{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,16]],"date-time":"2026-05-16T01:40:17Z","timestamp":1778895617333,"version":"3.51.4"},"reference-count":49,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2023,4,13]],"date-time":"2023-04-13T00:00:00Z","timestamp":1681344000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,8,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Objectives<\/jats:title>\n                  <jats:p>The 2019 American Society of Colposcopy and Cervical Pathology management guidelines recommend that patients with an unsatisfactory Papanicolaou (Pap) test (UPT) and negative human papillomavirus (HPV) cotest undergo repeat age-based screening in 2 to 4 months. The rationale is that a negative HPV test in the setting of an UPT may reflect an inadequate sample and therefore should not be interpreted as truly \u201cnegative.\u201d For patients 25 years and older who are cotested, if HPV is positive for the 16 or 18 genotypes, direct referral for colposcopy is recommended. Our study aimed to determine if a negative HPV cotest result is predictive of the absence of a high-grade squamous intraepithelial lesion (HSIL) and whether these patients may be called back for repeat testing at an interval longer than 2 to 4 months.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>Follow-up cervical cytology and biopsy results in women with UPT and HPV cotests from January 2017 to December 2021 were collected. Original UPT and HPV cotest results were correlated with the follow-up Pap and biopsy results.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>There were 1,496 (2.28%) UPT cases out of 65,641 total Pap tests. Among the 1,496 UPT cases, 1,010 (67.5%) had HPV cotesting; 676 (45.1%) were followed by repeat Pap or biopsy within 4 months and 850 (56.8%) within 12 months. The total follow-up rate was 81%, with a range of 3 days to 36 months. The HSIL rate in HPV-positive cases was 5.7% (3\/53) vs 0.4% (2\/539) (P = .006) in HPV-negative cases. In UPT, HPV cotesting showed negative predictive values for low-grade and high-grade squamous intraepithelial lesion detection of 98.5% and 99.6%, respectively, while positive predictive values were 19% and 5.7%.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>A negative HPV cotest in individuals with UPT predicted the lack of HSIL in our study. Compliance with the recommended follow-up time of 2 to 4 months for women with UPT was low (45.1%). Our study suggests that women with UPT and negative HPV cotest may be safely called back at an interval longer than 4 months.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/ajcp\/aqad026","type":"journal-article","created":{"date-parts":[[2023,4,13]],"date-time":"2023-04-13T15:46:47Z","timestamp":1681400807000},"page":"137-143","source":"Crossref","is-referenced-by-count":5,"title":["HPV Cotesting of Unsatisfactory Papanicolaou Tests: Implications for Follow-up Intervals"],"prefix":"10.1093","volume":"160","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8005-4399","authenticated-orcid":false,"given":"Fei","family":"Chen","sequence":"first","affiliation":[{"name":"Department of Pathology, NYU Langone Health , New York, NY , US"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lawrence","family":"Hsu Lin","sequence":"additional","affiliation":[{"name":"Department of Pathology, NYU Langone Health , New York, NY , US"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0890-7112","authenticated-orcid":false,"given":"Issa","family":"Hindi","sequence":"additional","affiliation":[{"name":"Department of Pathology, NYU Langone Health , New York, NY , US"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wei","family":"Sun","sequence":"additional","affiliation":[{"name":"Department of Pathology, NYU Langone Health , New York, NY , US"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Negin","family":"Shafizadeh","sequence":"additional","affiliation":[{"name":"Department of Pathology, NYU Langone Health , New York, NY , US"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Oliver","family":"Szeto","sequence":"additional","affiliation":[{"name":"Department of Pathology, NYU Langone Health , New York, NY , US"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tamar C","family":"Brandler","sequence":"additional","affiliation":[{"name":"Department of Pathology, NYU Langone Health , New York, NY , US"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aylin","family":"Simsir","sequence":"additional","affiliation":[{"name":"Department of Pathology, NYU Langone Health , New York, NY , US"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2023,4,13]]},"reference":[{"key":"2023080113031299600_CIT0001","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1158\/1055-9965.EPI-04-0569","article-title":"Trends in cervical squamous cell carcinoma incidence in 13 European countries: changing risk and the effects of screening","volume":"14","author":"Bray","year":"2005","journal-title":"Cancer Epidemiol Biomarkers Prev."},{"key":"2023080113031299600_CIT0002","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1002\/cncy.21521","article-title":"The Pap test and Bethesda 2014","volume":"123","author":"Nayar","year":"2015","journal-title":"Cancer Cytopathol"},{"key":"2023080113031299600_CIT0003","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1002\/(SICI)1097-0142(19970625)81:3<137::AID-CNCR1>3.0.CO;2-O","article-title":"Managing risk in gynecologic cytology: reactive and unsatisfactory smears","volume":"81","author":"Austin","year":"1997","journal-title":"Cancer."},{"key":"2023080113031299600_CIT0004","first-page":"47","article-title":"Analysis of cervical smears obtained within three years of the diagnosis of invasive cervical cancer","volume":"35","author":"Kristensen","year":"1991","journal-title":"Acta Cytol."},{"key":"2023080113031299600_CIT0005","first-page":"337","article-title":"High-grade squamous intraepithelial lesions and invasive carcinoma following the report of three negative Papanicolaou smears: screening failures or rapid progression","volume":"5","author":"Sherman","year":"1992","journal-title":"Mod Pathol."},{"key":"2023080113031299600_CIT0006","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1258\/096914104774061047","article-title":"CIN 2\/3 and cervical cancer in an organised screening programme after an unsatisfactory or a normal Pap smear: a seven-year prospective study of the Norwegian population-based screening programme","volume":"11","author":"Nygard","year":"2004","journal-title":"J Med Screen."},{"key":"2023080113031299600_CIT0007","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1002\/(SICI)1097-0142(19970625)81:3<139::AID-CNCR2>3.0.CO;2-M","article-title":"Clinicopathologic correlation of the unsatisfactory Papanicolaou smear","volume":"81","author":"Ransdell","year":"1997","journal-title":"Cancer."},{"key":"2023080113031299600_CIT0008","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1002\/cncr.22865","article-title":"Papanicolaou smear history in women with low-grade cytology before cervical cancer diagnosis","volume":"111","author":"Bofin","year":"2007","journal-title":"Cancer."},{"key":"2023080113031299600_CIT0009","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1136\/jcp.56.8.592","article-title":"Outcome of women with inadequate cervical smears followed up for five years","volume":"56","author":"Hock","year":"2003","journal-title":"J Clin Pathol."},{"key":"2023080113031299600_CIT0010","doi-asserted-by":"crossref","first-page":"76","DOI":"10.5858\/arpa.2011-0113-OA","article-title":"Causes and relevance of unsatisfactory and satisfactory but limited smears of liquid-based compared with conventional cervical cytology","volume":"136","author":"Siebers","year":"2012","journal-title":"Arch Pathol Lab Med."},{"key":"2023080113031299600_CIT0011","doi-asserted-by":"crossref","first-page":"738","DOI":"10.1309\/GA19KPY3YLMKVWYU","article-title":"Clinical significance of unsatisfactory conventional Pap smears owing to inadequate squamous cellularity defined by the Bethesda 2001 criterion","volume":"123","author":"Adams","year":"2005","journal-title":"Am J Clin Pathol."},{"key":"2023080113031299600_CIT0012","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1097\/LGT.0b013e31818474fd","article-title":"High-risk human papillomavirus DNA test results are useful for disease risk stratification in women with unsatisfactory liquid-based cytology Pap test results","volume":"13","author":"Zhao","year":"2009","journal-title":"J Low Genit Tract Dis."},{"key":"2023080113031299600_CIT0013","first-page":"264","article-title":"Implementation of the ThinPrep Imaging System in a tertiary military medical center","volume":"117","author":"Duby","year":"2009","journal-title":"Cancer."},{"key":"2023080113031299600_CIT0014","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1111\/j.1365-2303.2012.00982.x","article-title":"Prospective parallel randomized trial of the MultiCyte ThinPrep((R)) imaging system: the Scottish experience","volume":"24","author":"Palmer","year":"2013","journal-title":"Cytopathology."},{"key":"2023080113031299600_CIT0015","first-page":"474","article-title":"A comparison of ThinPrep Imager-assisted with manual screening, and its place in the New Zealand cervical cancer screening program","volume":"45","author":"Yeong","year":"2013","journal-title":"Pathology (Phila)."},{"key":"2023080113031299600_CIT0016","doi-asserted-by":"crossref","first-page":"702","DOI":"10.1016\/j.ygyno.2006.10.048","article-title":"Age-specific detection of high risk HPV DNA in cytologically normal, computer-imaged ThinPrep Pap samples","volume":"104","author":"Cibas","year":"2007","journal-title":"Gynecol Oncol."},{"key":"2023080113031299600_CIT0017","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1002\/cncy.21490","article-title":"Follow-up and clinical significance of unsatisfactory liquid-based Papanicolaou tests","volume":"123","author":"Owens","year":"2015","journal-title":"Cancer Cytopathol."},{"key":"2023080113031299600_CIT0018","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1097\/LGT.0000000000000525","article-title":"2019 ASCCP risk-based management consensus guidelines for abnormal cervical cancer screening tests and cancer precursors","volume":"24","author":"Perkins","year":"2020","journal-title":"J Low Genit Tract Dis."},{"key":"2023080113031299600_CIT0019","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1097\/LGT.0000000000000628","article-title":"Erratum: 2019 ASCCP risk-based management consensus guidelines for abnormal cervical cancer screening tests and cancer precursors","volume":"25","author":"Perkins","year":"2021","journal-title":"J Low Genit Tract Dis."},{"key":"2023080113031299600_CIT0020","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1097\/LGT.0b013e3181585b9b","article-title":"Cervical cytology specimen adequacy: patient management guidelines and optimizing specimen collection","volume":"12","author":"Davey","year":"2008","journal-title":"J Low Genit Tract Dis."},{"key":"2023080113031299600_CIT0021","doi-asserted-by":"crossref","first-page":"104201","DOI":"10.1016\/j.jcv.2019.104201","article-title":"Clinical performance of the HPV-Risk assay on cervical samples in SurePath medium using the VALGENT-4 panel","volume":"121","author":"Heideman","year":"2019","journal-title":"J Clin Virol."},{"key":"2023080113031299600_CIT0022","doi-asserted-by":"crossref","first-page":"1478","DOI":"10.1128\/JCM.03386-12","article-title":"Development and characterization of the Cobas human papillomavirus test","volume":"51","author":"Rao","year":"2013","journal-title":"J Clin Microbiol."},{"key":"2023080113031299600_CIT0023","author":"College of American Pathologists"},{"key":"2023080113031299600_CIT0024","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1016\/j.jasc.2014.05.003","article-title":"Common causes for unsatisfactory Pap tests in a high-risk population: insights into a yet unresolved problem in gynecologic cytology","volume":"3","author":"Quiroga-Garza","year":"2014","journal-title":"J Am Soc Cytopathol"},{"key":"2023080113031299600_CIT0025","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1002\/dc.20627","article-title":"Implementation of the ThinPrep imaging system in a high-volume metropolitan laboratory","volume":"35","author":"Miller","year":"2007","journal-title":"Diagn Cytopathol."},{"key":"2023080113031299600_CIT0026","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1016\/j.ygyno.2006.07.025","article-title":"Comparison of computer-assisted and manual screening of cervical cytology","volume":"104","author":"Lozano","year":"2007","journal-title":"Gynecol Oncol."},{"key":"2023080113031299600_CIT0027","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1002\/dc.20779","article-title":"Effectiveness of the ThinPrep Imaging System: clinical experience in a low risk screening population","volume":"36","author":"Papillo","year":"2008","journal-title":"Diagn Cytopathol."},{"key":"2023080113031299600_CIT0028","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1111\/j.1479-828X.2009.00998.x","article-title":"Cervical parakeratosis\/hyperkeratosis as an important cause for false negative results of Pap smear and human papillomavirus test","volume":"49","author":"Xiao","year":"2009","journal-title":"Aust N Z J Obstet Gynaecol."},{"key":"2023080113031299600_CIT0029","doi-asserted-by":"crossref","first-page":"117","DOI":"10.5468\/ogs.2015.58.2.117","article-title":"Impact of age on the false negative rate of human papillomavirus DNA test in patients with atypical squamous cells of undetermined significance","volume":"58","author":"Won","year":"2015","journal-title":"Obstet Gynecol Sci"},{"key":"2023080113031299600_CIT0030","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1002\/cncr.22688","article-title":"Significance and possible causes of false-negative results of reflex human papillomavirus infection testing","volume":"111","author":"Eltoum","year":"2007","journal-title":"Cancer."},{"key":"2023080113031299600_CIT0031","doi-asserted-by":"crossref","first-page":"48.e148.e1","DOI":"10.1016\/j.ajog.2016.07.042","article-title":"Follow-up of women with cervical cytological abnormalities showing atypical squamous cells of undetermined significance or low-grade squamous intraepithelial lesion: a nationwide cohort study","volume":"216","author":"Sundstrom","year":"2017","journal-title":"Am J Obstet Gynecol."},{"key":"2023080113031299600_CIT0032","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1016\/j.cmi.2021.04.031","article-title":"2020 list of human papillomavirus assays suitable for primary cervical cancer screening","volume":"27","author":"Arbyn","year":"2021","journal-title":"Clin Microbiol Infect."},{"key":"2023080113031299600_CIT0033","doi-asserted-by":"crossref","first-page":"104336","DOI":"10.1016\/j.jcv.2020.104336","article-title":"Clinical validation of the Cobas 4800 HPV assay using cervical samples in SurePath medium under the VALGENT4 framework","volume":"128","author":"Ejegod","year":"2020","journal-title":"J Clin Virol."},{"key":"2023080113031299600_CIT0034","doi-asserted-by":"crossref","first-page":"e58153","DOI":"10.1371\/journal.pone.0058153","article-title":"HPV testing by Cobas HPV test in a population from Catalonia","volume":"8","author":"Lloveras","year":"2013","journal-title":"PLoS One."},{"key":"2023080113031299600_CIT0035","doi-asserted-by":"crossref","first-page":"3983","DOI":"10.1128\/JCM.05552-11","article-title":"Clinical validation of the Cobas 4800 HPV test for cervical screening purposes","volume":"49","author":"Heideman","year":"2011","journal-title":"J Clin Microbiol."},{"key":"2023080113031299600_CIT0036","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1002\/ijc.24010","article-title":"Guidelines for human papillomavirus DNA test requirements for primary cervical cancer screening in women 30 years and older","volume":"124","author":"Meijer","year":"2009","journal-title":"Int J Cancer."},{"key":"2023080113031299600_CIT0037","first-page":"CD008587","article-title":"Cytology versus HPV testing for cervical cancer screening in the general population","volume":"8","author":"Koliopoulos","year":"2017","journal-title":"Cochrane Database Syst Rev."},{"key":"2023080113031299600_CIT0038","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1158\/1940-6207.CAPR-14-0409","article-title":"Five-year cervical (pre)cancer risk of women screened by HPV and cytology testing","volume":"8","author":"Uijterwaal","year":"2015","journal-title":"Cancer Prev Res (Phila)"},{"key":"2023080113031299600_CIT0039","doi-asserted-by":"crossref","first-page":"3044","DOI":"10.1200\/JCO.2011.38.8389","article-title":"Clinical human papillomavirus detection forecasts cervical cancer risk in women over 18 years of follow-up","volume":"30","author":"Castle","year":"2012","journal-title":"J Clin Oncol."},{"key":"2023080113031299600_CIT0040","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1016\/j.ejca.2011.01.008","article-title":"A comparison of HPV DNA testing and liquid based cytology over three rounds of primary cervical screening: extended follow up in the ARTISTIC trial","volume":"47","author":"Kitchener","year":"2011","journal-title":"Eur J Cancer."},{"key":"2023080113031299600_CIT0041","doi-asserted-by":"crossref","first-page":"g130","DOI":"10.1136\/bmj.g130","article-title":"Long term duration of protective effect for HPV negative women: follow-up of primary HPV screening randomised controlled trial","volume":"348","author":"Elfstrom","year":"2014","journal-title":"BMJ."},{"key":"2023080113031299600_CIT0042","doi-asserted-by":"crossref","first-page":"2456","DOI":"10.1002\/ijc.30385","article-title":"Human papillomavirus testing versus cytology in primary cervical cancer screening: end-of-study and extended follow-up results from the Canadian cervical cancer screening trial","volume":"139","author":"Isidean","year":"2016","journal-title":"Int J Cancer."},{"key":"2023080113031299600_CIT0043","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1517\/17530050802705680","article-title":"An update review on HPV testing methods for cervical neoplasia","volume":"3","author":"Koliopoulos","year":"2009","journal-title":"Expert Opin Med Diagn."},{"key":"2023080113031299600_CIT0044","doi-asserted-by":"crossref","first-page":"696","DOI":"10.1002\/dc.20890","article-title":"Restoring satisfactory status in ThinPrep Pap test specimens with too few squamous cells and containing microscopic red blood cells","volume":"36","author":"Pang","year":"2008","journal-title":"Diagn Cytopathol."},{"key":"2023080113031299600_CIT0045","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1002\/dc.21271","article-title":"Not all unsatisfactory ThinPrep cervical Pap tests are unsatisfactory: reprocessing improves the satisfactory and detection rates of ThinPrep cervical cytology","volume":"38","author":"AbdullGaffar","year":"2010","journal-title":"Diagn Cytopathol."},{"key":"2023080113031299600_CIT0046","first-page":"231","article-title":"Predictors of unsatisfactory conventional Pap smears","volume":"11","author":"Sharma","year":"2020","journal-title":"J Midlife Health."},{"key":"2023080113031299600_CIT0047","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1002\/dc.23032","article-title":"Factors contributing to high ThinPrep(R) Pap test unsatisfactory rates in an academic medical center laboratory","volume":"42","author":"Selvaggi","year":"2014","journal-title":"Diagn Cytopathol."},{"key":"2023080113031299600_CIT0048","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1002\/dc.25030","article-title":"Cervicovaginal cytology, HPV testing and vaginal flora in transmasculine persons receiving testosterone","volume":"50","author":"Lin","year":"2022","journal-title":"Diagn Cytopathol."},{"key":"2023080113031299600_CIT0049","doi-asserted-by":"crossref","first-page":"742","DOI":"10.5858\/arpa.2021-0199-OA","article-title":"Histologic findings in gynecologic tissue from transmasculine individuals undergoing gender-affirming surgery","volume":"146","author":"Lin","year":"2022","journal-title":"Arch Pathol Lab Med."}],"container-title":["American Journal of Clinical Pathology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/ajcp\/article-pdf\/160\/2\/137\/51016265\/aqad026.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ajcp\/article-pdf\/160\/2\/137\/51016265\/aqad026.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,1]],"date-time":"2023-08-01T13:09:19Z","timestamp":1690895359000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ajcp\/article\/160\/2\/137\/7117591"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,13]]},"references-count":49,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,4,13]]},"published-print":{"date-parts":[[2023,8,1]]}},"URL":"https:\/\/doi.org\/10.1093\/ajcp\/aqad026","relation":{},"ISSN":["0002-9173","1943-7722"],"issn-type":[{"value":"0002-9173","type":"print"},{"value":"1943-7722","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,8,1]]},"published":{"date-parts":[[2023,4,13]]}}}