenocarcinoma, clear-cell carcinoma, sarcoma, and rarer cell types.30 Generally, tumors arising in endometriosis are low grade and confined to the site of origin. The “uterus-like” or “uterine-like” mass was first described by Cozzutto31 in 1981 and is defined as a cavity lined by endometrial-type mucosa surrounded by bundles of smooth muscle cells, with or without gross resemblance to the uterus. Using strict terminology, 23 English reports of 28 cases of “uterus-like,” “uteruslike,” or “uterine-like” masses have been reported in the small bowel, bowel mesentery, ovary, broad ligament, ovarian ligament, uterine cervix, vaginal cuff, lower uterine segment, uterine corpus, conus medullaris, filum terminale, appendix, sigmoid mesocolon, and subserosa.31-51 There have been associations with midline and laterality congenital defects,32,33,35,37,42,44,45,52 endometriosis,31,32,38,45,52,53 and known or presumed estrogenic stimulation33,34,38,41,45 There are rare cases of secondary tumors.34
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Figure 2. (A and B) Hematoxylin and eosin–stained lesional tissue demonstrating the intrahepatic location of endometrial stroma and glands and myometrium composed of smooth muscle arranged in concentric layers around a cystic cavity (20×, 100×). (C and D). Estrogen receptor (ER) and progesterone receptor (PR) immunohistochemical stains demonstrating endometrial coexpression (100×, 100×). (E and F) CD10 and smooth muscle actin (SMA) immunostains demonstrating CD10 expression within endometrial stromal cells, which “feather out” into SMA-expressing myometrial smooth muscle cells (200×, 200×).
Uterus-like masses and adenomyomas are both composed of endometrial glands and stroma and smooth muscle.41,54 Some authors assert that adenomyoma differs from adenomyosis in circumscription,41 and from uterus-like
masses by lack of organoid arrangement.54 Others assert that lesions described as adenomyoma, endomyometriosis, endometriosis, and tumor of Müllerian type reflect essentially identical histopathologic findings as the uterus-like
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Sopha et al mass and belong to a family of related disease entities with a common histogenesis.39,47,55 In any case, these differing viewpoints may represent extremes of a continuous spectrum of choristoma, a “mass of tissue histologically normal for an organ or part of the body other than the site at which it is located.”56 In the case reported here, the findings of endometrial glands and stroma with abundant smooth muscle proliferation and an organoid arrangement related to a cystic cavity fulfill the criteria of uterus-like mass. There are several theories on the histogenesis of endometriosis and the uterus-like mass (and the related spectrum discussed above), with considerable overlap. The main theories include the Müllerian fusion defect theory (including congenital and heterotopic cases),32,33,35,42,43,48,52,57 the transport/implantation theory,4,12 and the subcoelomic mesenchyme transformation theory (metaplastic theory).* The Müllerian fusion defect theory is supported by the fact that many uterus-like masses occur in association with other midline or laterality defects of organogenesis.32,33,35,37,42,44,45,52 The transport/ implantation theory is supported by the findings of endometrial tissue in anatomically remote organs.8,10,11,26 The metaplastic theory is supported by the association with known or presumed hyperestrogenic states in both males and females5-7,33,34,38,41,45,60 and the association of the uterus-like mass with endometriosis.31,32,38,45,53 The metaplastic theory is additionally supported electron microscopic findings demonstrating smooth muscle fibers and myofibroblasts in the uterus-like mass,31 and by a cytogenetic abnormality similar but not identical to findings in leiomyomas, del2p21, identified in a case of endomyometriosis.1 CD10, a cell surface enzyme found not only in acute lymphoblastic leukemia but also in hormone- or peptide-sensitive tissues such as normal endometrial stroma (but not myometrium),61 may provide additional insight into the histogenesis. Two reports of uterus-like masses or adenoymyomas demonstrate that the respective lesions demonstrated CD10-positive endometrial stroma, with SMA-positive myometrium,48,58 with the assertion that these findings support the metaplastic theory.58 In the case presented here, we report an indistinct junction between the CD10+/SMA− endometrial stroma and CD10−/SMA+ myometrium, with CD10+ endometrial stromal cells “feathering out” into myometrium, lending further support to the theory of metaplasia. The histogenesis debate continues, and it is possible that 2 distinct clinical scenarios exist leading to the rise of endometriosis/ uterus-like masses, and that the 2 theories are not necessarily mutually exclusive. Clinically, right upper quadrant pain and pain along prior implantation sites are common presenting *References 1, 12, 31, 34, 37-41, 46, 47, 49, 53, 58, 59.
symptoms.14,20,21,23,24 Prior bouts of endometriosis are common but these are not found in all cases of hepatic endometriosis.12,24 Ultrasound, CT, and magnetic resonance imaging can be used to support the diagnosis in a peripherally located liver mass, although imaging features vary widely.16 Imaging usually demonstrates a low attenuation, heterogeneous, nonenhancing peripheral mass on CT.14,18,21 Ultrasound can show mixed reflectivity and magnetic resonance imaging can demonstrate increased signal on T1- and T2-weighted images.21 Very large lesions (ie, 12 cm) may cause mass effects resulting in hepatic dysfunction18 or portal vein obstruction.19 Correlation with imaging can aid the pathologist in the differential diagnosis of hepatic cysts. Although in isolation, the small glands may resemble primitive vascular structures, the imaging findings of a cyst, without contrast characteristics of a vascular lesion, in combination with classic morphology showing an organoid arrangement of glands and endometrial stroma with a layer of smooth muscle, should direct the pathologist toward the diagnosis of uterus-like mass, rather than a primitive vascular tumor. Surgical resection of the uterus-like mass/endometriosis lesion is curative.
Conclusion This rare case illustrates the need for high suspicion of endometriosis/uterus-like mass in any patient with a cystic liver lesion refractory to broad-spectrum antibiotics. Moreover, given the heterogeneous nature of solid-cystic endometriomas, which can reach large sizes, and because of the possibility of harboring secondary tumors, fine needle biopsy or core biopsy may not be representative of lesional identity. Minimally invasive laparoscopic excision, as in this case, is a therapeutic approach which can provide a definitive diagnosis, prevent the overuse of antibiotics, exclude/prophylaxe the possibility of secondary malignancies, and improve or eliminate painful symptoms. The unusual location and immunophenotype provide insight into the histogenesis of endometriosis and uteruslike mass lesions. A literature review shows that the finding of a uterus-like mass should prompt investigation of other midline or laterality defects, particularly spinal or genitourinary. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
138 References 1. Verhest A, Simonart T, Noel JC. A unique clonal chromosome 2 deletion in endomyometriosis. Cancer Genet Cytogenet. 1996;86:174-176. 2. Benagiano G, Brosens I. Who identified endometriosis? Fertil Steril. 2011;95:13-16. 3. Benagiano G, Brosens I. The history of endometriosis: identifying the disease. Hum Reprod. 1991;6:963-968. 4. Markham SM, Carpenter SE, Rock JA. Extrapelvic endometriosis. Obstet Gynecol Clin North Am. 1989;16:193-219. 5. Martin JD Jr, Hauck AE. Endometriosis in the male. Am Surg. 1985;51:426-430. 6. Oliker AJ, Harris AE. Endometriosis of the bladder in a male patient. J Urol. 1971;106:858-859. 7. Schrodt GR, Alcorn MO, Ibanez J. Endometriosis of the male urinary system: a case report. J Urol. 1980;124: 722-723. 8. Finkel L, Marchevsky A, Cohen B. Endometrial cyst of the liver. Am J Gastroenterol. 1986;81:576-578. 9. Grabb A, Carr L, Goodman JD, Mendelson DS, Cohen B, Finkel L. Hepatic endometrioma. J Clin Ultrasound. 1986;14:478-480. 10. Rovati V, Faleschini E, Vercellini P, Nervetti G, Tagliabue G, Benzi G. Endometrioma of the liver. Am J Obstet Gynecol. 1990;163(5 pt 1):1490-1492. 11. Cravello L, D’Ercole C, Le Treut YP, Blanc B. Hepatic endometriosis: a case report. Fertil Steril. 1996;66:657-659. 12. Verbeke C, Harle M, Sturm J. Cystic endometriosis of the upper abdominal organs. Report on three cases and review of the literature. Pathol Res Pract. 1996;192:300-304. 13. Chung CC, Liew CT, Hewitt PM, Leung KL, Lau WY. Endometriosis of the liver. Surgery. 1998;123:106-108. 14. Weinfeld RM, Johnson SC, Lucas CE, Saksouk FA. CT diagnosis of perihepatic endometriosis complicated by malignant transformation. Abdom Imaging. 1998;23:183-184. 15. N’Senda P, Wendum D, Balladur P, Dahan H, Tubiana JM, Arrivé L. Adenosarcoma arising in hepatic endometriosis. Eur Radiol. 2000;10:1287-1289. 16. Inal M, Biçakçi K, Soyupak S, et al. Hepatic endometrioma: a case report and review of the literature. Eur Radiol. 2000;10:431-434. 17. Huang WT, Chen WJ, Chen CL, Cheng YF, Wang JH, Eng HL. Endometrial cyst of the liver: a case report and review of the literature. J Clin Pathol. 2002;55:715-717. 18. Jeanes AC, Murray D, Davidson B, Hamilton M, Watkinson AF. Case report: hepatic and retro-peritoneal endometriosis presenting as obstructive jaundice with ascites: a case report and review of the literature. Clin Radiol. 2002;57:226-229. 19. Khan AW, Craig M, Jarmulowicz M, Davidson BR. Liver tumours due to endometriosis and endometrial stromal sarcoma. HPB (Oxford). 2002;4:43-45. 20. Tuech JJ, Rousselet MC, Boyer J, Descamps P, Arnaud JP, Ronceray J. Endometrial cyst of the liver: case report and review. Fertil Steril. 2003;79:1234-1236. 21. Groves AM, Whitfield R, Lomas DJ, Gibbs P. Imaging of a hepatic endometrioma in a patient with multiple haemangiomas. J Hepatol. 2003;38:547. 22. Reid GD, Kowalski D, Cooper MJ, Kaloo P. Hepatic endometriosis: a case report and review of the literature. Aust N Z J Obstet Gynaecol. 2003;43:87-89.
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Sopha et al 43. Menn KA, Qin L, Fedoriw GD, Gillette ME, McCarthy S. Uterus-like mass: MRI appearance of a very rare entity. J Magn Reson Imaging. 2007;26:162-164. 44. Sharma MC, Sarkar C, Jain D, Suri V, Garg A, Vaishya S. Uterus-like mass of mullerian origin in the lumbosacral region causing cord tethering. Report of two cases. J Neurosurg Spine. 2007;6:73-76. 45. Kaufman Y, Lam A. The pelvic uterus-like mass—a primary or secondary Mullerian system anomaly? J Minim Invasive Gynecol. 2008;15:494-497. 46. Liang YJ, Hao Q, Wu YZ, Wu B. Uterus-like mass in the left broad ligament misdiagnosed as a malformation of the uterus: a case report of a rare condition and review of the literature. Fertil Steril. 2010;93:1347.e13-1347.e16. 47. Shin SY, Kim HJ, Kim YW, Lee KY. CT characteristics of a uterus-like mass in the sigmoid mesocolon. Br J Radiol. 2011;84:e1-e3. 48. Khurana A, Meta A, Sardana M. Extrauterine adenomyoma with uterus like features: a rare entity presenting 17 years post hysterectomy. Indian J Pathol Microbiol. 2011;54: 572-573. 49. Tijani EH, Meryem T, Lamya GA, Abdelouahed J. Giant uterus-like mass of the uterus. Indian J Pathol Microbiol. 2010;53:793-795. 50. Kim HC, Yang DM, Kim SW, Kim GY, Choi SI, Park SJ. Uterus-like mass involving the appendix: US and CT findings. J Clin Ultrasound. 2010;40:518-521. 51. Carvalho FM, Carvalho JP, Pereira RM, Ceccato BP Jr, Lacordia R, Baracat EC. Leiomyomatosis peritonealis disseminata associated with endometriosis and multiple uteruslike mass: report of two cases. Clin Med Insights Case Rep. 2012;5:63-68. 52. Rosai J. Uteruslike mass replacing ovary. Arch Pathol Lab Med. 1982;106:364-365.
139 53. Seki A, Maeshima A, Nakagawa H, et al. A subserosal uterus-like mass presenting after a sliding hernia of the ovary and endometriosis: a rare entity with a discussion of the histogenesis. Fertil Steril. 2011;95:1788.e15-1788. e19. 54. Lax SF, Vang R, Tavassoli FA. In: Tavassoli FA, Deville P, eds. World Health Organization Classification of Tumors. Pathology and Genetics of Tumours of the Breast and Female Genital Organs. Lyon, France: IARC Press; 2003:212-216. 55. Stewart CJ, Leung YC, Mathew R, McCartney AL. Extrauterine adenomyoma with atypical (symplastic) smooth muscle cells: a report of 2 cases. Int J Gynecol Pathol. 2009;28:23-28. 56. Kurman RJ, Funk RL, Kirshenbaum AH. Spina bifida with associated choristoma of Mullerian origin. J Pathol. 1969;99:324-327. 57. Batt RE. Pathogenesis of a parauterine uterus-like mass: developmentally misplaced mullerian tissue—mullerianosis. Fertil Steril. 2010;94:e45. 58. Jung WY, Shin BK, Kim I. Uterine adenomyoma with uterus-like features: a report of two cases. Int J Surg Pathol. 2002;10:163-166. 59. Baker PM, Clement PB, Bell DA, Young RH. Superficial endometriosis of the uterine cervix: a report of 20 cases of a process that may be confused with endocervical glandular dysplasia or adenocarcinoma in situ. Int J Gynecol Pathol. 1999;18:198-205. 60. Young RH, Scully RE. Testicular and paratesticular tumors and tumor-like lesions of ovarian common epithelial and mullerian types. Am J Clin Pathol. 1986;86:146-152. 61. Chu PG, Arber DA, Weiss LM, Chang KL. Utility of CD10 in distinguishing between endometrial stromal sarcoma and uterine smooth muscle tumors: an immunohistochemical comparison of 34 cases. Mod Pathol. 2001;14:465-471.
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research-article2014
IJSXXX10.1177/1066896914534465International Journal of Surgical PathologySopha et al
Case Report
Hepatic Uterus-Like Mass Misdiagnosed as Hepatic Abscess
International Journal of Surgical Pathology 2015, Vol. 23(2) 134–139 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1066896914534465 ijs.sagepub.com
Sabrina C. Sopha, MD1, Flavia G. N. Rosado, MD2, J. J. Smith, MD, PhD3, Nipun B. Merchant, MD4, and Chanjuan Shi, MD, PhD4
Abstract Background. Hepatic endometriosis/uterus-like mass is rare and may be overlooked during hepatic cyst workups. We report a case of uterus-like mass, misdiagnosed as hepatic abscess. Case Report: A 47-year-old woman developed abdominal pain and vomiting. Infectious colitis with hepatic abscess was diagnosed, and remained antibiotic-refractory. Fine-needle aspiration and core biopsies showed benign contents. The patient presented to our institution with symptoms and normal blood work. Laparoscopic excision demonstrated a 1.4-cm cyst composed of endometrial glands (estrogen receptor+ and progesterone receptor+) and stroma (CD10+) with smooth muscle actin (SMA+), arranged in an organoid fashion. The patient, status-post hysterectomy, had no history or symptoms of endometriosis. Conclusion. This rare case illustrates the merit of considering uterus-like mass/endometriosis in the differential diagnosis of antibiotic-refractory hepatic cysts. Cyst heterogeneity may confound needle biopsy. We report the first instance of a hepatic uterus-like mass, with a review of related entities, postulated histogenesis, and important clinical associations. Keywords uterus-like mass, endometriosis, hepatic cyst
Introduction (Case Report) A 47-year-old Caucasian woman with a long history of diarrhea presented to an outside hospital with acute right upper quadrant and back pain with nausea and vomiting. Other pertinent medical history includes right salpingoophorectomy at age 18 years for teratoma, and Caesarian section at age 26 years, wherein a second teratoma was incidentally encountered and resected. There was a remote laparoscopic procedure for possible malrotation, and the patient underwent a supracervical hysterectomy at age 40 years for unclear reasons. She had taken estrogen for 7 years. She had no previous history of endometriosis or pelvic pain. At the time of this presentation, an abdominal computed tomography (CT) scan showed an area of abnormal enhancement, diagnosed as a liver abscess. Stool culture and serum tests were positive for Aeromonas sp and Entamoeba histolytica, respectively. She was diagnosed with infectious enterocolitis and completed 5 days of intravenous piperacilin/tazobactam, 10 days of ertapenem, and 2 weeks of levofloxacin. The patient had several recurrent episodes of right abdominal pain and right chest pain with effusion and was treated with oral and intravenous antibiotics. During this period, a repeat abdominal CT demonstrated a 13-mm fluid collection in segment VII in the perirenal retrohepatic space, with no abnormalities of the genitourinary system
(Figure 1, arrow). A CT-guided fine-needle aspiration of the lesion revealed necrotic debris, histiocytes, and inflammatory cells consistent with an abscess. A CT-guided liver biopsy revealed smooth muscle, interpreted as incidental diaphragmatic sampling. On the fourth episode of symptoms, the patient presented to Vanderbilt University Medical Center. Blood laboratory tests, including liver function tests and electrolytes, were normal, except for mild leukocytosis (11.5 × 103/mL) with a normal differential. The patient’s symptoms and white blood cell count normalized after three days of analgesic treatment. She was referred to surgical oncology for further evaluation. Because of debilitating symptoms, a laparoscopic segment VII excisional biopsy was performed. An intraoperative frozen section showed endometriosis. Formal pathologic evaluation revealed a 1.4-cm hepatic nodule 1
The Johns Hopkins Hospital, Baltimore, MD, USA The Mayo Clinic, Rochester, MN, USA 3 Memorial Sloan-Kettering Cancer Center, New York, NY, USA 4 Vanderbilt University Medical Center, Nashville, TN, USA 2
Corresponding Author: Sabrina C. Sopha, Department of Pathology, The Johns Hopkins Hospital, Weinberg 2267, 201 N. Broadway, Baltimore, MD 21231, USA. Email: [email protected]
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with epitope retrieval solution 1 for 5 minutes and the antibody incubation was 15 minutes. CD10 antigen retrieval was with epitope retrieval solution 2 for 10 minutes and the antibody incubation was 15 minutes.
Discussion
Figure 1. Noncontrast abdominal computed tomography imaging demonstrating a segment VII, peripherally and posteriorly located cystic lesion.
composed of endometrial-type glands and stroma with associated smooth muscle proliferation in layers recapitulating endometrium and myometrium, arranged around a cystic cavity (Figure 2A and B). Estrogen receptor (ER) and progesterone receptor (PR) immunohistochemical stains confirmed the diagnosis (Figure 2C and D). CD10 and smooth muscle actin (SMA) immunohistochemical stains highlighted endometrial stroma and smooth muscle, respectively, with CD10+ endometrial stromal cells “feathering out” into myometrium (Figure 2E and F). The patient has been asymptomatic on follow-up evaluation.
Materials and Methods Fresh liver tissue was fixed in 10% formalin and processed in the standard fashion. Five micrometers thick sections of paraffin-embedded tissue were stained with hematoxylin and eosin according to standard protocol. Immunohistochemical staining was performed as follows: estrogen receptor (ER, clone SP1 rabbit monoclonal, product code 790-4325 from Ventana Medical Systems, Tucson, AZ) and progesterone receptor (PR, clone 1E2 rabbit monoclonal, product code 790-2223 from Ventana Medical Systems, Tucson, AZ) were run on the Ventana Benchmark XT (Ventana Medical Systems, Tucson, AZ) using the Ultraview DAB Detection kit. Antigen retrieval was with cell conditioning 1 for 30 minutes and the antibody incubations were 4 and 8 minutes, respectively. Smooth muscle actin (SMA, clone asm-1 mouse monoclonal, diluted 1:5, product code PA0943, Leica Microsystems, Bannockburn, IL) and CD10 (clone 56C6 mouse monoclonal, predilute, product code PA0270, Leica Microsystems, Bannockburn, IL) were run on the Leica Bondmax (Leica Microsystems, Bannockburn, IL) using the Refine DAB Detection kit. SMA antigen retrieval was
Endometriosis is defined as a “heterotopic island of endometrial mucosa represented with both its glandular and stromal components.”1 The exact “discoverer” of endometriosis is not clear because the designation is complicated by continuing subtleties in terminology, the recognition (or lack thereof) of endometriosis as a pathologic finding, and the inability to recover all scientific and medical literature on the subject. Benagiano and Brosens2,3 discuss these issues and the contributions of Schrön, Rokitansky, von Recklinghausen, Iwanoff, Russel, Mayer, Orloff, Schroeder, Lockyer, Cullen, and Sampson to the field. Involvement of nearly every organ except the spleen has been described,4 and endometriosis has been reported in males.5-7 The first case of hepatic endometriosis was reported separately in 1986 by Finkel et al8 and Grabb et al9. In total, there are 22 reports of 24 cases of hepatic endometriosis in the English literature.8-29 Most of these lesions are cystic or solid-cystic, with intrahepatic, perihepatic, and hepatic capsular surface locations. One case demonstrated continuity with the biliary system,13 while another developed a bronchobiliary fistula.25 A subset of hepatic endometriosis cases are described with secondary tumors, including endometrioid adenosquamous carcinoma,14 adenosarcoma,15 and endometrial stromal sarcoma.19 One case had a coexisting hemangioma.21 Secondary tumors in endometriosis were first reported by Sampson in 1925.30 The ovary is the primary site in 78.7% of cases, and extragonadal sites compose the remaining 21.3%. Tumor subtypes include endometrioid adenocarcinoma, clear-cell carcinoma, sarcoma, and rarer cell types.30 Generally, tumors arising in endometriosis are low grade and confined to the site of origin. The “uterus-like” or “uterine-like” mass was first described by Cozzutto31 in 1981 and is defined as a cavity lined by endometrial-type mucosa surrounded by bundles of smooth muscle cells, with or without gross resemblance to the uterus. Using strict terminology, 23 English reports of 28 cases of “uterus-like,” “uteruslike,” or “uterine-like” masses have been reported in the small bowel, bowel mesentery, ovary, broad ligament, ovarian ligament, uterine cervix, vaginal cuff, lower uterine segment, uterine corpus, conus medullaris, filum terminale, appendix, sigmoid mesocolon, and subserosa.31-51 There have been associations with midline and laterality congenital defects,32,33,35,37,42,44,45,52 endometriosis,31,32,38,45,52,53 and known or presumed estrogenic stimulation33,34,38,41,45 There are rare cases of secondary tumors.34
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Figure 2. (A and B) Hematoxylin and eosin–stained lesional tissue demonstrating the intrahepatic location of endometrial stroma and glands and myometrium composed of smooth muscle arranged in concentric layers around a cystic cavity (20×, 100×). (C and D). Estrogen receptor (ER) and progesterone receptor (PR) immunohistochemical stains demonstrating endometrial coexpression (100×, 100×). (E and F) CD10 and smooth muscle actin (SMA) immunostains demonstrating CD10 expression within endometrial stromal cells, which “feather out” into SMA-expressing myometrial smooth muscle cells (200×, 200×).
Uterus-like masses and adenomyomas are both composed of endometrial glands and stroma and smooth muscle.41,54 Some authors assert that adenomyoma differs from adenomyosis in circumscription,41 and from uterus-like
masses by lack of organoid arrangement.54 Others assert that lesions described as adenomyoma, endomyometriosis, endometriosis, and tumor of Müllerian type reflect essentially identical histopathologic findings as the uterus-like
137
Sopha et al mass and belong to a family of related disease entities with a common histogenesis.39,47,55 In any case, these differing viewpoints may represent extremes of a continuous spectrum of choristoma, a “mass of tissue histologically normal for an organ or part of the body other than the site at which it is located.”56 In the case reported here, the findings of endometrial glands and stroma with abundant smooth muscle proliferation and an organoid arrangement related to a cystic cavity fulfill the criteria of uterus-like mass. There are several theories on the histogenesis of endometriosis and the uterus-like mass (and the related spectrum discussed above), with considerable overlap. The main theories include the Müllerian fusion defect theory (including congenital and heterotopic cases),32,33,35,42,43,48,52,57 the transport/implantation theory,4,12 and the subcoelomic mesenchyme transformation theory (metaplastic theory).* The Müllerian fusion defect theory is supported by the fact that many uterus-like masses occur in association with other midline or laterality defects of organogenesis.32,33,35,37,42,44,45,52 The transport/ implantation theory is supported by the findings of endometrial tissue in anatomically remote organs.8,10,11,26 The metaplastic theory is supported by the association with known or presumed hyperestrogenic states in both males and females5-7,33,34,38,41,45,60 and the association of the uterus-like mass with endometriosis.31,32,38,45,53 The metaplastic theory is additionally supported electron microscopic findings demonstrating smooth muscle fibers and myofibroblasts in the uterus-like mass,31 and by a cytogenetic abnormality similar but not identical to findings in leiomyomas, del2p21, identified in a case of endomyometriosis.1 CD10, a cell surface enzyme found not only in acute lymphoblastic leukemia but also in hormone- or peptide-sensitive tissues such as normal endometrial stroma (but not myometrium),61 may provide additional insight into the histogenesis. Two reports of uterus-like masses or adenoymyomas demonstrate that the respective lesions demonstrated CD10-positive endometrial stroma, with SMA-positive myometrium,48,58 with the assertion that these findings support the metaplastic theory.58 In the case presented here, we report an indistinct junction between the CD10+/SMA− endometrial stroma and CD10−/SMA+ myometrium, with CD10+ endometrial stromal cells “feathering out” into myometrium, lending further support to the theory of metaplasia. The histogenesis debate continues, and it is possible that 2 distinct clinical scenarios exist leading to the rise of endometriosis/ uterus-like masses, and that the 2 theories are not necessarily mutually exclusive. Clinically, right upper quadrant pain and pain along prior implantation sites are common presenting *References 1, 12, 31, 34, 37-41, 46, 47, 49, 53, 58, 59.
symptoms.14,20,21,23,24 Prior bouts of endometriosis are common but these are not found in all cases of hepatic endometriosis.12,24 Ultrasound, CT, and magnetic resonance imaging can be used to support the diagnosis in a peripherally located liver mass, although imaging features vary widely.16 Imaging usually demonstrates a low attenuation, heterogeneous, nonenhancing peripheral mass on CT.14,18,21 Ultrasound can show mixed reflectivity and magnetic resonance imaging can demonstrate increased signal on T1- and T2-weighted images.21 Very large lesions (ie, 12 cm) may cause mass effects resulting in hepatic dysfunction18 or portal vein obstruction.19 Correlation with imaging can aid the pathologist in the differential diagnosis of hepatic cysts. Although in isolation, the small glands may resemble primitive vascular structures, the imaging findings of a cyst, without contrast characteristics of a vascular lesion, in combination with classic morphology showing an organoid arrangement of glands and endometrial stroma with a layer of smooth muscle, should direct the pathologist toward the diagnosis of uterus-like mass, rather than a primitive vascular tumor. Surgical resection of the uterus-like mass/endometriosis lesion is curative.
Conclusion This rare case illustrates the need for high suspicion of endometriosis/uterus-like mass in any patient with a cystic liver lesion refractory to broad-spectrum antibiotics. Moreover, given the heterogeneous nature of solid-cystic endometriomas, which can reach large sizes, and because of the possibility of harboring secondary tumors, fine needle biopsy or core biopsy may not be representative of lesional identity. Minimally invasive laparoscopic excision, as in this case, is a therapeutic approach which can provide a definitive diagnosis, prevent the overuse of antibiotics, exclude/prophylaxe the possibility of secondary malignancies, and improve or eliminate painful symptoms. The unusual location and immunophenotype provide insight into the histogenesis of endometriosis and uteruslike mass lesions. A literature review shows that the finding of a uterus-like mass should prompt investigation of other midline or laterality defects, particularly spinal or genitourinary. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The author(s) received no financial support for the research, authorship, and/or publication of this article.
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