Accuracy of human papillomavirus tests on self-collected urine versus clinician-collected samples for the detection of cervical precancer: a systematic review and meta-analysis

Hyun-Woong Cho, Sung Ryul Shim, Jae Kwan Lee, Jin Hwa Hong, Hyun-Woong Cho, Sung Ryul Shim, Jae Kwan Lee, Jin Hwa Hong

Abstract

Objective: The human papillomavirus (HPV) test is an effective screening tool to prevent cervical cancer. Urinary sampling for HPV detection improves the accessibility and participation of screening services and reduces the cost and burden on physicians. The clinical accuracy of urinary HPV test has yet to be determined via meta-analysis. This study assessed the clinical accuracy of these tests to detect cervical intraepithelial neoplasia (CIN) 2 or worse.

Methods: Relevant studies were identified using the PubMed, Embase, and Cochrane databases. Research eligibility was based on the clinical accuracy of HPV test on clinician-collected samples as a comparator test, and urine as an index test. The reference standard was the presence of CIN2 or worse. The pooled absolute, relative sensitivity, and specificity of the urinary HPV test versus clinician-collected samples were assessed using a bivariate model.

Results: The pooled sensitivity of urinary HPV test was significantly lower than that of clinician-collected samples (ratio=0.84, 95% confidence interval [CI]=0.78-0.91). However, some polymerase chain reaction (PCR)-based HPV test such as GP5+/6+ (relative sensitivity=0.98, 95% CI=0.91-1.05), SPF10 (relative sensitivity=0.98, 85% CI=0.88-1.08) and non GP5+/6+ PCR (relative sensitivity=1.00, 95% CI=0.88-1.14) showed similar sensitivity in both the urine and clinician-collected samples.

Conclusion: Our findings indicate that HPV test with some PCR-based assay on urine versus clinician-collected samples demonstrate similar clinical accuracy to detect CIN2 or worse. It suggests that urinary HPV test may present itself as a decent alternative screening tool for the detection of cervical pre-cancer.

Trial registration: PROSPERO identifier: CRD42021227901.

Keywords: Cervical Intraepithelial Neoplasia; Human Papillomavirus DNA Test; Urine; Uterine Cervical Neoplasms.

Conflict of interest statement

No potential conflict of interest relevant to this article was reported.

Copyright © 2022. Asian Society of Gynecologic Oncology, Korean Society of Gynecologic Oncology, and Japan Society of Gynecologic Oncology.

Figures

Fig. 1. Flow chart of study identification…
Fig. 1. Flow chart of study identification and selection.
CIN, cervical intraepithelial neoplasia; HPV, human papillomavirus.
Fig. 2. (A) Relative sensitivity; and (B)…
Fig. 2. (A) Relative sensitivity; and (B) specificity of urinary versus cervical HPV test, by clinical setting, for the detection of cervical intraepithelial neoplasia 2 or worse.
CI, confidence interval; HPV, human papillomavirus.

References

    1. Melnikow J, Henderson JT, Burda BU, Senger CA, Durbin S, Weyrich MS. Screening for cervical cancer with high-risk human papillomavirus testing: updated evidence report and systematic review for the us preventive services task force. JAMA. 2018;320:687–705.
    1. US Preventive Services Task Force. Curry SJ, Krist AH, Owens DK, Barry MJ, Caughey AB, et al. Screening for cervical cancer: US preventive services task force recommendation statement. JAMA. 2018;320:674–686.
    1. Arbyn M, Weiderpass E, Bruni L, de Sanjosé S, Saraiya M, Ferlay J, et al. Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis. Lancet Glob Health. 2020;8:e191–203.
    1. Arbyn M, Smith SB, Temin S, Sultana F, Castle P Collaboration on Self-Sampling and HPV Testing. Detecting cervical precancer and reaching underscreened women by using HPV testing on self samples: updated meta-analyses. BMJ. 2018;363:k4823.
    1. Ginsburg O, Paskett ED. Ethnic and racial disparities in cervical cancer: lessons from a modelling study of cervical cancer prevention. Lancet Public Health. 2018;3:e8–9.
    1. Peto J, Gilham C, Fletcher O, Matthews FE. The cervical cancer epidemic that screening has prevented in the UK. Lancet. 2004;364:249–256.
    1. Sellors JW, Lorincz AT, Mahony JB, Mielzynska I, Lytwyn A, Roth P, et al. Comparison of self-collected vaginal, vulvar and urine samples with physician-collected cervical samples for human papillomavirus testing to detect high-grade squamous intraepithelial lesions. CMAJ. 2000;163:513–518.
    1. Shin HY, Lee B, Hwang SH, Lee DO, Sung NY, Park JY, et al. Evaluation of satisfaction with three different cervical cancer screening modalities: clinician-collected Pap test vs. HPV test by self-sampling vs. HPV test by urine sampling. J Gynecol Oncol. 2019;30:e76.
    1. Chamot E, Mulambia C, Kapambwe S, Shrestha S, Parham GP, Macwan'gi M, et al. Preference for human papillomavirus-based cervical cancer screening: results of a choice-based conjoint study in Zambia. J Low Genit Tract Dis. 2015;19:119–123.
    1. Van Keer S, Pattyn J, Tjalma WAA, Van Ostade X, Ieven M, Van Damme P, et al. First-void urine: a potential biomarker source for triage of high-risk human papillomavirus infected women. Eur J Obstet Gynecol Reprod Biol. 2017;216:1–11.
    1. Pathak N, Dodds J, Zamora J, Khan K. Accuracy of urinary human papillomavirus testing for presence of cervical HPV: systematic review and meta-analysis. BMJ. 2014;349:g5264.
    1. Cuzick J, Cadman L, Ahmad AS, Ho L, Terry G, Kleeman M, et al. Performance and diagnostic accuracy of a urine-based human papillomavirus assay in a referral population. Cancer Epidemiol Biomarkers Prev. 2017;26:1053–1059.
    1. Leeman A, Del Pino M, Molijn A, Rodriguez A, Torné A, de Koning M, et al. HPV testing in first-void urine provides sensitivity for CIN2+ detection comparable with a smear taken by a clinician or a brush-based self-sample: cross-sectional data from a triage population. BJOG. 2017;124:1356–1363.
    1. Senkomago V, Des Marais AC, Rahangdale L, Vibat CR, Erlander MG, Smith JS. Comparison of urine specimen collection times and testing fractions for the detection of high-risk human papillomavirus and high-grade cervical precancer. J Clin Virol. 2016;74:26–31.
    1. Alameda F, Bellosillo B, Fusté P, Musset M, Mariñoso ML, Mancebo G, et al. Human papillomavirus detection in urine samples: an alternative screening method. J Low Genit Tract Dis. 2007;11:5–7.
    1. Asciutto KC, Henningsson AJ, Borgfeldt H, Darlin L, Borgfeldt C. Vaginal and urine self-sampling compared to cervical sampling for HPV-testing with the Cobas 4800 HPV test. Anticancer Res. 2017;37:4183–4187.
    1. Asciutto KC, Ernstson A, Forslund O, Borgfeldt C. Self-sampling with HPV mRNA analyses from vagina and urine compared with cervical samples. J Clin Virol. 2018;101:69–73.
    1. Bernal S, Palomares JC, Artura A, Parra M, Cabezas JL, Robles A, et al. Comparison of urine and cervical samples for detecting human papillomavirus (HPV) with the Cobas 4800 HPV test. J Clin Virol. 2014;61:548–552.
    1. Buchegger K, Viscarra T, Andana A, Ili C, López J, Zanella L, et al. Detection and genotyping of human papillomavirus virus (HPV): a comparative analysis of clinical performance in cervical and urine samples in Chilean women. Int J Clin Exp Pathol. 2018;11:5413–5421.
    1. Arias M, Jang D, Dockter J, Ratnam S, Shah A, Elit L, et al. Treatment of first-void urine with Aptima Transfer Solution increases detection of high-risk HPV E6/E7 mRNA. J Virol Methods. 2019;267:48–52.
    1. Padhy RR, Davidov A, Madrigal L, Alcide G, Spahiu A. Detection of high-risk human papillomavirus RNA in urine for cervical cancer screening with HPV 16 & 18/45 genotyping. Heliyon (Lond) 2020;6:e03745
    1. Piyathilake CJ, Badiga S, Chambers MM, Brill IK, Matthews R, Partridge EE. Accuracy of urinary human papillomavirus testing for the presence of cervical human papillomaviruses and higher grades of cervical intraepithelial neoplasia. Cancer. 2016;122:2836–2844.
    1. Rohner E, Rahangdale L, Sanusi B, Knittel AK, Vaughan L, Chesko K, et al. Test accuracy of human papillomavirus in urine for detection of cervical intraepithelial neoplasia. J Clin Microbiol. 2020;58:e01443-19.
    1. Sahasrabuddhe VV, Gravitt PE, Dunn ST, Brown D, Allen RA, Eby YJ, et al. Comparison of human papillomavirus detections in urine, vulvar, and cervical samples from women attending a colposcopy clinic. J Clin Microbiol. 2014;52:187–192.
    1. Sahasrabuddhe VV, Gravitt PE, Dunn ST, Robbins D, Brown D, Allen RA, et al. Evaluation of clinical performance of a novel urine-based HPV detection assay among women attending a colposcopy clinic. J Clin Virol. 2014;60:414–417.
    1. Sargent A, Fletcher S, Bray K, Kitchener HC, Crosbie EJ. Cross-sectional study of HPV testing in self-sampled urine and comparison with matched vaginal and cervical samples in women attending colposcopy for the management of abnormal cervical screening. BMJ Open. 2019;9:e025388
    1. Sorbi F, Malentacchi F, Bussani C, Fantappie G, Pavone D, Turrini I, et al. HPV-DNA genotyping in women with cervical intraepithelial neoplasia undergoing to conization: comparison between cervical cytobrush and corresponding self-collected urine samples. Int J Gynecol Cancer. 2017;27:423.
    1. Stanczuk GA, Currie H, Baxter G, Foster A, Gibson L, Graham C, et al. Cobas 4800 HPV detection in the cervical, vaginal and urine samples of women with high-grade CIN before and after treatment. J Clin Pathol. 2015;68:567–570.
    1. Stanczuk G, Baxter G, Currie H, Lawrence J, Cuschieri K, Wilson A, et al. Clinical validation of hrHPV testing on vaginal and urine self-samples in primary cervical screening (cross-sectional results from the Papillomavirus Dumfries and Galloway-PaVDaG study) BMJ Open. 2016;6:e010660
    1. Tshomo U, Franceschi S, Tshokey T, Tobgay T, Baussano I, Tenet V, et al. Evaluation of the performance of human papillomavirus testing in paired urine and clinician-collected cervical samples among women aged over 30 years in Bhutan. Virol J. 2017;14:74.
    1. Xu H, Yu Y, George W, Smith JS, Hu S, Dang L, et al. Comparison of the performance of paired urine and cervical samples for cervical cancer screening in screening population. J Med Virol. 2020;92:234–240.
    1. Arbyn M, Verdoodt F, Snijders PJ, Verhoef VM, Suonio E, Dillner L, et al. Accuracy of human papillomavirus testing on self-collected versus clinician-collected samples: a meta-analysis. Lancet Oncol. 2014;15:172–183.
    1. Snijders PJ, van den Brule AJ, Meijer CJ. The clinical relevance of human papillomavirus testing: relationship between analytical and clinical sensitivity. J Pathol. 2003;201:1–6.
    1. Enerly E, Olofsson C, Nygård M. Monitoring human papillomavirus prevalence in urine samples: a review. Clin Epidemiol. 2013;5:67–79.
    1. Atkinson AE, Mandujano CAM, Bejarano S, Kennedy LS, Tsongalis GJ. Screening for human papillomavirus in a low- and middle-income country. J Glob Oncol. 2019;5:JGO1800233.
    1. de Martel C, Plummer M, Vignat J, Franceschi S. Worldwide burden of cancer attributable to HPV by site, country and HPV type. Int J Cancer. 2017;141:664–670.
    1. Brenner H, Gefeller O. Variation of sensitivity, specificity, likelihood ratios and predictive values with disease prevalence. Stat Med. 1997;16:981–991.
    1. Chaowawanit W, Tangjitgamol S, Kantathavorn N, Phoolcharoen N, Kittisiam T, Khunnarong J, et al. Knowledge, attitudes and behavior of Bangkok metropolitan women regarding cervical cancer screening. Asian Pac J Cancer Prev. 2016;17:945–952.
    1. Polman NJ, Ebisch RMF, Heideman DAM, Melchers WJG, Bekkers RLM, Molijn AC, et al. Performance of human papillomavirus testing on self-collected versus clinician-collected samples for the detection of cervical intraepithelial neoplasia of grade 2 or worse: a randomised, paired screen-positive, non-inferiority trial. Lancet Oncol. 2019;20:229–238.

Source: PubMed

スポンサーと協力者

医学的状態

薬物療法

3
購読する