{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T22:33:41Z","timestamp":1790980421737,"version":"4.1.0"},"reference-count":58,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2023,9,19]],"date-time":"2023-09-19T00:00:00Z","timestamp":1695081600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Department of Pathology and Laboratory Medicine at the UW-Madison","award":["P01 CA02443"],"award-info":[{"award-number":["P01 CA02443"]}]},{"name":"Department of Pathology and Laboratory Medicine at the UW-Madison","award":["R35 CA210807"],"award-info":[{"award-number":["R35 CA210807"]}]},{"name":"Department of Pathology and Laboratory Medicine at the UW-Madison","award":["P30CA014520-49"],"award-info":[{"award-number":["P30CA014520-49"]}]},{"DOI":"10.13039\/100000009","name":"NIH","doi-asserted-by":"publisher","award":["P01 CA02443"],"award-info":[{"award-number":["P01 CA02443"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000009","name":"NIH","doi-asserted-by":"publisher","award":["R35 CA210807"],"award-info":[{"award-number":["R35 CA210807"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000009","name":"NIH","doi-asserted-by":"publisher","award":["P30CA014520-49"],"award-info":[{"award-number":["P30CA014520-49"]}],"id":[{"id":"10.13039\/100000009","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Approximately 40% of vulvar squamous cell carcinoma (vSCC) cases are etiologically associated with high-risk human papillomaviruses (HPVs) of the alpha genera (\u03b1-HPV) that cause other anogenital cancers; however, the etiology of \u03b1-HPV-negative vSCC is poorly understood. HPVs of the beta genera (\u03b2-HPV) are risk factors for cutaneous squamous cell carcinoma (cSCC) and may be related to carcinomas originating in other cutaneous sites such as the vulva. In this study, we investigate the presence of \u03b2-HPVs, with an emphasis on p16-negative squamous lesions adjacent to vSCC. We subjected 28 vulvar squamous intraepithelial lesions adjacent to vSCC for comprehensive HPV genotyping, p16 and p53 immunohistochemistry, and consensus morphology review. Selected cases were subjected to qPCR and RNA in situ hybridization. Clinical data were obtained from medical records. \u03b2-HPV DNA was detected in eight of ten p16-negative lesions and three of fourteen p16-positive high-grade squamous intraepithelial lesions. The HPV DNA loads in vulvar squamous intraepithelial lesions ranged between less than 1 HPV DNA copy per cell to more than 100 HPV DNA copies per cell. This is, to the best of our knowledge, the first report of the association of p16-negative vulvar intraepithelial squamous lesions with detection of \u03b2-HPVs. These findings expand possible etiologic mechanisms that may contribute to p16-negative lesions of the vulva.<\/jats:p>","DOI":"10.3390\/v15091950","type":"journal-article","created":{"date-parts":[[2023,9,19]],"date-time":"2023-09-19T02:47:52Z","timestamp":1695091672000},"page":"1950","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Betapapillomaviruses in p16-Negative Vulvar Intraepithelial Lesions Associated with Squamous Cell Carcinoma"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2893-5580","authenticated-orcid":false,"given":"Taja","family":"Lozar","sequence":"first","affiliation":[{"name":"McArdle Laboratory for Cancer Research, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USA"},{"name":"University of Wisconsin Carbone Cancer Center, Madison, WI 53705, USA"},{"name":"University of Ljubljana, 1000 Ljubljana, Slovenia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aysenur","family":"Keske","sequence":"additional","affiliation":[{"name":"Department of Pathology and Laboratory Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI 53726, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Racheal S.","family":"Dube Mandishora","sequence":"additional","affiliation":[{"name":"Center for Immunization and Infection Research in Cancer (CIIRC), Moffit Cancer Center, Tampa, FL 33612, USA"},{"name":"Medical Microbiology Unit, University of Zimbabwe Faculty of Health Sciences, Harare P.O. Box A178, Zimbabwe"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiqi","family":"Yu","sequence":"additional","affiliation":[{"name":"Department of Pathology, Johns Hopkins School of Medicine, Baltimore, MD 21205, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam","family":"Bailey","sequence":"additional","affiliation":[{"name":"Department of Pathology and Laboratory Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI 53726, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jin","family":"Xu","sequence":"additional","affiliation":[{"name":"Department of Pathology and Laboratory Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI 53726, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Massimo","family":"Tommasino","sequence":"additional","affiliation":[{"name":"IRCCS Istituto Tumori Giovanni Paolo ll, 70124 Bari, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephanie M.","family":"McGregor","sequence":"additional","affiliation":[{"name":"University of Wisconsin Carbone Cancer Center, Madison, WI 53705, USA"},{"name":"Department of Pathology and Laboratory Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI 53726, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7983-2755","authenticated-orcid":false,"given":"Paul F.","family":"Lambert","sequence":"additional","affiliation":[{"name":"McArdle Laboratory for Cancer Research, University of Wisconsin School of Medicine and Public Health, Madison, WI 53705, USA"},{"name":"University of Wisconsin Carbone Cancer Center, Madison, WI 53705, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7088-337X","authenticated-orcid":false,"given":"Tarik","family":"Gheit","sequence":"additional","affiliation":[{"name":"International Agency for Research on Cancer, 69007 Lyon, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Megan B.","family":"Fitzpatrick","sequence":"additional","affiliation":[{"name":"University of Wisconsin Carbone Cancer Center, Madison, WI 53705, USA"},{"name":"Department of Pathology and Laboratory Medicine, University of Wisconsin School of Medicine and Public Health, Madison, WI 53726, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,9,19]]},"reference":[{"key":"ref_1","unstructured":"World Health Organization (2020). Female Genital TUMOURS, World Health Organization. [5th ed.]."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1053\/j.semdp.2020.09.006","article-title":"Putative precancerous lesions of vulvar squamous cell carcinoma","volume":"38","author":"Jenkins","year":"2021","journal-title":"Semin. Diagn. Pathol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1111\/his.14451","article-title":"DEVIL, VAAD and vLSC constitute a spectrum of HPV-independent, p53-independent intra-epithelial neoplasia of the vulva","volume":"19","author":"Roy","year":"2021","journal-title":"Histopathology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1097\/PAS.0000000000001047","article-title":"Differentiated Vulvar Intraepithelial Neoplasia-like and Lichen Sclerosus-like Lesions in HPV-associated Squamous Cell Carcinomas of the Vulva","volume":"42","author":"Rakislova","year":"2018","journal-title":"Am. J. Surg. Pathol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2011","DOI":"10.1038\/s41379-020-0573-5","article-title":"Differentiated exophytic vulvar intraepithelial lesion: Clinicopathologic and molecular analysis documenting its relationship with verrucous carcinoma of the vulva","volume":"33","author":"Akbari","year":"2020","journal-title":"Mod. Pathol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3739075","DOI":"10.1155\/2020\/3739075","article-title":"The Clinical Relevance of p16 and p53 Status in Patients with Squamous Cell Carcinoma of the Vulva","volume":"2020","author":"Barlow","year":"2020","journal-title":"J. Oncol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1506","DOI":"10.1097\/PAS.0000000000001540","article-title":"HPV-independent Precursors Mimicking High-grade Squamous Intraepithelial Lesions (HSIL) of the Vulva","volume":"44","author":"Rakislova","year":"2020","journal-title":"Am. J. Surg. Pathol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"102866","DOI":"10.1016\/j.critrevonc.2020.102866","article-title":"Precursor lesions of vulvar squamous cell carcinoma\u2014Histology and biomarkers: A systematic review","volume":"147","author":"Dasgupta","year":"2020","journal-title":"Crit. Rev. Oncol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1097\/LGT.0000000000000572","article-title":"Diagnostic Criteria for Differentiated Vulvar Intraepithelial Neoplasia and Vulvar Aberrant Maturation","volume":"25","author":"Heller","year":"2021","journal-title":"J. Low. Genit. Tract Dis."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/j.pathol.2016.02.015","article-title":"Squamous precursor lesions of the vulva: Current classification and diagnostic challenges","volume":"48","author":"Hoang","year":"2016","journal-title":"Pathology"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"448","DOI":"10.1038\/modpathol.2016.187","article-title":"Differentiated exophytic vulvar intraepithelial lesions are genetically distinct from keratinizing squamous cell carcinomas and contain mutations in PIK3CA","volume":"30","author":"Watkins","year":"2017","journal-title":"Mod. Pathol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1097\/00000478-200405000-00012","article-title":"Vulvar Acanthosis with Altered Differentiation: A Precursor to Verrucous Carcinoma?","volume":"28","author":"Nascimento","year":"2004","journal-title":"Am. J. Surg. Pathol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1038\/s41379-021-00942-3","article-title":"Molecular landscape of vulvovaginal squamous cell carcinoma: New insights into molecular mechanisms of HPV-associated and HPV-independent squamous cell carcinoma","volume":"35","author":"Salama","year":"2022","journal-title":"Mod. Pathol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"6781","DOI":"10.1158\/1078-0432.CCR-17-1302","article-title":"Genomic Characterization of Vulvar (Pre)cancers Identifies Distinct Molecular Subtypes with Prognostic Significance","volume":"23","author":"Nooij","year":"2017","journal-title":"Clin. Cancer Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1317","DOI":"10.1038\/s41379-022-01079-7","article-title":"HPV-independent, p53-wild-type vulvar intraepithelial neoplasia: A review of nomenclature and the journey to characterize verruciform and acanthotic precursor lesions of the vulva","volume":"35","author":"Nucci","year":"2022","journal-title":"Mod. Pathol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1038\/nature12965","article-title":"Comprehensive molecular characterization of urothelial bladder carcinoma","volume":"507","author":"Weinstein","year":"2014","journal-title":"Nature"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1229","DOI":"10.1136\/ijgc-2022-003763","article-title":"Significance of p53 and presence of differentiated vulvar intra-epithelial neoplasia (dVIN) at resection margin in early stage human papillomavirus-independent vulvar squamous cell carcinoma","volume":"32","author":"Thompson","year":"2022","journal-title":"Int. J. Gynecol. Cancer"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1595","DOI":"10.1038\/s41379-020-0524-1","article-title":"Major p53 immunohistochemical patterns in in situ and invasive squamous cell carcinomas of the vulva and correlation with TP53 mutation status","volume":"33","author":"Kortekaas","year":"2020","journal-title":"Mod. Pathol."},{"key":"ref_19","unstructured":"Hpvcenter (2021, October 20). HPV Reference Clones. Available online: https:\/\/www.hpvcenter.se\/human_reference_clones\/."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/S1470-2045(09)70096-8","article-title":"A review of human carcinogens\u2014Part B: Biological agents","volume":"10","author":"Bouvard","year":"2009","journal-title":"Lancet Oncol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1016\/S1470-2045(05)70086-3","article-title":"Carcinogenicity of human papillomaviruses","volume":"6","author":"Cogliano","year":"2005","journal-title":"Lancet Oncol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"100196","DOI":"10.1016\/j.pvr.2020.100196","article-title":"Detection of human papillomaviruses in paired healthy skin and actinic keratosis by next generation sequencing","volume":"9","author":"Galati","year":"2020","journal-title":"Papillomavirus Res."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1128\/JVI.01003-18","article-title":"An Emerging Issue in Oncogenic Virology: The Role of Beta Human Papillomavirus Types in the Development of Cutaneous Squamous Cell Carcinoma","volume":"93","author":"Rollison","year":"2019","journal-title":"J. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Romero-Medina, M.C., Venuti, A., Melita, G., Robitaille, A., Ceraolo, M.G., Pacini, L., Sirand, C., Viarisio, D., Taverniti, V., and Gupta, P. (2020). Human papillomavirus type 38 alters wild-type p53 activity to promote cell proliferation via the downregulation of integrin alpha 1 expression. PLoS Pathog., 16.","DOI":"10.1371\/journal.ppat.1008792"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/j.virusres.2016.11.013","article-title":"The biology of beta human papillomaviruses","volume":"231","author":"Tommasino","year":"2017","journal-title":"Virus Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"8241","DOI":"10.1038\/s41598-018-26589-w","article-title":"Beta and gamma human papillomaviruses in anal and genital sites among men: Prevalence and determinants","volume":"8","author":"Smelov","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1128\/JCM.00991-09","article-title":"Abundance of Multiple High-Risk Human Papillomavirus (HPV) Infections Found in Cervical Cells Analyzed by Use of an Ultrasensitive HPV Genotyping Assay","volume":"48","author":"Schmitt","year":"2010","journal-title":"J. Clin. Microbiol."},{"key":"ref_28","first-page":"604","article-title":"Human Papillomaviruses in Transplant-Associated Skin Cancers","volume":"30","author":"Stockfleth","year":"2004","journal-title":"Dermatol. Surg."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"4639","DOI":"10.1038\/onc.2011.589","article-title":"Cutaneous papillomavirus E6 oncoproteins associate with MAML1 to repress transactivation and NOTCH signaling","volume":"31","author":"Brimer","year":"2012","journal-title":"Oncogene"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"13174","DOI":"10.1128\/JVI.02172-12","article-title":"Comprehensive Analysis of Host Cellular Interactions with Human Papillomavirus E6 Proteins Identifies New E6 Binding Partners and Reflects Viral Diversity","volume":"86","author":"White","year":"2012","journal-title":"J. Virol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Brimer, N., Drews, C.M., and Pol, S.B.V. (2017). Association of papillomavirus E6 proteins with either MAML1 or E6AP clusters E6 proteins by structure, function, and evolutionary relatedness. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006781"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1016\/j.jaad.2014.01.857","article-title":"Role of human papillomavirus in cutaneous squamous cell carcinoma: A meta-analysis","volume":"70","author":"Wang","year":"2014","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e435","DOI":"10.1016\/j.lpm.2014.08.008","article-title":"Cutaneous HPV and skin cancer","volume":"43","author":"Accardi","year":"2014","journal-title":"Presse Med."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1186\/s13027-020-00286-8","article-title":"Role of human papillomavirus infection in the etiology of vulvar cancer in Italian women","volume":"15","author":"Preti","year":"2020","journal-title":"Infect. Agents Cancer"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1111\/j.0022-202X.2005.23733.x","article-title":"Human Papillomavirus-DNA Loads in Actinic Keratoses Exceed those in Non-Melanoma Skin Cancers","volume":"125","author":"Weissenborn","year":"2005","journal-title":"J. Investig. Dermatol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1111\/j.0022-202X.2005.23635.x","article-title":"Human Papillomavirus Gene Expression in Cutaneous Squamous Cell Carcinomas from Immunosuppressed and Immunocompetent Individuals","volume":"125","author":"Purdie","year":"2005","journal-title":"J. Investig. Dermatol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Viarisio, D., M\u00fcller-Decker, K., Accardi, R., Robitaille, A., D\u00fcrst, M., Beer, K., Jansen, L., Flechtenmacher, C., Bozza, M., and Harbottle, R. (2018). Beta HPV38 oncoproteins act with a hit-and-run mechanism in ultraviolet radiation-induced skin carcinogenesis in mice. PLoS Pathog., 14.","DOI":"10.1371\/journal.ppat.1006783"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e1006723","DOI":"10.1371\/journal.ppat.1006723","article-title":"The interplay of UV and cutaneous papillomavirus infection in skin cancer development","volume":"13","author":"Hasche","year":"2017","journal-title":"PLoS Pathog."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"5661","DOI":"10.1038\/s41598-021-85030-x","article-title":"Four-decade trends in lymph node status of patients with vulvar squamous cell carcinoma in northern Italy","volume":"11","author":"Preti","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"830","DOI":"10.1136\/ijgc-2021-003262","article-title":"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","volume":"32","author":"Preti","year":"2022","journal-title":"Int. J. Gynecol. Cancer"},{"key":"ref_41","first-page":"151","article-title":"Revising the WHO classification: Female genital tract tumours","volume":"76","author":"ACree","year":"2019","journal-title":"Histopathology"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1038\/s41379-020-00651-3","article-title":"Molecular characterization of invasive and in situ squamous neoplasia of the vulva and implications for morphologic diagnosis and outcome","volume":"34","author":"Pors","year":"2021","journal-title":"Mod. Pathol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1097\/PGP.0b013e31826916c7","article-title":"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","volume":"32","author":"Darragh","year":"2013","journal-title":"Int. J. Gynecol. Pathol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1111\/his.14238","article-title":"Comparison of p53 immunohistochemical staining in differentiated vulvar intraepithelial neoplasia (dVIN) with that in inflammatory dermatoses and benign squamous lesions in the vulva","volume":"78","author":"Liu","year":"2021","journal-title":"Histopathology"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1111\/his.14109","article-title":"Performance of the pattern-based interpretation of p53 immunohistochemistry as a surrogate for TP53 mutations in vulvar squamous cell carcinoma","volume":"77","author":"Kortekaas","year":"2020","journal-title":"Histopathology"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1016\/j.vaccine.2008.11.041","article-title":"Prevalence of human papillomavirus types in cervical and oral cancers in central India","volume":"27","author":"Gheit","year":"2009","journal-title":"Vaccine"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2025","DOI":"10.1128\/JCM.02305-05","article-title":"Development of a Sensitive and Specific Assay Combining Multiplex PCR and DNA Microarray Primer Extension to Detect High-Risk Mucosal Human Papillomavirus Types","volume":"44","author":"Gheit","year":"2006","journal-title":"J. Clin. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/nprot.2009.153","article-title":"Quantification of beta-human papillomavirus DNA by real-time PCR","volume":"5","author":"Weissenborn","year":"2009","journal-title":"Nat. Protoc."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"6327","DOI":"10.1038\/s41388-020-01431-8","article-title":"HPV E2, E4, E5 drive alternative carcinogenic pathways in HPV positive cancers","volume":"39","author":"Ren","year":"2020","journal-title":"Oncogene"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1038\/s41586-019-1719-9","article-title":"Immunity to commensal papillomaviruses protects against skin cancer","volume":"575","author":"Strickley","year":"2019","journal-title":"Nature"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1026","DOI":"10.1038\/jid.2008.317","article-title":"High \u03b2-HPV DNA Loads and Strong Seroreactivity Are Present in Epidermodysplasia Verruciformis","volume":"129","author":"Azzimonti","year":"2009","journal-title":"J. Investig. Dermatol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2467","DOI":"10.1099\/vir.0.2008\/001925-0","article-title":"Four novel human betapapillomaviruses of species 2 preferentially found in actinic keratosis","volume":"89","author":"Hazard","year":"2008","journal-title":"J. Gen. Virol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2624","DOI":"10.1158\/1078-0432.CCR-14-2667","article-title":"Contribution of Beta-HPV Infection and UV Damage to Rapid-Onset Cutaneous Squamous Cell Carcinoma during BRAF-Inhibition Therapy","volume":"21","author":"Cohen","year":"2015","journal-title":"Clin. Cancer Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.jinf.2015.02.001","article-title":"Alpha, beta and gamma Human Papillomaviruses in the anal canal of HIV-infected and uninfected men who have sex with men","volume":"71","author":"Gheit","year":"2015","journal-title":"J. Infect."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"595.e1","DOI":"10.1016\/j.ajog.2020.12.1220","article-title":"p53 and p16 expression profiles in vulvar cancer: A translational analysis by the Arbeitsgemeinschaft Gyn\u00e4kologische Onkologie Chemo and Radiotherapy in Epithelial Vulvar Cancer study group","volume":"224","author":"Woelber","year":"2021","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1016\/j.ygyno.2020.09.024","article-title":"Vulvar cancer subclassification by HPV and p53 status results in three clinically distinct subtypes","volume":"159","author":"Kortekaas","year":"2020","journal-title":"Gynecol. Oncol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1016\/S0002-9378(96)70654-3","article-title":"Sites of failure and times to failure in carcinoma of the vulva treated conservatively: A Gynecologic Oncology Group study","volume":"174","author":"Stehman","year":"1996","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1111\/j.1743-6109.2011.02520.x","article-title":"Sexual, Psychological, and Relational Functioning in Women after Surgical Treatment for Vulvar Malignancy: A Literature Review","volume":"9","author":"Aerts","year":"2012","journal-title":"J. Sex. Med."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/15\/9\/1950\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:53:27Z","timestamp":1760129607000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/15\/9\/1950"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,19]]},"references-count":58,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2023,9]]}},"alternative-id":["v15091950"],"URL":"https:\/\/doi.org\/10.3390\/v15091950","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,9,19]]}}}