{"paper_id":"15732d98-acc5-4fc8-995a-4f0776a0e8fe","body_text":"The Role of CD10 Staining in Distinguishing Invasive\nEndometrial Adenocarcinoma from Adenocarcinoma\nInvolving Adenomyosis\nAlessandra F. Nascimento, M.D., Michelle S. Hirsch, M.D., Ph.D., Aida Cviko, M.D., Ph.D.,\nBradley J. Quade, M.D., Ph.D., Marisa R. Nucci, M.D.\nDepartment of Pathology, Division of Women’s and Perinatal Pathology, Brigham and Women’s Hospital\nand Harvard Medical School, Boston, Massachusetts\nAdenomyosis may be involved by endometrial ade-\nnocarcinoma, but in contrast to true myometrial\ninvasion, the depth of an adenomyotic focus in-\nvolved by carcinoma does not alter pathologic tu-\nmor staging. Therefore, distinction from carcinoma\ninvading myometrium is clinically relevant. We hy-\npothesized that CD10, a marker of non-neoplastic\nand neoplastic endometrial stroma, would highlight\nthe stromal component of adenomyotic foci and be\nuseful in this distinction. Thirty-nine cases of endo-\nmetrial adenocarcinoma were analyzed and divided\ninto three groups: I, invasive endometrial adenocar-\ncinoma (n /H1154914); II, endometrial adenocarcinoma\ninvolving adenomyosis but without myometrial in-\nvasion (n /H1154918); and III, adenomyosis involved by\nendometrial adenocarcinoma with concomitant in-\nvasive component (n /H115497). All cases of adenomyosis\ninvolved by endometrial adenocarcinoma demon-\nstrated CD10 expression in the stromal cells of ad-\nenomyotic foci. Eleven of 21 cases (52%) of invasive\nadenocarcinoma also showed CD10 expression, at\nleast focally, in cells immediately surrounding the\ninfiltrating glands. Of these, two cases (from Group\nIII) also had associated adenomyotic involvement\nby carcinoma. The remaining cases of invasive car-\ncinoma were negative for CD10. Therefore, pres-\nence of CD10 staining immediately surrounding\nneoplastic glands does not equate with involvement\nof adenomyosis by endometrial adenocarcinoma.\nIn contrast, absence of CD10 expression excludes\ninvolvement of adenomyosis by adenocarcinoma.\nKEY WORDS: Adenomyosis, CD10, Endometrial ad-\nenocarcinoma, Endometrial stroma.\nMod Pathol 2003;16(1):22–27\nAdenomyosis is usually defined as endometrial\nglands and stroma located in the wall of the uterus\nat least one low-power field away from the surface\nendometrium. It affects reproductive-aged women\nwith a history of multiple pregnancies, appears to\nbe associated with estrogen therapy (1, 2), and may\neven be a clonal process (3). Although endometrial\nadenocarcinoma may arise in foci of adenomyosis\n(4 –9), adenomyosis is more often secondarily in-\nvolved by endometrial adenocarcinoma that has\narisen in surface endometrium. The distinction be-\ntween this condition and true myometrial invasion\nby endometrial adenocarcinoma may sometimes\nbe difficult, particularly if there is extensive involve-\nment of adenomyosis by adenocarcinoma, if the\nsecondarily involved adenomyosis extends deeply\ninto the uterine wall, or if the presence of adeno-\nmyosis is masked by subtotal replacement by ade-\nnocarcinoma. This distinction is important because\npathological staging, and consequentially, therapy\nis dependent on the presence and depth of invasion\n(10). In contrast, involvement of adenomyosis by\nendometrial adenocarcinoma carries no adverse\nprognostic significance (11, 12). We hypothesized\nthat CD10, a marker of non-neoplastic and neoplas-\ntic endometrial stroma (13–15), would be useful in\nthis distinction by highlighting the stroma of ad-\nenomyotic foci involved by endometrial adenocar-\ncinoma and being absent around foci of invasion.\nMATERIALS AND METHODS\nThirty-nine cases corresponding to hysterectomy\nspecimens removed between the years of 1998 and\nCopyright © 2003 by The United States and Canadian Academy of\nPathology, Inc.\nVOL. 16, NO. 1, P. 22, 2003 Printed in the U.S.A.\nDate of acceptance: October 3, 2002.\nSupported by a grant (RPG CNE-100283) from the American Cancer\nSociety (BJQ).\nPresented in part at the United States and Canadian Pathology Meeting,\nChicago, IL, 2002.\nAddress reprint requests to: Marisa R. Nucci, M.D., Department of Pa-\nthology, Division of Women’s and Perinatal Pathology, Brigham and\nWomen’s Hospital, 75 Francis Street, Boston, MA 02115; e-mail:\nmnucci@partners.org; fax: 617-277-9015.\nDOI: 10.1097/01.MP.0000043523.03519.FC\n22\n\n2001 for pathological diagnoses of endometrial ad-\nenocarcinoma were retrieved from the surgical files\nof the Women’s and Perinatal Pathology Division of\nthe Brigham and Women ’s Hospital (Boston, MA).\nIn all cases, hematoxylin-and-eosin (H&E) stained\nsections were available for review, and the diag-\nnoses were confirmed. The endometrial carcinoma\nwas graded using the FIGO staging system (10).\nThe cases were subsequently divided into three\ngroups. Group I consisted of cases of invasive en-\ndometrial adenocarcinoma. Group II included\nspecimens with endometrial adenocarcinoma in-\nvolving adenomyosis but without myometrial inva-\nsion. Group III was composed of cases with adeno-\nmyosis involved by endometrial adenocarcinoma\nwith coexistent myometrial invasion. Invasion of\nthe myometrium was based on established criteria\n(16); features of invasion included irregular pattern\nof infiltration, irregular glandular outlines, alter-\nations in the cytomorphology of the neoplastic cells\n(particularly eosinophilic change to the cytoplasm),\nand presence of periglandular desmoplasia, edema,\nand inflammation.\nAll cases were stained for CD10 (Novocastra Lab-\noratories, LTD, Tyne, U.K.) using mouse monoclo-\nnal antibody (clone 56C6), at a dilution of 1:80. After\nhigh-temperature antigen retrieval, the sections\nwere incubated for 60 minutes with the primary\nantibody at 25 °C, followed by the standard ABC\ntechnique. The stain was considered positive when\npresent, at least focally, immediately surrounding\nthe neoplastic glands. Non-neoplastic surface en-\ndometrial stromal cells and stroma present in un-\ninvolved foci of adenomyosis were used as an in-\nternal positive control.\nNine cases in which there was available mate-\nrial (seven cases in Group I and two cases in\nGroup III) were stained with antibody to the mus-\ncle markers desmin (monoclonal clone D33; dilu-\ntion 1:500; DAKO Corporation, Carpinteria, CA)\nand h-caldesmon (monoclonal clone h-CD; dilu-\ntion 1:300; DAKO). The latter antibody required\n30 minutes of antigen retrieval. The myometrium\nwas used as an internal positive control.\nRESULTS\nA summary of the immunohistochemical results\nfor CD10 in all groups is summarized in Table 1.\nGroup I: Invasive Endometrial Adenocarcinoma\nGroup I included 14 cases of invasive endome-\ntrial adenocarcinoma. Patients ’ ages ranged be-\ntween 49 and 77 years (median, 60.5 y). Twelve of 14\ncases (85.7%) were diagnosed as endometrial ade-\nnocarcinoma, endometrioid subtype. Two cases\nhad mixed endometrioid, papillary serous, and\nclear cell features. Six cases were Grade 1, four were\nGrade 2, and four were Grade 3 (of 3 grades). Three\nof fourteen cases (21.4%) showed additional unin-\nvolved foci of adenomyosis. All tumors but one\nshowed myometrial invasion ranging from 10 to\n95% of the myometrial thickness (median 50%); one\nadenocarcinoma superficially invaded a submuco-\nsal leiomyoma.\nFive of the 14 cases (35.8%) showed absence of\nCD10 staining in cells adjacent to the invasive\nglands (Fig. 1A –B). However, 9 of the 14 cases\n(64.2%) revealed CD10 expression in cells immedi-\nately surrounding the neoplastic glands (Fig. 2A –B).\nOf these nine cases, four cases had a circumferen-\ntial staining pattern, whereas five showed only focal\nstaining ( /H1102150% of the gland circumference). In\neight of the nine cases (89%) with CD10 expression\nsurrounding invasive glands, CD10-expressing cells\nwere part of a desmoplastic reaction. In the remain-\ning case, there was no desmoplastic reaction by\nH&E examination and, although the invasive bor-\nder was rounded, the extent and pattern of invasion\nwere consistent with invasive adenocarcinoma.\nImmunoperoxidase stains for desmin and\nh-caldesmon, performed in seven of the nine tu-\nmors with CD10-expressing cells, revealed in five of\nthem scattered rare positive cells for both markers\nin the cells that were also positive for CD10, includ-\ning the one tumor with a rounded border of inva-\nsion. The staining was weaker than in the adjacent\nmyometrium. In the other two cases in which CD10\nwas positive, both muscle markers were negative in\nthe cells immediately surrounding the invasive\nTABLE 1. Summary of CD10 Staining\nGroup CD10/H11001\nInvasive\nCD10/H11002\nInvasive\nCD10/H11001\nAdenomyosis\nCD10/H11002\nAdenomyosis\nI 9/14 a (64.2) 5/14 (35.7) N/A N/A\nII N/A N/A 18/18 (100) 0/18 (0)\nIII 2/7 b (28.5) 5/7 (71.4) 7/7 (100) 0/7 (0)\nAll data are n (%).\nN/A, not applicable; Group I, invasive endometrial adenocarcinoma; Group II, endometrial adenocarcinoma involving adenomyosis without\nmyometrial invasion; Group III, endometrial adenocarcinoma involving adenomyosis with myometrial invasion.\na Focal in five cases.\nb Focal in one case.\nCD10 Staining and Endometrial Adenocarcinoma (A.F. Nascimento et al .) 23\n\nglands. In general, the expression of the muscle\nmarkers was weaker than in the surrounding myo-\nmetrium and more focal than in the CD10-\nexpressing cells (Fig. 3A –B).\nGroup II: Endometrial Adenocarcinoma Involving\nAdenomyosis But without Myometrial Invasion\nGroup II included 18 cases of endometrial ade-\nnocarcinoma involving adenomyosis without myo-\nmetrial invasion. Patients ’ ages ranged from 40 to\n83 years of age (median, 60.5 y). All carcinomas\nwere of the endometrioid subtype, with a predom-\ninance of Grade 1 tumors (13 of 18; 72.2%). Four\ntumors were classified as Grade 2 and one as Grade\n3 (of 3). Two cases also had foci of adenomyosis\nuninvolved by carcinoma. Strong and diffuse CD10\nexpression in the endometrial stromal cells of ad-\nenomyotic foci immediately around neoplastic\nglands was present in all cases (Fig. 4A –B).\nGroup III: Adenomyosis Involved by Endometrial\nAdenocarcinoma with Coexistent\nMyometrial Invasion\nGroup III included seven cases of endometrial\nadenocarcinoma with involvement of adenomyosis\nand coexistent myometrial invasion. Patient age\nranged between 36 and 69 years (median 55 y). Six\nof seven cases (85.7%) were subclassified as endo-\nmetrioid type; one case had an admixed papillary\nserous component, which accounted for approxi-\nmately 20% of the tumor. The depth of invasion\nvaried from 25 to 60% of the myometrial thickness\n(median 40%). Four of seven tumors (57.1%) were\nGrade 2, one tumor was Grade 1, and two tumors\nwere Grade 3 (of 3 grades).\nAll tumors showed CD10 staining around foci of\nadenomyosis (Fig. 5); however, two cases (28.5%)\nalso exhibited CD10 staining immediately sur-\nrounding foci of invasive adenocarcinoma. In the\nFIGURE 1. A, B, invasive endometrial adenocarcinoma (H&E stain).\nC, lack of CD10 staining around the neoplastic glands. Intraluminal and\nstromal granulocytes are an internal positive control.\nFIGURE 2. A, invasive adenocarcinoma with accompanying\ndesmoplastic reaction (H&E stain). B, CD10-expressing cells are present\nimmediately adjacent to the invasive focus.\n24 Modern Pathology\n\nother five cases, cells surrounding the invasive\nglands were negative for CD10 (Fig. 5). Correlation\nbetween H&E- and immunoperoxidase-stained\nsections demonstrated that one of the two tumors\nwith CD10-positive cells immediately adjacent to\ninvasive carcinoma corresponded with a peritu-\nmoral desmoplastic reaction. The other case\nshowed direct invasion into the myometrium with-\nout definitive desmoplastic reaction. In these two\ncases, the muscle markers for desmin and caldes-\nmon were also positive in these peritumoral cells,\nalthough in a weaker and more focal manner com-\npared with surrounding myometrium.\nDISCUSSION\nThe prevalence of adenomyosis is quite variable,\nranging from 10 to 88%, probably reflecting differ-\ning criteria and low diagnostic reproducibility (17 –\n20). Diagnostic criteria for adenomyosis varies\nwidely, but the most widely accepted one is the\nseparation of a candidate focus from the surface\nendometrium by at least one low-power field (4 /H11003\nmagnification). Recently, a distance of /H113503 mm from\nthe endomyometrial junction and the presence of\nconcentric myometrial hyperplasia has been pro-\nposed as more reliable diagnostic criterion (17). The\nrisk factors for and the pathophysiology of adeno-\nmyosis are unclear. Multiparity (21) and constant\nestrogen exposure, such as tamoxifen therapy (1, 2),\nare believed to be associated with its development.\nPandis et al. (3) found clonal deletion of the long\narm of chromosome 7 in three cases, raising the\npossibility of a neoplastic process.\nAdenomyosis may be associated with or be con-\ncurrently involved by endometrial hyperplasia and\nadenocarcinoma. The latter situation may, in some\ninstances, give rise to diagnostic difficulty with re-\ngard to assessment of depth of myometrial inva-\nsion. This distinction is clinically relevant because\ndepth of invasion is an important independent\nprognostic factor for patients with endometrial ad-\nenocarcinoma (10). Although adenomyosis might\nbe located deep within the myometrium, its in-\nvolvement by endometrial adenocarcinoma does\nnot alter the patient ’s stage. Deep involvement of\nadenomyosis by endometrial adenocarcinoma\nwithout myometrial invasion has been shown to\nhave a more favorable prognosis than tumors inva-\nsive to a similar depth (11, 12). In a study of 18\npatients, Mittal et al. (22) showed that adenocarci-\nnomas of low histologic grade confined to adeno-\nmyosis had an excellent prognosis.\nFIGURE 3. A, invasive endometrial adenocarcinoma (H&E stain). B,\nfocal desmin-expressing cells are present immediately adjacent to the\ninvasive glands (myometrium as internal positive control); these cells\nalso expressed CD10.\nFIGURE 4. A, partial replacement of adenomyotic focus by\nendometrial adenocarcinoma without myometrial invasion (H&E stain).\nB, the stromal cells of the adenomyotic focus are positive for CD10.\nCD10 Staining and Endometrial Adenocarcinoma (A.F. Nascimento et al .) 25\n\nCommon acute lymphoblastic leukemia antigen\n(CALLA), or CD10, is a monomeric Type II integral\nmembrane peptidase expressed by lymphoid pro-\ngenitor cells found in normal bone marrow and\nthymus, and by mature granulocytes (23). It also is\nexpressed in some acute lymphoid leukemias, such\nas acute lymphoblastic leukemia, and some non-\nHodgkin’s lymphomas, such as follicular and Bur-\nkitt’s lymphomas (23). Besides hematopoietic tis-\nsues and malignancies, non-neoplastic non-\nhematopoietic tissues such as renal tubular and\nglomerular cells, small intestine epithelium, normal\nand malignant cells of the epithelium of the stom-\nach and colon, and myoepithelial cells of the breast\nalso express CD10 (24 –27). CD10 has also been\nshown to stain non-neoplastic and neoplastic en-\ndometrial stroma and thus may be helpful in the\ndifferential diagnosis of uterine stromal and\nsmooth muscle neoplasm (13, 15, 28). On the basis\nof these findings, we hypothesized that CD10 would\nbe a useful biomarker in the distinction of adeno-\nmyosis involved by endometrial adenocarcinoma\nfrom myoinvasive endometrial adenocarcinoma.\nBecause adenomyotic foci contain endometrial\nstroma, CD10 expression would be expected to be\npresent surrounding neoplastic glands involving\nsuch foci. In contrast, CD10-positive cells would\nnot be expected to be present around adenocarci-\nnoma invading myometrium.\nOur results demonstrate that endometrial adeno-\ncarcinoma involving adenomyosis is surrounded by\nCD10-expressing stromal cells reflecting the expected\npresence of endometrial stroma within adenomyotic\nfoci. However, in cases of invasive adenocarcinoma,\nwith or without associated adenomyotic involvement\nby carcinoma, invasive neoplastic glands were at least\npartially bounded by a rim of CD10-expressing cells in\n11 of 21 (52%) cases. The cells expressing CD10 cor-\nresponded to desmoplastic stromal cells in 9 cases\n(82%). In the remaining 2 cases, CD10-expressing\ncells not associated with desmoplasia were present\nsurrounding the invasive glands. Possible explana-\ntions for CD10 staining in these 11 cases include the\nfollowing: (1) the positive cells are endometrial stro-\nmal cells and the foci interpreted as invasion are\nactually occult involvement of adenomyosis, rather\nthan true myometrial invasion; (2) expression of\nCD10 by myometrial smooth muscle cells; (3) expres-\nsion of CD10 by fibroblasts within the desmoplastic\nreaction; (4) spurious expression of a CD10 epitope in\nanother protein; (5) tumor invasion accompanied by\nendometrial stroma; and (5) possible induction of\nstromal differentiation by the invasive tumor.\nThe first proposition, occult involvement of adeno-\nmyosis by carcinoma, can be excluded because the\ncases in this study were carefully examined and es-\ntablished criteria were cautiously applied to avoid this\npitfall. Furthermore, the neoplastic glands, with or\nwithout surrounding desmoplastic reaction, showed\nan invasive pattern with irregular borders and ab-\nsence of endometrial stroma or residual uninvolved\nendometrial glands indicative of adenomyosis. The\nseparation of endometrial stroma from myometrium\nby CD10 expression is hindered by the observation\nthat CD10 can be weakly and focally expressed by the\nmyometrial smooth muscle (28). The application of\ndesmin and h-caldesmon did not clearly identify the\nCD10-expressing cells immediately surrounding the\ninvasive carcinoma as myometrium. Although\nFIGURE 5. A, B, endometrial adenocarcinoma with involvement of\nadenomyosis and coexistent myometrial invasion. Focus of\nadenomyosis involved by endometrial adenocarcinoma (on left) and\nfocus of invasive tumor (on right). C, CD10 is positive in the stromal\ncells in the adenomyotic focus but absent in cells surrounding the\ninvasive focus.\n26 Modern Pathology\n\ndesmin and caldesmon were positive in these cells,\nthe staining pattern was weaker and more scattered\nwhen compared with the surrounding myometrium.\nIn our opinion, these findings did not support a\nsmooth muscle origin for these cells. Expression of\nCD10 by fibroblasts within the desmoplastic reaction,\nspurious expression of a CD10 epitope in another\nprotein, tumor invasion accompanied by endometrial\nstroma, and possible induction of stromal differenti-\nation by the invasive tumor are all reasonable possi-\nbilities that may be more definitively addressed by\nother, perhaps molecular, studies in the future.\nIn summary, involvement of adenomyosis by en-\ndometrial adenocarcinoma and its differentiation\nfrom invasive endometrial adenocarcinoma may in\nsome instances be diagnostically difficult. CD10 ex-\npression reliably identifies adenomyosis, but CD 10\nexpression may also be seen around foci of invasive\ncarcinoma. Thus, the presence of CD10 immediately\nsurrounding neoplastic glands does not equate with\ninvolvement of adenomyosis by endometrial adeno-\ncarcinoma, whereas absence of CD10 expression is\nindicative of invasive endometrial adenocarcinoma\nand excludes involvement of adenomyosis.\nREFERENCES\n1. Cohen I, Beyth Y, Tepper R, Figer A, Shapira J, Cordoba M, et\nal. Adenomyosis in postmenopausal breast cancer patients\ntreated with tamoxifen: a new entity? Gynecol Oncol 1995;\n58:86 –91.\n2. Cohen I, Beyth Y, Shapira J, Tepper R, Fishman A, Cordoba\nM, et al. High frequency of adenomyosis in postmenopausal\nbreast cancer patients treated with tamoxifen. Gynecol Ob-\nstet Invest 1997;44:200 –5.\n3. Pandis N, Karaiskos C, Bardi G, Sfikas K, Tserkezoglou A,\nFoliou S, et al. Chromosome analysis of uterine adenomyo-\nsis. 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CD10\n(CALLA) positive/h-caldesmon negative immunophenotype\neffectively distinguishes endometrial stromal tumors from\nuterine smooth muscle tumors [abstract]. Mod Pathol 2002;\n15:198A.\nCD10 Staining and Endometrial Adenocarcinoma (A.F. Nascimento et al .) 27","source_license":"CC0","license_restricted":false}