Journal of Pathology and Translational Medicine

Original Article

Evaluation of human papillomavirus (HPV) prediction using the International Endocervical Adenocarcinoma Criteria and Classification system, compared to p16 immunohistochemistry and HPV RNA in-situ hybridization: Hezhen Ren, Jennifer Pors, Christine Chow, Monica Ta, Simona Stolnicu, Robert Soslow, David Huntsman, Lynn Hoang; J Pathol Transl Med. 2020;54(6):480-488. Published online August 31, 2020; DOI: https://doi.org/10.4132/jptm.2020.07.18

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Background
The International Endocervical Adenocarcinoma Criteria and Classification (IECC) separated endocervical adenocarcinomas into human papillomavirus (HPV) associated (HPVA) and non–HPV-associated (NHPVA) categories by morphology alone. Our primary objective was to assess the accuracy of HPV prediction by the IECC system compared to p16 immunohistochemistry and HPV RNA in-situ hybridization (RISH). Our secondary goal was to directly compare p16 and HPV RISH concordance.
Methods
Cases were classified by IECC and stained for p16 and HPV RISH on tissue microarray, with discordant p16/HPV RISH cases re-stained on whole tissue sections. Remaining discordant cases (p16/HPV, IECC/p16, IECC/HPV discordances) were re-reviewed by the original pathologists (n = 3) and external expert pathologists (n = 2) blinded to the p16 and HPV RISH results. Final IECC diagnosis was assigned upon independent agreement between all reviewers.
Results
One hundred and eleven endocervical adenocarcinomas were classified originally into 94 HPVA and 17 NHPVA cases. p16 and HPV RISH was concordant in 108/111 cases (97%) independent of the IECC. HPV RISH and p16 was concordant with IECC in 103/111 (93%) and 106/111 (95%), respectively. After expert review, concordance improved to 107/111 (96%) for HPV RISH. After review of the eight discordant cases, one remained as HPVA, four were reclassified to NHPVA from HPVA, two were unclassifiable, and one possibly represented a mixed usual and gastric-type adenocarcinoma.
Conclusions
p16 and HPV RISH have excellent concordance in endocervical adenocarcinomas, and IECC can predict HPV status in most cases. Focal apical mitoses and apoptotic debris on original review led to the misclassification of several NHPVA as HPVA.

Citations

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Joint detection of multiple HPV-testing technologies and evaluation of clinicopathological characteristics discriminate between HPV-independent and low-copy HPV-associated cervical squamous cell carcinoma (CSCC) -an analysis of 3869 cases
Linghui Lu, Tianqi Liu, Shunni Wang, Jing Li, Feiran Zhang, Yan Ning, Yiqin Wang
Gynecologic Oncology.2023; 170: 59. CrossRef
Incidence and Clinicopathologic Characteristics of Human Papillomavirus–independent Invasive Squamous Cell Carcinomas of the Cervix
Simona Stolnicu, Douglas Allison, Aaron M. Praiss, Basile Tessier-Cloutier, Amir Momeni Boroujeni, Jessica Flynn, Alexia Iasonos, Rene Serrette, Lien Hoang, Andrei Patrichi, Cristina Terinte, Anna Pesci, Claudia Mateoiu, Ricardo R. Lastra, Takako Kiyokawa
American Journal of Surgical Pathology.2023; 47(12): 1376. CrossRef
Testing Algorithms for the Diagnosis of Malignant Glandular Tumors of the Uterine Cervix Histotyped per the International Endocervical Adenocarcinoma Criteria and Classification (IECC) System
Máire A. Duggan, Qiuli Duan, Ruth M. Pfeiffer, Mary Anne Brett, Sandra Lee, Mustapha Abubakar, Martin Köbel, Monica Rodriguez, Aylin Sar
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Local and Metastatic Relapses in a Young Woman with Papillary Squamous Cell Carcinoma of the Uterine Cervix
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Pathology.2022; 54(5): 548. CrossRef
Reproducibility of Morphologic Parameters of the International Endocervical Adenocarcinoma Criteria and Classification System and Correlation With Clinicopathologic Parameters: A Multi-Institutional Study
Pinar Bulutay, Nihan Haberal, Özlem Özen, Özlem Erdem, Emine H. Zeren, İbrahim Kulac, Çagatay Taskiran, Dogan Vatansever, Ali Ayhan, Nilgün Kapucuoğlu
International Journal of Gynecological Pathology.2022; 41(5): 447. CrossRef
HPV-Negative Cervical Cancer: A Narrative Review
Francesca Arezzo, Gennaro Cormio, Vera Loizzi, Gerardo Cazzato, Viviana Cataldo, Claudio Lombardi, Giuseppe Ingravallo, Leonardo Resta, Ettore Cicinelli
Diagnostics.2021; 11(6): 952. CrossRef
International Endocervical Adenocarcinoma Criteria and Classification (IECC): An Independent Cohort With Clinical and Molecular Findings
Hezhen Ren, Noorah Almadani, Jennifer Pors, Samuel Leung, Julie Ho, Christine Chow, Monica Ta, Kay J. Park, Simona Stolnicu, Robert Soslow, David Huntsman, Blake C. Gilks, Lynn Hoang
International Journal of Gynecological Pathology.2021; 40(6): 533. CrossRef

Case Study

A Pyloric Gland-Phenotype Ovarian Mucinous Tumor Resembling Lobular Endocervical Glandular Hyperplasia in a Patient with Peutz-Jeghers Syndrome: Eun Na Kim, Gu-Hwan Kim, Jiyoon Kim, In Ah Park, Jin Ho Shin, Yun Chai, Kyu-Rae Kim; J Pathol Transl Med. 2017;51(2):159-164. Published online August 22, 2016; DOI: https://doi.org/10.4132/jptm.2016.07.01

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7 Web of Science
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Abstract PDF

We describe an ovarian mucinous neoplasm that histologically resembles lobular endocervical glandular hyperplasia (LEGH) containing pyloric gland type mucin in a patient with Peutz-Jeghers syndrome (PJS). Although ovarian mucinous tumors rarely occur in PJS patients, their pyloric gland phenotype has not been clearly determined. The histopathologic features of the ovarian mucinous tumor were reminiscent of LEGH. The cytoplasmic mucin was stained with periodic acid-Schiff reaction after diastase treatment but was negative for Alcian blue pH 2.5, suggesting the presence of neutral mucin. Immunohistochemically, the epithelium expressed various gastric markers, including MUC6, HIK1083, and carbonic anhydrase-IX. Multiple ligation-dependent probe amplification detected a germline heterozygous deletion mutation at exons 1–7 of the STK11 gene (c.1-?_920+?del) in peripheral blood leukocytes and mosaic loss of heterozygosity in ovarian tumor tissue. Considering that LEGH and/or gastric-type cervical adenocarcinoma can be found in patients with PJS carrying germline and/or somatic STK11 mutations, our case indicates that STK11 mutations have an important role in the proliferation of pyloric-phenotype mucinous epithelium at various anatomical locations.

Citations

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Ovarian Mucinous Tumor Presenting Atypical Lobular Endocervical Glandular Hyperplasia-Like Appearance in a Patient With Germline STK11 p.F354L Variant: A Case Report
Hiroshi Yoshida, Kengo Hiranuma, Mariko Nakahara, Mayumi Kobayashi-Kato, Yasuhito Tanase, Masaya Uno, Kouya Shiraishi, Mitsuya Ishikawa, Tomoyasu Kato
International Journal of Surgical Pathology.2024; 32(2): 394. CrossRef
Preoperative multimodal ultrasonic imaging in a case of Peutz-Jeghers syndrome complicated by atypical lobular endocervical glandular hyperplasia: a case report and literature review
Liwen Yang, Duan Duan, Ying Xiong, Tianjiao Liu, Lijun Zhao, Fan Lai, Dingxian Gu, Liuying Zhou
Hereditary Cancer in Clinical Practice.2024;[Epub] CrossRef
Gastric‐type glandular lesions of the female genital tract excluding the cervix: emerging pathological entities
Richard W‐C Wong, Karen L Talia, W Glenn McCluggage
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Gastric-phenotype Mucinous Carcinoma of the Fallopian Tube with Secondary Ovarian Involvement in a Woman with Peutz-Jeghers Syndrome: A Case Report
Mónica Bronte Anaut, Javier Arredondo Montero, Maria Pilar Fernández Seara, Rosa Guarch Troyas
International Journal of Surgical Pathology.2023; 31(1): 92. CrossRef
Molecular characterization of gastric-type endocervical adenocarcinoma using next-generation sequencing
Swati Garg, Teddy S. Nagaria, Blaise Clarke, Orit Freedman, Zanobia Khan, Joerg Schwock, Marcus Q. Bernardini, Amit M. Oza, Kathy Han, Adam C. Smith, Tracy L. Stockley, Marjan Rouzbahman
Modern Pathology.2019; 32(12): 1823. CrossRef
The developing spectrum of gastric-type cervical glandular lesions
Karen L. Talia, W. Glenn McCluggage
Pathology.2018; 50(2): 122. CrossRef

Original Articles

Endocervical Glandular Lesions in Invasive and Intraepithelial Squamous Neoplasms of the Uterine Cervix.: Hye Kyoung Yoon, Mi Sun Kang, Young Ju Kim; Korean J Pathol. 1996;30(10):912-919.

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Abstract PDF: The incidence of adenocarcinoma of the uterine cervix had shown an increasing tendency, and which is related to the increased use of oral contraceptives or prevalent in human papillomavirus infection. Endocervical glandular dysplasia or adenocarcinoma in situ are occasionally associated with squamous neoplasms of the uterine cervix. This study was aimed to evaluate the histologic features and the incidence of endocervical glandular lesions associated with squamous neoplasms, the presence of human papillomavirus infection-suggesting histologic findings in adjacent squamous neoplasms and the immmunohistochemical findings of endocervical glandular lesions for carcinoembryonic antigen. The materials used were 105 cases of microinvasive and invasive squamous cell carcinoma, and 83 cases of squamous intraepithelial lesions which are consisted of 142 radical or total hystrectomy products and 46 conization or loop excision products. The results are as follows; 1. Among 188 cases, six cases(3.2%) had shown foci of high grade glandular dyaplasia, and 19 cases(10.1%) revealed the areas of low grade glandular dysplasia. There was no adenocarcinoma in situ case. 2. In four of six high grade glandular dysplasia cases, microinvasive or invasive squamous cell carcinomas were associated. In low grade glandular dysplasias, sqaumous intraepithelial lesions were occcupying 68.4%. 3. HPV infection-suggesting histologic findings had accompanied all high grade glandular dysplasia cases and in 17 cases(89.5%) of 19 low grade glandular dysplasias. 4. In 2 of 5 high grade glandular dysplasias and in 1 of 19 low grade glandular dysplasias, the immunohistochemical reaction for carcinoembryonic antigen was similar to that of adenocarcinoma. In conclusion, the clinicopathologic importance of endocervical glandular lesions associated with squamous neoplasms of the uterine cervix should be kept in mind, and further study for the relationship between endocervical glandular lesions and human papillomavirus infection or hormonal influence will be continued.

Expressions of p53 and MIB-1 in Glandular Lesions of the Uterine Cervix.: Seo Young Park, Mee Young Sol, Hye Kyoung Yoon; Korean J Pathol. 1999;33(8):589-595.

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Abstract PDF: The glandular lesions of the uterine cervix can be classified into endocervical glandular dysplasia (EGD), adenocarcinoma in situ (AIS) and adenocarcinoma, but the diagnostic criteria and the continuity of endocervical glandular lesions are still controversial. The aim of this study was to evaluate the significance of immunohistochemical findings of p53 and MIB-1 in the discrimination and the continuity of EGD, AIS and adenocarcinoma. The materials for the study included 11 cases of adenocarcinoma, 7 cases of AIS, 12 cases of high grade EGD, and 19 cases of low grade EGD. Also included were eleven benign glandular lesions (5 cases of tuboendometrial metaplasia, 3 cases of mesonephric remnant, 3 cases of microglandular hyperplasia). A strong reaction of more than 5% of the glandular epithelial nuclei was interpreted as positive for p53 protein. MIB-1 expression was analyzed semiquantitatively as negative, 1 , 2 , 3 , depending on the percentage of positive nuclei (less than 1%, 1~9%, 10~39%, > or = 40%, respectively). p53 protein expression was found in 3 (27.3%) out of 11 cases of adenocarcinoma, and 2 (28.6%) out of 7 cases of AIS. But all of high and low grade EGD cases were negative. High MIB-1 labelling index (> or =10%) was found in all adenocarcinoma cases and in 3 (42.9%) out of 7 cases of AIS. But only 2 (17.7%) out of 12 cases of high grade EGD showed high MIB-1 labelling index, and all of low grade EGD and benign lesions showed negligible MIB-1 positivities. In summary, MIB-1 labelling index might be valuable in the discrimination of malignant glandular lesions and endocervical glandular dysplasia from benign lesions, but p53 expression could be a useful parameter in the discrimination of malignant glandular lesions from endocervical glandular dysplasia and benign lesions.

Expressions of MIB-1, p53 and CEA in Endocervical Glandular Lesions.: Mi Jin Kim, Young Gi Lee, Dong Sug Kim; Korean J Pathol. 2001;35(1):41-47.

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Abstract PDF: BACKGROUND
Endocervical glandular lesions include glandular atypia (GA), endocervical glandular dysplasia (EGD), adenocarcinoma in situ (AIS), and invasive adenocarcinoma (IA). The diagnosis of malignant glandular lesions is occasionally difficult to distinguish from benign mimickers, and the morphologic features of EGD remain unsettled.
METHODS
Immunohistochemical stains for MIB-1, p53 and CEA were performed on 81 cases of paraffin-embedded endocervical glandular lesions including 22 IA, 15 AIS, 15 EGD, 13 GA, 8 microglandular hyperplasia (MGH) and 8 tubal metaplasia (TM).
RESULTS
The MIB-1 labelling index of IA was 59.68%, 69.53% for AIS, 26.60% for EGD, 16.03% for benign. p53 overexpression was noted in 4 (18%) cases of IA, 3 (20%) of AIS, but none of EGD and benign lesions. It was Interesting to note that one case of MGH showed p53 staining in low intensity. Diffuse strong cytoplasmic CEA positivity was present in all of IA and AIS, whereas seven (47%) of 15 EGD and 12 (41%) of 29 benign lesions showed focal cytoplasmic CEA positivity. There were significant differences in MIB-1 and CEA immunostainings among the adenocarcinoma, EGD, and benign glandular lesions. Adenocarcinoma was closely related to p53 overexpression, although occurring in a low percentage of the cases.
CONCLUSION
MIB-1 immunostaining can be useful in differentiating among endocervical adenocarcinoma, endocervical glandular dysplasia and benign glandular lesions. p53 overexpression might be helpful in the diagnosis of adenocarcinoma.

Cytologic Analysis of Adenocarcinoma of the Cervicovaginal Smears .: Jung Yeon Kim, Hye Jae Cho, Kyung Ja Cho, Hong Kyoon Lee; Korean J Cytopathol. 1998;9(2):147-154.

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Abstract PDF: We have investigated the cervicovaginal smears in order to define the cytologic features of uterine adenocarcinomas. Total 22 cases were reviewed(12 cases from the Sanggye Paik hospital, Inje university and 10 cases from the Korea Cancer Center Hospital) from January 1992 to December 1997. Five cases were endometrial adenocarcinomas and the remaining 17 cases were cervical adenocarcinomas. Se venteen cases of cervical adenocarcinomas were divided into endometrioid(6 cases), endocervical(7 cases), mixed endometrioid and endocervical(1 case), papillary (2 cases), and adenosquamous(1 case) carcinomas. The background of endocervical adenocarcinoma was hemorrhagic or inflammatory. The tumor diathesis was less prominent than that of the squamous cell carcinoma. The prominent features of the endocervical type adenocarcinomas were large and loose clusters, large intra cytoplasmic vacuoles, and prominent overlapping and peripheral palisading of nuclei. In contrast, the endometrioid adenocarcinomas showed small and compact clusters, and small intracytoplasmic vacuoles. The detection rate of endometrial adeno carcinoma was lower than that of the endocervical adenocarcinoma.

Histochemical and Immunohistochemical Properties of Endometrial and Endocervical Adenocarcinoma.: Kyu Rae Kim, In Joon Choi; Korean J Pathol. 1988;22(3):259-267.

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Abstract PDF: The histologic differentiation of endometrial and endocervical adenocarcinomas is a common diagnostic problum of clinical importance, because the staging, treatment and prognosis of these lesions are quite different. First, we examined the distribution of acid mucin in endometrial and endocervical adenocarcinoma (23 cases and 25 cases repectively), but distinguishing differences between endometrial and endocervical adenocarcinoma, especially of endometrioid type, were not observed. Secondly, the distribution of low-molecular weight cytokeratin, vimentin and carcino-embryonic antigen (CEA) by immunohistochemistry were examined in formalin-fixed tissues. CEA was present in 88% of endocervical adenocarcinomas and 34.8% of endometrial adenocarcinoma. vimentin was found in 91.3% of endometrial adenocarcinomas, in contrast with only in 16% of endocervical adenocarcinomas. This study showed that the presence of vimentin in neoplastic glands, in which CEA is negative, may be helpful in the differential diagnosis of endometrial from endocervical adenocarcinomas.

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