Gastric-type mucinous carcinoma of the cervix and its precursors - historical overview.
adenocarcinoma
cervix
gastric-type
mucinous
pathology
Journal
Histopathology
ISSN: 1365-2559
Titre abrégé: Histopathology
Pays: England
ID NLM: 7704136
Informations de publication
Date de publication:
Jan 2020
Jan 2020
Historique:
entrez:
18
12
2019
pubmed:
18
12
2019
medline:
13
8
2020
Statut:
ppublish
Résumé
The emerging concept of gastric-type mucinous carcinoma (GAS) of the uterine cervix has been accepted worldwide because of its aggressive clinical behaviour and the absence of high-risk human papillomavirus (HPV). GAS is included as a variant of mucinous carcinoma in the 2014 World Health Organization classification, and its recognition has provoked a discussion on endocervical adenocarcinoma as a single entity such that endocervical adenocarcinoma is now divided into HPV-associated and HPV-independent groups. This article reviews historical and conceptual aspects of GAS and its precursors, starting with minimal deviation adenocarcinoma (MDA), through the ensuing confusion, up to the recent paradigm shift in cervical adenocarcinoma subclassification. The gastric immunophenotype of MDA was demonstrated by a Japanese group in 1998 using the HIK1083 antibody, which recognises gastric pyloric gland mucin, and this elucidated the pathogenesis of this particular tumour. However, this information resulted in overdiagnosis of lobular endocervical glandular hyperplasia (LEGH), first described in 1999 and which represents pyloric gland metaplasia (PGM), as malignant. In the early 2000s the relationship between MDA and LEGH/PGM became a matter of controversy. In 2007 HIK1083 immunohistochemistry extended the morphological spectrum of endocervical adenocarcinoma showing gastric differentiation beyond MDA, which resulted in the proposal of GAS as a distinct entity including MDA as its very well-differentiated subtype. GAS is now considered to be an aggressive and chemoresistant neoplasm that is not related to high-risk HPV. The LEGH/PGM-GAS sequence is currently regarded as an HPV-independent pathway of carcinogenesis. Understanding the underlying molecular events in this process is key to the development of biomarkers for early detection and molecular targeted therapy.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
102-111Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Stolnicu S, Barsan I, Hoang L et al. International endocervical adenocarcinoma criteria and classification (IECC): a new pathogenetic classification for invasive adenocarcinomas of the endocervix. Am. J. Surg. Pathol. 2018; 42; 214-226.
Gusserow ALS. Ueber sarcoma des uterus. Arch. Gynakol. 1870; 1; 240-251.
McKelvey JL, Goodlin RR. Adenoma malignum of the cervix; a cancer of deceptively innocent histological pattern. Cancer 1963; 16; 549-557.
Silverberg SG, Hurt WG. Minimal deviation adenocarcinoma (‘adenoma malignum’) of the cervix: a reappraisal. Am. J. Obstet. Gynecol. 1975; 121; 971-975.
Kaku T, Enjoji M. Extremely well-differentiated adenocarcinoma (‘adenoma malignum’) of the cervix. Int. J. Gynecol. Pathol. 1983; 2; 28-41.
Gilks CB, Young RH, Aguirre P, DeLellis RA, Scully RE. Adenoma malignum (minimal deviation adenocarcinoma) of the uterine cervix. A clinicopathological and immunohistochemical analysis of 26 cases. Am. J. Surg. Pathol. 1989; 13; 717-729.
Scully RE, Bonfiglio TA, Kurman RJ, Silverberg SG, Wilkinson EJ. Histological typing of female genital tumours. 2nd ed. Berlin: Springer-Verlag, 1994.
Tavassoli FA, Devilee P eds. World Health Organization classification of tumours. Pathology and genetics of tumours of the breast and female genital organs. Lyon: IARC Press, 2003.
Fukushima M, Shimano S, Yamakawa Y et al. The detection of human papillomavirus (HPV) in a case of minimal deviation adenocarcinoma of the uterine cervix (adenoma malignum) using in situ hybridization. Jpn. J. Clin. Oncol. 1990; 20; 407-412.
Ferguson AW, Svoboda-Newman SM, Frank TS. Analysis of human papillomavirus infection and molecular alterations in adenocarcinoma of the cervix. Mod. Pathol. 1998; 11; 11-18.
Toki T, Zhai YL, Park JS, Fujii S. Infrequent occurrence of high-risk human papillomavirus and of p53 mutation in minimal deviation adenocarcinoma of the cervix. Int. J. Gynecol. Pathol. 1999; 18; 215-219.
Xu JY, Hashi A, Kondo T et al. Absence of human papillomavirus infection in minimal deviation adenocarcinoma and lobular endocervical glandular hyperplasia. Int. J. Gynecol. Pathol. 2005; 24; 296-302.
Ishii K, Hosaka N, Toki T et al. A new view of the so-called adenoma malignum of the uterine cervix. Virchows Arch. 1998; 432; 315-322.
Ishihara K, Kurihara M, Goso Y et al. Peripheral alpha-linked N-acetylglucosamine on the carbohydrate moiety of mucin derived from mammalian gastric gland mucous cells: epitope recognized by a newly characterized monoclonal antibody. Biochem. J. 1996; 318(Pt 2); 409-416.
Hayashi I, Tsuda H, Shimoda T. Reappraisal of orthodox histochemistry for the diagnosis of minimal deviation adenocarcinoma of the cervix. Am. J. Surg. Pathol. 2000; 24; 559-562.
Choi CG, Kim SH, Kim JS, Chi JG, Song ES, Han MC. Adenoma malignum of uterine cervix in Peutz-Jeghers syndrome: CT and US features. J. Comput. Assist. Tomogr. 1993; 17; 819-821.
Tsuruchi N, Tsukamoto N, Kaku T, Kamura T, Nakano H. Adenoma malignum of the uterine cervix detected by imaging methods in a patient with Peutz-Jeghers syndrome. Gynecol. Oncol. 1994; 54; 232-236.
Yamashita Y, Takahashi M, Katabuchi H, Fukumatsu Y, Miyazaki K, Okamura H. Adenoma malignum: MR appearances mimicking nabothian cysts. Am. J. Roentgenol. 1994; 162; 649-650.
Doi T, Yamashita Y, Yasunaga T et al. Adenoma malignum: MR imaging and pathologic study. Radiology 1997; 204; 39-42.
Jones MA, Young RH, Scully RE. Diffuse laminar endocervical glandular hyperplasia. A benign lesion often confused with adenoma malignum (minimal deviation adenocarcinoma). Am. J. Surg. Pathol. 1991; 15; 1123-1129.
Clement PB, Young RH. Deep nabothian cysts of the uterine cervix. A possible source of confusion with minimal-deviation adenocarcinoma (adenoma malignum). Int. J. Gynecol. Pathol. 1989; 8; 340-348.
Segal GH, Hart WR. Cystic endocervical tunnel clusters. A clinicopathologic study of 29 cases of so-called adenomatous hyperplasia. Am. J. Surg. Pathol. 1990; 14; 895-903.
Ferry JA, Scully RE. Mesonephric remnants, hyperplasia, and neoplasia in the uterine cervix. A study of 49 cases. Am. J. Surg. Pathol. 1990; 14; 1100-1111.
Young RH, Clement PB. Endocervicosis involving the uterine cervix: a report of four cases of a benign process that may be confused with deeply invasive endocervical adenocarcinoma. Int. J. Gynecol. Pathol. 2000; 19; 322-328.
Nucci MR, Clement PB, Young RH. Lobular endocervical glandular hyperplasia, not otherwise specified: a clinicopathologic analysis of thirteen cases of a distinctive pseudoneoplastic lesion and comparison with fourteen cases of adenoma malignum. Am. J. Surg. Pathol. 1999; 23; 886-891.
Mikami Y, Hata S, Fujiwara K, Imajo Y, Kohno I, Manabe T. Florid endocervical glandular hyperplasia with intestinal and pyloric gland metaplasia: worrisome benign mimic of ‘adenoma malignum’. Gynecol. Oncol. 1999; 74; 504-511.
Mikami Y, Manabe T. Lobular endocervical glandular hyperplasia represents pyloric gland metaplasia? Am. J. Surg. Pathol. 2000; 24; 323-324; author reply 325-326.
Fetissof F, Heitzman A, Machet MC, Lansac J. Unusual endocervical lesions with endocrine cells. Pathol. Res. Pract. 1993; 189; 928-939.
Tsuda H, Mikami Y, Kaku T et al. Reproducible and clinically meaningful differential diagnosis is possible between lobular endocervical glandular hyperplasia and ‘adenoma malignum’ based on common histopathological criteria. Pathol. Int. 2005; 55; 412-418.
Sasajima Y, Mikami Y, Kaku T et al. Gross features of lobular endocervical glandular hyperplasia in comparison with minimal-deviation adenocarcinoma and stage Ib endocervical-type mucinous adenocarcinoma of the uterine cervix. Histopathology 2008; 53; 487-490.
Yoden E, Mikami Y, Fujiwara K, Kohno I, Imajo Y. Florid endocervical glandular hyperplasia with pyloric gland metaplasia: a radiologic pitfall. J. Comput. Assist. Tomogr. 2001; 25; 94-97.
Mikami Y, McCluggage WG. Endocervical glandular lesions exhibiting gastric differentiation: an emerging spectrum of benign, premalignant, and malignant lesions. Adv. Anat. Pathol. 2013; 20; 227-237.
Ito M, Minamiguchi S, Mikami Y et al. Peutz-Jeghers syndrome-associated atypical mucinous proliferation of the uterine cervix: a case of minimal deviation adenocarcinoma (‘adenoma malignum’) in situ. Pathol. Res. Pract. 2012; 208; 623-627.
Kobayashi Y, Masuda K, Kimura T et al. A tumor of the uterine cervix with a complex histology in a Peutz-Jeghers syndrome patient with genomic deletion of the STK11 exon 1 region. Future Oncol. 2014; 10; 171-177.
Takei Y, Fujiwara H, Nagashima T, Takahashi Y, Takahashi S, Suzuki M. Successful pregnancy in a Peutz-Jeghers syndrome patient with lobular endocervical glandular hyperplasia. J. Obstet. Gynaecol. Res. 2015; 41; 468-473.
Mikami Y, Kiyokawa T, Hata S et al. Gastrointestinal immunophenotype in adenocarcinomas of the uterine cervix and related glandular lesions: a possible link between lobular endocervical glandular hyperplasia/pyloric gland metaplasia and ‘adenoma malignum’. Mod. Pathol. 2004; 17; 962-972.
Kondo T, Hashi A, Murata S et al. Endocervical adenocarcinomas associated with lobular endocervical glandular hyperplasia: a report of four cases with histochemical and immunohistochemical analyses. Mod. Pathol. 2005; 18; 1199-1210.
Nara M, Hashi A, Murata S et al. Lobular endocervical glandular hyperplasia as a presumed precursor of cervical adenocarcinoma independent of human papillomavirus infection. Gynecol. Oncol. 2007; 106; 289-298.
Takeuchi K, Tsujino T, Sugimoto M, Yoshida S, Kitazawa S. Endocervical adenocarcinoma associated with lobular endocervical glandular hyperplasia showing rapid reaccumulation of hydrometra. Int. J. Gynecol. Cancer 2008; 18; 1285-1288.
Ohta Y, Suzuki T, Hamatani S, Shiokawa A, Kushima M, Ota H. Lobular endocervical glandular hyperplasia might become a precursor of adenocarcinoma with pyloric gland features. Pathol. Res. Pract. 2008; 204; 683-687.
Nishio S, Tsuda H, Fujiyoshi N et al. Clinicopathological significance of cervical adenocarcinoma associated with lobular endocervical glandular hyperplasia. Pathol. Res. Pract. 2009; 205; 331-337.
Tsuji T, Togami S, Nomoto M et al. Uterine cervical carcinomas associated with lobular endocervical glandular hyperplasia. Histopathology 2011; 59; 55-62.
Mikami Y, Kojima A, Kiyokawa T, Manabe T. Ki67 labelling index and p53 status indicate neoplastic nature of atypical lobular endocervical glandular hyperplasia (ALEGH). Histopathology 2009; 55; 362-364.
Kawauchi S, Kusuda T, Liu XP et al. Is lobular endocervical glandular hyperplasia a cancerous precursor of minimal deviation adenocarcinoma? A comparative molecular-genetic and immunohistochemical study. Am. J. Surg. Pathol. 2008; 32; 1807-1815.
Matsubara A, Sekine S, Ogawa R et al. Lobular endocervical glandular hyperplasia is a neoplastic entity with frequent activating GNAS mutations. Am. J. Surg. Pathol. 2014; 38; 370-376.
Takatsu A, Miyamoto T, Fuseya C et al. Clonality analysis suggests that STK11 gene mutations are involved in progression of lobular endocervical glandular hyperplasia (LEGH) to minimal deviation adenocarcinoma (MDA). Virchows Arch. 2013; 462; 645-651.
Kojima A, Mikami Y, Sudo T et al. Gastric morphology and immunophenotype predict poor outcome in mucinous adenocarcinoma of the uterine cervix. Am. J. Surg. Pathol. 2007; 31; 664-672.
Vang R, Gown AM, Farinola M et al. p16 expression in primary ovarian mucinous and endometrioid tumors and metastatic adenocarcinomas in the ovary: utility for identification of metastatic HPV-related endocervical adenocarcinomas. Am. J. Surg. Pathol. 2007; 31; 653-663.
Kusanagi Y, Kojima A, Mikami Y et al. Absence of high-risk human papillomavirus (HPV) detection in endocervical adenocarcinoma with gastric morphology and phenotype. Am. J. Pathol. 2010; 177; 2169-2175.
Houghton O, Jamison J, Wilson R, Carson J, McCluggage WG. p16 immunoreactivity in unusual types of cervical adenocarcinoma does not reflect human papillomavirus infection. Histopathology 2010; 57; 342-350.
Park KJ, Kiyokawa T, Soslow RA et al. Unusual endocervical adenocarcinomas: an immunohistochemical analysis with molecular detection of human papillomavirus. Am. J. Surg. Pathol. 2011; 35; 633-646.
Kawakami F, Mikami Y, Kojima A, Ito M, Nishimura R, Manabe T. Diagnostic reproducibility in gastric-type mucinous adenocarcinoma of the uterine cervix: validation of novel diagnostic criteria. Histopathology 2010; 56; 551-553.
Mikami Y, Minamiguchi S, Teramoto N, Nagura M, Haga H, Konishi I. Carbonic anhydrase type IX expression in lobular endocervical glandular hyperplasia and gastric-type adenocarcinoma of the uterine cervix. Pathol. Res. Pract. 2013; 209; 173-178.
Carleton C, Hoang L, Sah S et al. A detailed immunohistochemical analysis of a large series of cervical and vaginal gastric-type adenocarcinomas. Am. J. Surg. Pathol. 2016; 40; 636-644.
Stolnicu S, Barsan I, Hoang L et al. Diagnostic algorithmic proposal based on comprehensive immunohistochemical evaluation of 297 invasive endocervical adenocarcinomas. Am. J. Surg. Pathol. 2018; 42; 989-1000.
Asaka S, Nakajima T, Momose M, Miyamoto T, Uehara T, Ota H. Trefoil factor family 2 protein: a potential immunohistochemical marker for aiding diagnosis of lobular endocervical glandular hyperplasia and gastric-type adenocarcinoma of the uterine cervix. Virchows Arch. 2019; 474; 79-86.
Karamurzin YS, Kiyokawa T, Parkash V et al. Gastric-type endocervical adenocarcinoma: an aggressive tumor with unusual metastatic patterns and poor prognosis. Am. J. Surg. Pathol. 2015; 39; 1449-1457.
Kido A, Mikami Y, Koyama T et al. Magnetic resonance appearance of gastric-type adenocarcinoma of the uterine cervix in comparison with that of usual-type endocervical adenocarcinoma: a pitfall of newly described unusual subtype of endocervical adenocarcinoma. Int. J. Gynecol. Cancer 2014; 24; 1474-1479.
Kojima A, Shimada M, Mikami Y et al. Chemoresistance of gastric-type mucinous carcinoma of the uterine cervix: a study of the Sankai Gynecology Study Group. Int. J. Gynecol. Cancer 2018; 28; 99-106.
Kurman RJ, Carcangiu ML, Herrington CS, Young RH eds. Glandular tumours and precursors. In World Health Organization classification of tumours of female reproductive organs. 4th ed. Lyon: IARC Press, 2014; 183-194.
Mikami Y. Non-human-papillomavirus (HPV)-related adenocarcinomas and their precursors. In Herrington CS ed. Pathology of the cervix. Cham: Springer International Publishing, 2017; 185-199.
Rodriguez-Carunchio L, Soveral I, Steenbergen RD et al. HPV-negative carcinoma of the uterine cervix: a distinct type of cervical cancer with poor prognosis. BJOG 2015; 122; 119-127.
Miura S, Matsumoto K, Oki A et al. Do we need a different strategy for HPV screening and vaccination in East Asia? Int. J. Cancer 2006; 119; 2713-2715.
Sheng Z, Minato H, Sasagawa T et al. Detection of high-risk human papillomavirus subtypes in cervical glandular neoplasia by in situ hybridization. Int. J. Clin. Exp. Pathol. 2013; 6; 2168-2177.
Baalbergen A, Ewing-Graham PC, Eijkemans MJ, Helmerhorst TJ. Prognosis of adenocarcinoma of the uterine cervix: p53 expression correlates with higher incidence of mortality. Int. J. Cancer 2007; 121; 106-110.
Zielinski GD, Snijders PJ, Rozendaal L et al. The presence of high-risk HPV combined with specific p53 and p16INK4a expression patterns points to high-risk HPV as the main causative agent for adenocarcinoma in situ and adenocarcinoma of the cervix. J. Pathol. 2003; 201; 535-543.
Fujiwara K, Monk B, Devouassoux-Shisheboran M. Adenocarcinoma of the uterine cervix: why is it different? Curr. Oncol. Rep. 2014; 16; 416.
Hopkins MP, Morley GW. A comparison of adenocarcinoma and squamous cell carcinoma of the cervix. Obstet. Gynecol. 1991; 77; 912-917.
Irie T, Kigawa J, Minagawa Y et al. Prognosis and clinicopathological characteristics of Ib-IIb adenocarcinoma of the uterine cervix in patients who have had radical hysterectomy. Eur. J. Surg. Oncol. 2000; 26; 464-467.
Shimada M, Kigawa J, Nishimura R et al. Ovarian metastasis in carcinoma of the uterine cervix. Gynecol. Oncol. 2006; 101; 234-237.
Landoni F, Maneo A, Colombo A et al. Randomised study of radical surgery versus radiotherapy for stage Ib-IIa cervical cancer. Lancet 1997; 350; 535-540.
Nishio S, Mikami Y, Tokunaga H et al. Analysis of gastric-type mucinous carcinoma of the uterine cervix - an aggressive tumor with a poor prognosis: a multi-institutional study. Gynecol. Oncol. 2019; 153; 13-19.
Holl K, Nowakowski AM, Powell N et al. Human papillomavirus prevalence and type-distribution in cervical glandular neoplasias: results from a European multinational epidemiological study. Int. J. Cancer 2015; 137; 2858-2868.
Talia KL, Stewart CJR, Howitt BE, Nucci MR, McCluggage WG. HPV-negative gastric type adenocarcinoma in situ of the cervix: a spectrum of rare lesions exhibiting gastric and intestinal differentiation. Am. J. Surg. Pathol. 2017; 41; 1023-1033.
Mikami Y, Kiyokawa T, Sasajima Y et al. Reappraisal of synchronous and multifocal mucinous lesions of the female genital tract: a close association with gastric metaplasia. Histopathology 2009; 54; 184-191.
Takatsu A, Shiozawa T, Miyamoto T et al. Preoperative differential diagnosis of minimal deviation adenocarcinoma and lobular endocervical glandular hyperplasia of the uterine cervix: a multicenter study of clinicopathology and magnetic resonance imaging findings. Int. J. Gynecol. Cancer 2011; 21; 1287-1296.
Omori M, Kondo T, Nakazawa K et al. Interpretation of endocervical cells with gastric-type mucin on pap smears: a proposal for a cytologic category ‘atypical endocervical cells with gastric-type mucin’. Am. J. Clin. Pathol. 2018; 150; 255-269.
Nagaria T, Garg S, Stockley T, Clark B, Bernardini MQ, Rouzbahman M. Molecular landscape of gastric-type endocervical adenocarcinomas (GAS) - next generation sequencing of 14 cases. Lab. Invest. 2018; 98; 440.
Mills AM, Liou S, Kong CS, Longacre TA. Are women with endocervical adenocarcinoma at risk for Lynch syndrome? Evaluation of 101 cases including unusual subtypes and lower uterine segment tumors. Int. J. Gynecol. Pathol. 2012; 31; 463-469.