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Clinicopathological Characteristics and KRAS Mutation Status of Endometrial Mucinous Metaplasia and Carcinoma JI-YOUN SUNG 1, YOON YANG JUNG 2 and HYUN-SOO KIM 3

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Clinicopathological Characteristics and KRAS Mutation Status of Endometrial Mucinous Metaplasia and Carcinoma JI-YOUN SUNG 1, YOON YANG JUNG 2 and HYUN-SOO KIM 3 ANTICANCER RESEARCH 38 : 2779-2786 (2018) doi:10.21873/anticanres.12521 Clinicopathological Characteristics and KRAS Mutation Status of Endometrial Mucinous Metaplasia and Carcinoma JI-YOUN SUNG 1, YOON YANG JUNG 2 and HYUN-SOO KIM 3 1Department of Pathology, Kyung Hee University School of Medicine, Seoul, Republic of Korea; 2Department of Pathology, Myongji Hospital, Goyang, Republic of Korea; 3Department of Pathology, Severance Hospital, Yonsei University College of Medicine, Seoul, Republic of Korea Abstract. Background/Aim: Mucinous metaplasia of the papillary mucinous metaplasia suggests that papillary endometrium occurs as a spectrum of epithelial alterations mucinous metaplasia may be a precancerous lesion of a ranging from the formation of simple, tubular glands to certain subset of mucinous carcinomas of the endometrium. architecturally complex glandular proliferation with intraglandular papillary projection and cellular tufts. Endometrial metaplasia is defined as epithelial differentiation Endometrial mucinous metaplasia often presents a diagnostic that differs from the conventional morphological appearance challenge in endometrial curettage. Materials and Methods: of the endometrial glandular epithelium (1). Endometrial We analyzed the clinicopathological characteristics and the mucinous metaplasia is particularly relevant as it is mutation status for V-Ki-ras2 Kirsten rat sarcoma viral frequently encountered in endometrial curettage specimens oncogene homolog (KRAS) of 11 cases of endometrial obtained from peri-menopausal or postmenopausal women mucinous metaplasia. Electronic medical record review and (2). Mucinous epithelial lesions of the endometrium present histopathological examination were performed. KRAS a frequent disparity between cytological atypia and mutation status was analyzed using a pyrosequencing architectural alteration, and often present significant technique. Results: Cases were classified histopathologically diagnostic challenges to pathologists. Endometrial mucinous into simple (5/11) or papillary (6/11) mucinous metaplasias. metaplasia can occur as a spectrum of alterations ranging All (6/6) papillary mucinous metaplasias were associated with from benign-appearing simple mucinous epithelium to atypical hyperplasia/endometrioid intraepithelial neoplasia malignant-appearing complex epithelial proliferation (1). It (AH/EIN; 1/6) or carcinoma (5/6), whereas in a single patient is often encountered in hyperestrogenic states or in with simple mucinous metaplasia, grade 1 endometrioid postmenopausal women receiving hormone replacement carcinoma was incidentally detected. The difference in therapy (1). Even though endometrial mucinous metaplasia frequency of association of the metaplasia with AH/EIN or is typically asymptomatic, when associated with endometrial carcinoma was significant (p=0.015). KRAS mutations were polyps, it may present with menorrhagia, metrorrhagia, identified in five out of six cases of papillary mucinous dysmenorrhea, and postmenopausal bleeding (3). metaplasias, comprising three cases with G12D and two with Endometrial mucinous metaplasia can be also associated G12V mutations; the frequency of KRAS mutation was with cervical stenosis and may produce mucometra (4). significantly higher (p=0.015) than in cases of simple Furthermore, it was recently shown to be associated with mucinous metaplasia (0/5). Conclusion: Papillary mucinous concurrent or subsequent endometrial neoplastic lesions (2). metaplasia is frequently associated with endometrial Endometrial endometrioid carcinomas frequently exhibit neoplastic lesions. The high incidence of KRAS mutations in mucinous differentiation, and a subset of such cases are classified as mucinous carcinomas, when the tumor possesses 50% or more of mucinous components (2). Mucinous carcinoma is an uncommon type of endometrial carcinoma Correspondence to: Hyun-Soo Kim, Department of Pathology, comprising fewer than 10% of endometrial carcinomas, and Severance Hospital, Yonsei University College of Medicine, 50-1 includes specific variants such as low-grade mucinous Yonsei-ro, Seodaemun-gu, Seoul 03722, Republic of Korea. Tel: +82 222281794/+82 23620860, e-mail: [email protected] carcinoma and microglandular adenocarcinoma (5-10). It has been hypothesized that subtypes of endometrial mucinous Key Words: Endometrium, papillary, mucinous, metaplasia, metaplasia are pathogenetically related to endometrial carcinoma, KRAS . carcinoma as possible precursor lesions, and different 2779 ANTICANCER RESEARCH 38 : 2779-2786 (2018) morphological classification systems have been proposed to mucinous lesions were classified histopathologically as either predict the risk of subsequent endometrial carcinoma (4, 11- simple or papillary mucinous metaplasia (5). Simple mucinous 13). Classification of endometrial mucinous metaplasia into metaplasia referred to cases in which simple, tubular-shaped glands were lined by a single layer of columnar, mucin-containing simple and papillary lesion-type based on the presence of epithelium and had a flat luminal border. In contrast, papillary intraglandular papillary tufts and complex glandular mucinous metaplasia referred either to cases with intraluminally architecture, was recently proposed (2, 5, 12). Papillary projecting papillary tufts with or without fibrovascular cores, or to mucinous metaplasia has a high incidence of mutations of V- cases with complex or cribriform mucinous glandular architecture Ki-ras2 Kirsten rat sarcoma viral oncogene homolog ( KRAS ), without malignant nuclear features. In addition, endometrial suggesting that it may be a possible precursor lesion of hyperplasia was classified according to the 2014 World Health mucinous carcinoma of the endometrium (2, 5). Organization into two groups: hyperplasia without atypia, and AH/EIN (16). Any subsequently available endometrial curettage, To date, only few studies have investigated the resectoscopic endometrial polypectomy, or hysterectomy specimens clinicopathological and molecular features of mucinous were obtained and examined histopathologically. metaplasia of the endometrium. The small numbers of studies regarding endometrial mucinous metaplasia suggest that it is Pyrosequencing. Depending on the size of the tissue sample, quite a rare entity. In this study, we report our experience with genomic deoxyribonucleic acid (DNA) was extracted from six to a series of 11 patients who presented with simple or papillary ten 10- μm-thick formalin-fixed, paraffin-embedded slices using a mucinous metaplasia of the endometrium. We herein present Maxwell CSC DNA FFPE Kit (Promega Corporation, Madison, WI, USA). The lesions were macrodissected with a scalpel and a thorough analysis of the clinicopathological characteristics transferred to 1.5 ml tubes for tissue digestion. The quality and and KRAS mutation status of these cases and a discussion of concentration of the extracted DNA was determined using a relevant literature. NanoDrop spectrophotometer (Thermo Fisher Scientific, Fremont, CA, USA), and adjusted to a concentration of 50 ng/ μl. Materials and Methods Pyrosequencing analysis of KRAS codons 12, 13, and 61 was performed using Therascreen KRAS Pyro Kit (Qiagen, Valencia, Case selection. This study (4-2017-0987) was reviewed and CA, USA) according to manufacturer’s recommendations. Two approved by the Institutional Review Board at the Severance nanograms of DNA was used per analysis, and polymerase chain Hospital (Seoul, Republic of Korea). The cases were extracted from reaction amplification of the target region was performed on a T100 computerized files of the Department of Pathology at the Severance Thermal Cycler (Bio-Rad Laboratories, Hercules, CA, USA). For Hospital (Seoul, Republic of Korea). A thorough search of archived the pyrosequencing reaction on the PyroMark Q24 System (Qiagen), surgical pathology cases was performed using the key words amplicons were immobilized to the wells of a PyroMark Q24 Plate “endometrium,” “mucinous metaplasia,” and “mucinous (Qiagen) using Streptavidin Sepharose High Performance (GE differentiation”. From January 2015 to September 2017, 11 patients Healthcare Life Sciences, Uppsala, Sweden). Pyrosequencing results were diagnosed as having mucinous metaplasia of the endometrium. were analyzed using PyroMark Q24 Software version 2.0 (Qiagen) The relevant patient electric medical records were reviewed. The with Therascreen KRAS Plug-in Report (Qiagen). clinical profile data including age at the time of diagnosis, menopausal status, coexisting gynecological lesions, association Results with endometrial atypical hyperplasia/endometrioid intraepithelial neoplasia (AH/EIN) or carcinoma, and International Federation of Clinical characteristics. Eleven patients with an average age Gynecology and Obstetrics (FIGO) grade (14) and stage (15) of of 53.9 years (range=40-62 years) were included in our associated endometrial carcinoma were extracted. study. Table I summarizes the clinical characteristics of 11 patients with endometrial mucinous metaplasia. Nine patients Pathological examination. Resected tissues (obtained by were postmenopausal. The endometrial tissue was obtained gynecological oncology surgeons at the Severance Hospital) were from hysterectomies and polypectomies in eight and three initially examined by pathologists before fixation in 10% neutral- patients, respectively. The clinical reasons for hysterectomy buffered formalin for 12-24 hours. The tissues were then thoroughly included endometrial carcinoma
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