The European Society of Gynaecological Oncology (ESGO), the International Society for the Study of Vulvovaginal Disease (ISSVD), the European College for the Study of Vulval Disease (ECSVD), and the European Federation for Colposcopy (EFC) Consensus Statement on the Management of Vaginal Intraepithelial Neoplasia.
Journal
Journal of lower genital tract disease
ISSN: 1526-0976
Titre abrégé: J Low Genit Tract Dis
Pays: United States
ID NLM: 9704963
Informations de publication
Date de publication:
01 Apr 2023
01 Apr 2023
Historique:
entrez:
23
3
2023
pubmed:
24
3
2023
medline:
28
3
2023
Statut:
ppublish
Résumé
The European Society of Gynaecological Oncology (ESGO), the International Society for the Study of Vulvovaginal Disease (ISSVD), the European College for the Study of Vulval Disease (ECSVD), and the European Federation for Colposcopy (EFC) developed consensus statements on pre-invasive vulvar lesions in order to improve the quality of care for patients with vaginal intraepithelial neoplasia (VaIN). The management of VaIN varies according to the grade of the lesion: VaIN 1 (low grade vaginal squamous intraepithelial lesions (SIL)) can be subjected to follow-up, while VaIN 2-3 (high-grade vaginal SIL) should be treated. Treatment needs individualization according to the patient's characteristics, disease extension and previous therapeutic procedures. Surgical excision is the mainstay of treatment and should be performed if invasion cannot be excluded. Total vaginectomy is used only in highly selected cases of extensive and persistent disease. Carbon dioxide (CO2) laser may be used as both an ablation method and an excisional one. Reported cure rates after laser excision and laser ablation are similar. Topical agents are useful for persistent, multifocal lesions or for patients who cannot undergo surgical treatment. Imiquimod was associated with the lowest recurrence rate, highest human papillomavirus (HPV) clearance, and can be considered the best topical approach. Trichloroacetic acid and 5-fluorouracil are historical options and should be discouraged. For VaIN after hysterectomy for cervical intraepithelial neoplasia (CIN) 3, laser vaporization and topical agents are not the best options, since they cannot reach epithelium buried in the vaginal scar. In these cases surgical options are preferable. Brachytherapy has a high overall success rate but due to late side effects should be reserved for poor surgical candidates, having multifocal disease, and with failed prior treatments. VaIN tends to recur and ensuring patient adherence to close follow-up visits is of the utmost importance. The first evaluation should be performed at 6 months with cytology and an HPV test during 2 years and annually thereafter. The implementation of vaccination against HPV infection is expected to contribute to the prevention of VaIN and thus cancer of the vagina. The effects of treatment can have an impact on quality of life and result in psychological and psychosexual issues which should be addressed. Patients with VaIN need clear and up-to-date information on a range of treatment options including risks and benefits, as well as the need for follow-up and the risk of recurrence.
Identifiants
pubmed: 36951985
doi: 10.1097/LGT.0000000000000732
pii: 00128360-202304000-00005
pmc: PMC10026974
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
131-145Informations de copyright
Copyright © 2023 ESGO, ISSVD, EFC, ECSVD. Published by Wolters Kluwer Health, Inc. on behalf of the ASCCP.
Déclaration de conflit d'intérêts
The authors have declared they have no conflicts of interest.
Références
Preti M, Joura E, Vieira-Baptista P, et al. The European Society of Gynaecological Oncology (ESGO), the International Society for the Study of Vulvovaginal Disease (ISSVD), the European College for the Study of Vulval Disease (ECSVD) and the European Federation for Colposcopy (EFC) consensus statements on pre-invasive vulvar lesions. Int J Gynecol Cancer 2022;32:830–785.
Darragh TM, Colgan TJ, Cox JT, et al. The lower anogenital squamous terminology standardization project for HPV-associated lesions: background and consensus recommendations from the College of American Pathologists and the American Society for Colposcopy and Cervical Pathology. J Low Genit Tract Dis 2012;16:205–163.
Chiu T-L, Jones RW, et al. Multifocal multicentric squamous cell carcinomas arising in vulvovaginal lichen planus. J Low Genit Tract Dis 2011;15:246–239.
Regauer S, Reich O, Kashofer K, et al. HPV-negative squamous cell carcinomas of the cervix with special focus on intraepithelial precursor lesions. Am J Surg Pathol 2022;46:147–89.
WHO Classification of Tumors Editorial Board. Female genital tumors, WHO classification of tumors, 5th edition, volume 4; 2020.
Bornstein J, Bentley J, Bösze P, et al. 2011 colposcopic terminology of the International Federation for Cervical Pathology and Colposcopy. Obstet Gynecol 2012;120:166–94.
Sopracordevole F, Barbero M, Clemente N, et al. Colposcopic patterns of vaginal intraepithelial neoplasia: a study from the Italian Society of Colposcopy and Cervico-Vaginal Pathology. Eur J Cancer Prev 2018;27:152–145.
Zhou Q, Zhang F, Sui L, et al. Application of 2011 International Federation for Cervical Pathology and Colposcopy terminology on the detection of vaginal intraepithelial neoplasia. Cancer Manag Res 2020;12:5987–5892.
Stuebs FA, Koch MC, Mehlhorn G, et al. Accuracy of colposcopic findings in detecting vaginal intraepithelial neoplasia: a retrospective study. Arch Gynecol Obstet 2020;301:769–692.
Reich O, Pickel H, et al. 100 years of iodine testing of the cervix: a critical review and implications for the future. Eur J Obstet Gynecol Reprod Biol 2021;261:34–6.
Piccoli R, Mandato VD, Lavitola G, et al. Atypical squamous cells and low squamous intraepithelial lesions in postmenopausal women: implications for management. Eur J Obstet Gynecol Reprod Biol 2008;140:269–195.
Boonlikit S, Noinual N, et al. Vaginal intraepithelial neoplasia: a retrospective analysis of clinical features and colpohistology. J Obstet Gynaecol Res 2010;36:94–6.
Indraccolo U, Baldoni A, et al. A simplified classification for describing colposcopic vaginal patterns. J Low Genit Tract Dis 2012;16:75–66.
Gurumurthy M, Cruickshank ME, et al. Management of vaginal intraepithelial neoplasia. J Low Genit Tract Dis 2012;16:306–294.
Cardosi RJ, Bomalaski JJ, Hoffman MS, et al. Diagnosis and management of vulvar and vaginal intraepithelial neoplasia. Obstet Gynecol Clin North Am 2001;28:685–17.
Frega A, Sopracordevole F, Assorgi C, et al. Vaginal intraepithelial neoplasia: a therapeutical dilemma. Anticancer Res 2013;33:29–9.
Sopracordevole F, Barbero M, Clemente N, et al. High-grade vaginal intraepithelial neoplasia and risk of progression to vaginal cancer: a multicentre study of the Italian Society of Colposcopy and Cervico-Vaginal Pathology (SICPCV). Eur Rev Med Pharmacol Sci 2016;20:818–794.
Sillman FH, Fruchter RG, Chen YS, et al. Vaginal intraepithelial neoplasia: risk factors for persistence, recurrence, and invasion and its management. Am J Obstet Gynecol 1997;176(1 Pt 1):93–84.
González Bosquet E, Torres A, Busquets M, et al. Prognostic factors for the development of vaginal intraepithelial neoplasia. Eur J Gynaecol Oncol 2008;29:43–38.
Kurdgelashvili G, Dores GM, Srour SA, et al. Incidence of potentially human papillomavirus-related neoplasms in the United States, 1978 to 2007. Cancer 2013;119:2291–2282.
Levi F, Randimbison L, La Vecchia C, et al. Descriptive epidemiology of vulvar and vaginal cancers in Vaud, Sswitzerland, 1974-1994. Ann Oncol 1998;9:1229–1197.
Bertoli HK, Baandrup L, Aalborg GL, et al. Time trends in the incidence and survival of vaginal squamous cell carcinoma and high-grade vaginal intraepithelial neoplasia in Denmark - a nationwide population-based study. Gynecol Oncol 2020;158:734–725.
Bertoli HK, Rasmussen CL, Sand FL, et al. Human papillomavirus and p16 in squamous cell carcinoma and intraepithelial neoplasia of the vagina. Int J Cancer 2019;145:78–8.
Sherman JF, Mount SL, Evans MF, et al. Smoking increases the risk of high-grade vaginal intraepithelial neoplasia in women with oncogenic human papillomavirus. Gynecol Oncol 2008;110:396–5.
Jamieson DJ, Paramsothy P, Cu-Uvin S, et al. Vulvar, vaginal, and perianal intraepithelial neoplasia in women with or at risk for human immunodeficiency virus. Obstet Gynecol 2006;107:1023–1015.
Schockaert S, Poppe W, Arbyn M, et al. Incidence of vaginal intraepithelial neoplasia after hysterectomy for cervical intraepithelial neoplasia: a retrospective study. Am J Obstet Gynecol 2008;199:113.
Dodge JA, Eltabbakh GH, Mount SL, et al. Clinical features and risk of recurrence among patients with vaginal intraepithelial neoplasia. Gynecol Oncol 2001;83:363–354.
Gunderson CC, Nugent EK, Elfrink SH, et al. A contemporary analysis of epidemiology and management of vaginal intraepithelial neoplasia. Am J Obstet Gynecol 2013;208:410.
Ratnavelu N, Patel A, Fisher AD, et al. High-grade vaginal intraepithelial neoplasia: can we be selective about who we treat? BJOG 2013;120:887–794.
Liao JB, Jean S, Wilkinson-Ryan I, et al. Vaginal intraepithelial neoplasia (VaIN) after radiation therapy for gynecologic malignancies: a clinically recalcitrant entity. Gynecol Oncol 2011;120:108–96.
Pang L, Li L, Zhu L, et al. Malignant transformation of vaginal adenosis to clear cell carcinoma without prenatal diethylstilbestrol exposure: a case report and literature review. BMC Cancer 2019;19:798.
Adebamowo SN, Adeyemo AA, Rotimi CN, et al. Genome-wide association study of prevalent and persistent cervical high-risk human papillomavirus (HPV) infection. BMC Med Genet 2020;21:231.
Brown MA, Leo PJ, et al. Genetic susceptibility to cervical neoplasia. Papillomavirus Res 2019;7:132–128.
Bowden SJ, Bodinier B, Kalliala I, et al. Genetic variation in cervical preinvasive and invasive disease: a genome-wide association study. Lancet Oncol 2021;22:548–491.
Espinoza H, Ha KT, Pham TT, et al. Genetic predisposition to persistent human papillomavirus-infection and virus-induced cancers. Microorganisms 2021;9:2092.
von Knebel Doeberitz M, Prigge E-S, et al. Role of DNA methylation in HPV associated lesions. Papillomavirus Res 2019;7:180–177.
Del Pino M, Sierra A, Marimon L, et al. CADM1, MAL, and mir124 promoter methylation as biomarkers of transforming cervical intrapithelial lesions. Int J Mol Sci 2019;20:2262.
Phillips S, Cassells K, Garland SM, et al. Gene methylation of CADM1 and MAL identified as a biomarker of high grade anal intraepithelial neoplasia. Sci Rep 2022;12:3565.
Brusselaers N, Shrestha S, van de Wijgert J, et al. Vaginal dysbiosis and the risk of human papillomavirus and cervical cancer: systematic review and meta-analysis. Am J Obstet Gynecol 2019;221:9–9.
Mitra A, MacIntyre DA, Lee YS, et al. Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity. Sci Rep 2015;5:16865.
Gillet E, Meys JFA, Verstraelen H, et al. Association between bacterial vaginosis and cervical intraepithelial neoplasia: systematic review and meta-analysis. PLoS One 2012;7:e45201.
Plisko O, Zodzika J, Jermakova I, et al. Aerobic vaginitis - underestimated risk factor for cervical intraepithelial neoplasia. Diagnostics (Basel) 2021;11:97.
Kyrgiou M, Moscicki A-B, et al. Vaginal microbiome and cervical cancer. Semin Cancer Biol 2022;86:189–91.
Ravel J, Gajer P, Abdo Z, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A 2011;108 Suppl 1:4680–4673.
Norenhag J, Du J, Olovsson M, et al. The vaginal microbiota, human papillomavirus and cervical dysplasia: a systematic review and network meta-analysis. BJOG 2020;127:171–91.
Zhou F-Y, Zhou Q, Zhu Z-Y, et al. Types and viral load of human papillomavirus, and vaginal microbiota in vaginal intraepithelial neoplasia: a cross-sectional study. Ann Transl Med 2020;8:1408.
Mitra A, MacIntyre DA, Paraskevaidi M, et al. The vaginal microbiota and innate immunity after local excisional treatment for cervical intraepithelial neoplasia. Genome Med 2021;13:176.
Mitra A, MacIntyre DA, Marchesi JR, et al. The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome 2016;4:58.
Mitrović-Jovanović A, Stanimirović B, Nikolić B, et al. Cervical, vaginal and vulvar intraepithelial neoplasms. Vojnosanit Pregl 2011;68:1051–1045.
Adams TS, Cuello MA, et al. Cancer of the vagina. Int J Gynaecol Obstet 2018;143 Suppl 2:14–7.
Li H, Guo Y, Zhang J, et al. Risk factors for the development of vaginal intraepithelial neoplasia. Chin Med J (Engl) 2012;125:1219–1196.
Preti M, Rosso S, Micheletti L, et al. Risk of HPV-related extra-cervical cancers in women treated for cervical intraepithelial neoplasia. BMC Cancer 2020;20:972.
Cao D, Wu D, Xu Y, et al. Vaginal intraepithelial neoplasia in patients after total hysterectomy. Curr Probl Cancer 2021;45:100687.
Massad LS, Xie X, Greenblatt RM, et al. Effect of human immunodeficiency virus infection on the prevalence and incidence of vaginal intraepithelial neoplasia. Obstet Gynecol 2012;119:582–573.
Bornstein J, Adam E, Adler-Storthz K, et al. Development of cervical and vaginal squamous cell neoplasia as a late consequence of in utero exposure to diethylstilbestrol. Obstet Gynecol Surv 1988;43:15–6.
Cong Q, Song Y, Wang Q, et al. A retrospective study of cytology, high-risk HPV, and colposcopy results of vaginal intraepithelial neoplasia patients. Biomed Res Int 2018;2018:5894801.
Zhang L, Wang Q, Zhang H, et al. Screening history in vaginal precancer and cancer: a retrospective study of 2131 cases in China. Cancer Manag Res 2021;13:8855–8792.
Reich O, et al. Colposcopy of the vagina. In: Burghardt’s Primary Care Colposcopy: Textbook and Atlas . Stuttgart: Thieme; 2017.
Kim MK, Lee IH, Lee KH, et al. Clinical outcomes and risk of recurrence among patients with vaginal intraepithelial neoplasia: a comprehensive analysis of 576 cases. J Gynecol Oncol 2018;29:e6.
Zeligs KP, Byrd K, Tarney CM, et al. A clinicopathologic study of vaginal intraepithelial neoplasia. Obstet Gynecol 2013;122:1223–1193.
Aho M, Vesterinen E, Meyer B, et al. Natural history of vaginal intraepithelial neoplasia. Cancer 1991;68:195–188.
Rome RM, England PG, et al. Management of vaginal intraepithelial neoplasia: a series of 132 cases with long-term follow-up. Int J Gynecol Cancer 2000;10:382–292.
Ao M, Zheng D, Wang J, et al. Risk factors analysis of persistence, progression and recurrence in vaginal intraepithelial neoplasia. Gynecol Oncol 2021;162:584–575.
Field A, Bhagat N, Clark S, et al. Vaginal intraepithelial neoplasia: a retrospective study of treatment and outcomes among a cohort of UK women. J Low Genit Tract Dis 2020;24:43–36.
Hodeib M, Cohen JG, Mehta S, et al. Recurrence and risk of progression to lower genital tract malignancy in women with high grade vain. Gynecol Oncol 2016;141:507–497.
Cheng D, Ng TY, Ngan HY, et al. Wide local excision (WLE) for vaginal intraepithelial neoplasia (VaIN). Acta Obstet Gynecol Scand 1999;78:648–596.
Chai YK, Cheung SYC, Chan KKL, et al. Outcome of vaginal stripping for vaginal intraepithelial neoplasia: a 20-year observational study. J Obstet Gynaecol Res 2020;46:2511–2504.
Sopracordevole F, Clemente N, Barbero M, et al. Colposcopic patterns of vaginal intraepithelial neoplasia: a focus on low-grade lesions. Eur Rev Med Pharmacol Sci 2017;21:2823–2815.
Atay V, Muhcu M, Caliskan A, et al. Treatment of vaginal intraepithelial neoplasia. Cancer Ther 2007; 5:19–9.
Indermaur MD, Martino MA, Fiorica JV, et al. Upper vaginectomy for the treatment of vaginal intraepithelial neoplasia. Am J Obstet Gynecol 2005;193:577–497;
Luyten A, Hastor H, Vasileva T, et al. Laser-skinning colpectomy for extended vaginal intraepithelial neoplasia and microinvasive cancer. Gynecol Oncol 2014;135:217–195.
Bhati P, Samynathan K, Sebastian A, et al. Proximal partial vaginectomy for vaginal intraepithelial neoplasia. J Obstet Gynaecol India 2019;69:160–156.
Youn JH, Lee MA, Ju W, et al. Total vaginectomy for refractory vaginal intraepithelial neoplasia III of the vaginal vault. Obstet Gynecol Sci 2016;59:71–67.
Matsuo K, Chi DS, Walker LD, et al. Ultrasonic surgical aspiration for vaginal intraepithelial neoplasia. Int J Gynecol Obstet 2009;105:71–68.
Robinson JB, Sun CC, Bodurka-Bevers D, et al. Cavitational ultrasonic surgical aspiration for the treatment of vaginal intraepithelial neoplasia. Gynecol Oncol 2000;78:235–194.
Powell JL, Asbery DS, et al. Treatment of vaginal dysplasia: just a simple loop electrosurgical excision procedure? Am J Obstet Gynecol 2000;182:731–729.
Massad LS, et al. Outcomes after diagnosis of vaginal intraepithelial neoplasia. J Low Genit Tract Dis 2008;12:16–7.
Terzakis E, Androutsopoulos G, Zygouris D, et al. Loop electrosurgical excision procedure in Greek patients with vaginal intraepithelial neoplasia and history of cervical cancer. Eur J Gynaecol Oncol 2011;32:530–527.
Sopracordevole F, Clemente N, Di Giuseppe J, et al. Clinical characteristics and long-term follow-up of patients treated for high-grade vaginal intraepithelial neoplasia: results from a 20-year survey in Italy. J Low Genit Tract Dis 2020;24:381–375.
Cui C, Xiao Y, Lin E, et al. Precise measurement of the thickness of vaginal intraepithelial neoplasia. J Low Genit Tract Dis 2022;26:245–236.
Jentschke M, Hoffmeister V, Soergel P, et al. Clinical presentation, treatment and outcome of vaginal intraepithelial neoplasia. Arch Gynecol Obstet 2016;293:415–406.
Wang Y, Kong W-M, Wu Y-M, et al. Therapeutic effect of laser vaporization for vaginal intraepithelial neoplasia following hysterectomy due to premalignant and malignant lesions. J Obstet Gynaecol Res 2014;40:1740–1733.
Perrotta M, Marchitelli CE, Velazco AF, et al. Use of CO2 laser vaporization for the treatment of high-grade vaginal intraepithelial neoplasia. J Low Genit Tract Dis 2013;17:23–16.
Wee WW, Chia YN, Yam PKL, et al. Diagnosis and treatment of vaginal intraepithelial neoplasia. Int J Gynaecol Obstet 2012;117:15–8.
Yalcin OT, Rutherford TJ, Chambers SK, et al. Vaginal intraepithelial neoplasia: treatment by carbon dioxide laser and risk factors for failure. Eur J Obstet Gynecol Reprod Biol 2003;106:64–56.
Zhang T, Hu R, Tang Y, et al. The effect of local photodynamic therapy with 5-aminolevulinic acid in the treatment of vaginal intraepithelial lesions with high-risk HPV infection. Photodiagnosis Photodyn Ther 2022;37:102728.
Fehr MK, Hornung R, Degen A, et al. Photodynamic therapy of vulvar and vaginal condyloma and intraepithelial neoplasia using topically applied 5-aminolevulinic acid. Lasers Surg Med 2002;30:273–264.
Su Y, Zhang Y, Tong Y, et al. Effect and rational application of topical photodynamic therapy (PDT) with 5-aminolevulinic acid (5-ALA) for treatment of cervical intraepithelial neoplasia with vaginal intraepithelial neoplasia. Photodiagnosis Photodyn Ther 2022;37:102634.
Hu Z, Zheng H, Zeng K, et al. Patterns of multiple human papillomavirus clearance during 5-aminolevulinic acid-based photodynamic therapy in patients with genital warts. Photodiagnosis Photodyn Ther 2021;35:102454.
Chen L, Hu D, Xu S, et al. Clinical features, treatment and outcomes of vaginal intraepithelial neoplasia in a Chinese tertiary centre. Ir J Med Sci 2016;185:111–107.
Beavis A, Najjar O, Murdock T, et al. Treatment of vulvar and vaginal dysplasia: plasma energy ablation versus carbon dioxide laser ablation. Int J Gynecol Cancer 2021;31:1410–1405.
Diakomanolis E, Rodolakis A, Boulgaris Z, et al. Treatment of vaginal intraepithelial neoplasia with laser ablation and upper vaginectomy. Gynecol Obstet Invest 2002;54:17–3.
Chen F-P, et al. Efficacy of imiquimod 5% cream for persistent human papillomavirus in genital intraepithelial neoplasm. Taiwan J Obstet Gynecol 2013;52:475–467.
Lin C-T, Qiu J-T, Wang C-J, et al. Topical imiquimod treatment for human papillomavirus infection in patients with and without cervical/vaginal intraepithelial neoplasia. Taiwan J Obstet Gynecol 2012;51:533–525.
Buck HW, Guth KJ, et al. Treatment of vaginal intraepithelial neoplasia (primarily low grade) with imiquimod 5 % cream. J Low Genit Tract Dis 2003;7:290–287.
Tainio K, Jakobsson M, Louvanto K, et al. Randomised trial on treatment of vaginal intraepithelial neoplasia - imiquimod, laser vaporisation and expectant management. Int J Cancer 2016;139:2353–2345.
Inayama Y, Yamanishi Y, Nakatani E, et al. Imiquimod for vaginal intraepithelial neoplasia 2-3: a systematic review and meta-analysis. Gynecol Oncol 2021;160:140–133.
Fiascone S, Vitonis AF, Feldman S, et al. Topical 5-fluorouracil for women with high-grade vaginal intraepithelial neoplasia. Obstet Gynecol 2017;130:1237–1194.
Gonzalez-Sanchez JL, Flores-Murrieta G, Deolarte-Melgarejo JM, et al. Effectiveness of 5-fluorouracil in the treatment of vaginal intraepithelial neoplasia in a Mexican population. J Low Genit Tract Dis 1998;2:221–217.
Murta EFC, Neves Junior MA, Sempionato LRF, et al. Vaginal intraepithelial neoplasia: clinical-therapeutic analysis of 33 cases. Arch Gynecol Obstet 2005;272:261–257.
Taner ZM, Taskiran C, Onan AM, et al. Therapeutic value of trichloroacetic acid in the treatment of isolated genital warts on the external female genitalia. J Reprod Med 2007;52:521–516.
Rhodes HE, Chenevert L, Munsell M, et al. Vaginal intraepithelial neoplasia (VaIN 2/3): comparing clinical outcomes of treatment with intravaginal estrogen. J Low Genit Tract Dis 2014;18:115–94.
Mock U, Kucera H, Fellner C, et al. High-dose-rate (HDR) brachytherapy with or without external beam radiotherapy in the treatment of primary vaginal carcinoma: long-term results and side effects. Int J Radiat Oncol Biol Phys 2003;56:950–943.
Blanchard P, Monnier L, Dumas I, et al. Low-dose-rate definitive brachytherapy for high-grade vaginal intraepithelial neoplasia. Oncologist 2011;16:182–174.
Zolciak-Siwinska A, Gruszczynska E, Jonska-Gmyrek J, et al. Brachytherapy for vaginal intraepithelial neoplasia. Eur J Obstet Gynecol Reprod Biol 2015;194:73–66.
Song JH, Lee JH, Lee JH, et al. High-dose-rate brachytherapy for the treatment of vaginal intraepithelial neoplasia. Cancer Res Treat 2014;46:74–6.
Graham K, Wright K, Cadwallader B, et al. 20-year retrospective review of medium dose rate intracavitary brachytherapy in VAIN3. Gynecol Oncol 2007;106:105–94.
Sasagasako N, Kosaka K, Sagae Y, et al. Recurrent vaginal intraepithelial neoplasia successfully treated with topical imiquimod: a case report. Mol Clin Oncol 2020;13:19.
Yao H, Zhang H, Pu X, et al. Photodynamic therapy combined with carbon dioxide laser for low-grade vaginal intraepithelial neoplasia: a retrospective analysis. Photodiagnosis Photodyn Ther 2020;30:101731.
Bogani G, Ditto A, Martinelli F, et al. LASER treatment for women with high-grade vaginal intraepithelial neoplasia: a propensity-matched analysis on the efficacy of ablative versus excisional procedures. Lasers Surg Med 2018;50:933–924.
von Gruenigen VE, Gibbons HE, Gibbins K, et al. Surgical treatments for vulvar and vaginal dysplasia: a randomized controlled trial. Obstet Gynecol 2007;109:942–935.
García-Iglesias Á, et al. CO2 laser treatment for vaginal intraepithelial neoplasia, assessment of recurrence. J Gynecol Res Obstet 2016;2:017–3.
Yu D, Qu P, Liu M, et al. Clinical presentation, treatment, and outcomes associated with vaginal intraepithelial neoplasia: a retrospective study of 118 patients. J Obstet Gynaecol Res 2021;47:1624–1594.
Cho HW, Hong JH, Lee JK, et al. Detection of high-risk human papillomavirus infection and treatment of high-grade vaginal intraepithelial neoplasia: a single-institution study. Int J Gynaecol Obstet 2021;154:227–195.
Coutinho L, Sousa R, Branco EC, et al. Neoplasia intraepitelial vaginal de alto grau – revisão de 23 casos. Acta Obstet Ginecol Port 2014;8:240–236.
De Vuyst H, Clifford GM, Nascimento MC, et al. Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta-analysis. Int J Cancer 2009;124:1626–1590.
Khan MJ, Massad LS, Kinney W, et al. A common clinical dilemma: management of abnormal vaginal cytology and human papillomavirus test results. Gynecol Oncol 2016;141:364–294.
Kesić V, Vieira-Baptista P, Stockdale CK, et al. Early diagnostics of vulvar intraepithelial neoplasia. Cancers (Basel) 2022;14:1822.
Lamos C, Mihaljevic C, Aulmann S, et al. Detection of human papillomavirus infection in patients with vaginal intraepithelial neoplasia. PLoS One 2016;11:e0167386.
World Health Organization. New WHO recommendations on screening and treatment to prevent cervical cancer among women living with HIV: policy brief; 2022.
Thimm MA, Rositch AF, VandenBussche C, et al. Lower genital tract dysplasia in female solid organ transplant recipients. Obstet Gynecol 2019;134:385–291.
Kim SC, Glynn RJ, Giovannucci E, et al. Risk of high-grade cervical dysplasia and cervical cancer in women with systemic inflammatory diseases: a population-based cohort study. Ann Rheum Dis 2015;74:1360–1353.
Foster E, Malloy MJ, Jokubaitis VG, et al. Increased risk of cervical dysplasia in females with autoimmune conditions - results from an Australia database linkage study. PLoS One 2020;15:e0234813.
Dillner J, Kjaer SK, Wheeler CM, et al. Four year efficacy of prophylactic human papillomavirus quadrivalent vaccine against low grade cervical, vulvar, and vaginal intraepithelial neoplasia and anogenital warts: randomised controlled trial. BMJ 2010;341:c3493.
Joura EA, Leodolter S, Hernandez-Avila M, et al. Efficacy of a quadrivalent prophylactic human papillomavirus (types 6, 11, 16, and 18) L1 virus-like-particle vaccine against high-grade vulval and vaginal lesions: a combined analysis of three randomised clinical trials. Lancet 2007;369:1693–991.
Dehlendorff C, Baandrup L, Kjaer SK, et al. Real-world effectiveness of human papillomavirus vaccination against vulvovaginal high-grade precancerous lesions and cancers. J Natl Cancer Inst 2021;113:869–795.
Ebisch RMF, Rutten DWE, IntHout J, et al. Long-lasting increased risk of human papillomavirus-related carcinomas and premalignancies after cervical intraepithelial neoplasia grade 3: a population-based cohort study. J Clin Oncol 2017;35:2542–2492.
Di Donato V, Caruso G, Bogani G, et al. HPV vaccination after primary treatment of HPV-related disease across different organ sites: a multidisciplinary comprehensive review and meta-analysis. Vaccines (Basel) 2022;10:239.
Dreyer G, et al. Clinical implications of the interaction between HPV and HIV infections. Best Pract Res Clin Obstet Gynaecol 2018;47:95–11.
Vangipuram R, Tyring SK, et al. AIDS-associated malignancies. Cancer Treat Res 2019;177:1–20.
Rubinstein PG, Aboulafia DM, Zloza A, et al. Malignancies in HIV/AIDS: from epidemiology to therapeutic challenges. AIDS 2014;28:453–388.
Carbone A, Vaccher E, Gloghini A, et al. Diagnosis and management of lymphomas and other cancers in HIV-infected patients. Nat Rev Clin Oncol 2014;11:223–185.
Conley LJ, Ellerbrock TV, Bush TJ, et al. HIV-1 infection and risk of vulvovaginal and perianal condylomata acuminata and intraepithelial neoplasia: a prospective cohort study. Lancet 2002;359:108–95.
Grulich AE, van Leeuwen MT, Falster MO, et al. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet 2007;370:59–8.
Denny L, Boa R, Williamson A-L, et al. Human papillomavirus infection and cervical disease in human immunodeficiency virus-1-infected women. Obstet Gynecol 2008;111:1380–1373.
Bradbury M, Xercavins N, García-Jiménez Á, et al. Vaginal intraepithelial neoplasia: clinical presentation, management, and outcomes in relation to HIV infection status. J Low Genit Tract Dis 2019;23:7–5.
Toby M, Conway K, Sethi G, et al. Usual vulval intraepithelial neoplasia in HIV-positive women - a case series. Int J STD AIDS 2016;27:1253–1247.
Okoye JO, Erinle C, Ngokere AA, et al. Low CD4 cells and viral co-infection increase the risk of VaIN: use of SCCA1 and ki67 as diagno-prognostic biomarkers. Pathophysiology 2018;25:51–45.
Smeltzer S, Yu X, Schmeler K, et al. Abnormal vaginal pap test results after hysterectomy in human immunodeficiency virus-infected women. Obstet Gynecol 2016;128:52–45.
Pearce KF, Haefner HK, Sarwar SF, et al. Cytopathological findings on vaginal papanicolaou smears after hysterectomy for benign gynecologic disease. N Engl J Med 1996;335:1559–1497.
Piscitelli JT, Bastian LA, Wilkes A, et al. Cytologic screening after hysterectomy for benign disease. Am J Obstet Gynecol 1995;173:424–394;
Guidelines for the prevention and treatment of opportunistic infections in adults and adolescents with HIV; Available: https://clinicalinfo.hiv.gov/en/guidelines/hiv-clinical-guidelines-adult-and-adolescent-opportunistic-infections/human-0?view=full [Accessed 12 Jan 2023].
Wielgos A, Pietrzak B, Suchonska B, et al. A six-year gynecological follow-up of immunosuppressed women with a high-risk human papillomavirus infection. Int J Environ Res Public Health 2022;19:3531.
Tranoulis A, Georgiou D, Laios A, et al. 5-flouorouracil is an attractive medical treatment in women with vaginal intraepithelial neoplasia: a meta-analysis. J Low Genit Tract Dis 2018;22:375–294.
Massad LS, Silverberg MJ, Springer G, et al. Effect of antiretroviral therapy on the incidence of genital warts and vulvar neoplasia among women with the human immunodeficiency virus. Am J Obstet Gynecol 2004;190:1241–1233.
Kelly H, Chikandiwa A, Alemany Vilches L, et al. Association of antiretroviral therapy with anal high-risk human papillomavirus, anal intraepithelial neoplasia, and anal cancer in people living with HIV: a systematic review and meta-analysis. Lancet HIV 2020;7:e262–184.
Conway EL, Farmer KC, Lynch WJ, et al. Quality of life valuations of HPV-associated cancer health states by the general population. Sex Transm Infect 2012;88:517–496.
Herson M, Kulkarni J, et al. Hormonal agents for the treatment of depression associated with the menopause. Drugs Aging 2022;39:607–589.
Koyanagi Y, Kubo C, Nagata S, et al. Detection of pagetoid urothelial intraepithelial neoplasia extending to the vagina by cervical screening cytology: a case report with renewed immunochemical summary. Diagn Pathol 2019;14:9.
Brown HM, Wilkinson EJ, et al. Uroplakin-III to distinguish primary vulvar paget disease from Paget disease secondary to urothelial carcinoma. Hum Pathol 2002;33:545–537.
Konstantinova AM, Kazakov DV, et al. Extramammary Paget disease of the vulva. Semin Diagn Pathol 2021;38:50687.
Liao X, Liu X, Fan X, et al. Perianal Paget’s disease: a clinicopathological and immunohistochemical study of 13 cases. Diagn Pathol 2020;15:29.
Parra-Medina R, Morales SD, et al. Diagnostic utility of epithelial and melanocitic markers with double sequential immunohistochemical staining in differentiating melanoma in situ from invasive melanoma. Ann Diagn Pathol 2017;26:70–66.