Accuracy of urinary human papillomavirus testing for presence of cervical HPV: systematic review and meta-analysis

Neha Pathak, Julie Dodds, Javier Zamora, Khalid Khan, Neha Pathak, Julie Dodds, Javier Zamora, Khalid Khan

Abstract

Objective: To determine the accuracy of testing for human papillomavirus (HPV) DNA in urine in detecting cervical HPV in sexually active women.

Design: Systematic review and meta-analysis.

Data sources: Searches of electronic databases from inception until December 2013, checks of reference lists, manual searches of recent issues of relevant journals, and contact with experts.

Eligibility criteria: Test accuracy studies in sexually active women that compared detection of urine HPV DNA with detection of cervical HPV DNA.

Data extraction and synthesis: Data relating to patient characteristics, study context, risk of bias, and test accuracy. 2 × 2 tables were constructed and synthesised by bivariate mixed effects meta-analysis.

Results: 16 articles reporting on 14 studies (1443 women) were eligible for meta-analysis. Most used commercial polymerase chain reaction methods on first void urine samples. Urine detection of any HPV had a pooled sensitivity of 87% (95% confidence interval 78% to 92%) and specificity of 94% (95% confidence interval 82% to 98%). Urine detection of high risk HPV had a pooled sensitivity of 77% (68% to 84%) and specificity of 88% (58% to 97%). Urine detection of HPV 16 and 18 had a pooled sensitivity of 73% (56% to 86%) and specificity of 98% (91% to 100%). Metaregression revealed an increase in sensitivity when urine samples were collected as first void compared with random or midstream (P=0.004).

Limitations: The major limitations of this review are the lack of a strictly uniform method for the detection of HPV in urine and the variation in accuracy between individual studies.

Conclusions: Testing urine for HPV seems to have good accuracy for the detection of cervical HPV, and testing first void urine samples is more accurate than random or midstream sampling. When cervical HPV detection is considered difficult in particular subgroups, urine testing should be regarded as an acceptable alternative.

Conflict of interest statement

Competing interests: All authors have completed the ICMJE uniform disclosure form at www.icmje.org/coi_disclosure.pdf and declare: no support from any organisation for the submitted work; no financial relationships with any organisations that might have an interest in the submitted work in the previous three years; no other relationships or activities that could appear to have influenced the submitted work.

© Pathak et al 2014.

Figures

https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4793832/bin/patn020452.f1_default.jpg
Fig 1 Study selection process
https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4793832/bin/patn020452.f2_default.jpg
Fig 2 QUADAS-2 quality assessment of 14 studies included in meta-analysis
https://www.ncbi.nlm.nih.gov/pmc/articles/instance/4793832/bin/patn020452.f3_default.jpg
Fig 3 Receiver operating characteristic plots for studies evaluating accuracy of detecting human papillomavirus (HPV) in urine compared with in cervix

References

    1. Einstein MH, Schiller JT, Viscidi RP, Strickler HD, Coursaget P, Tan T, et al. Clinician’s guide to human papillomavirus immunology: knowns and unknowns. Lancet Infect Dis 2009;9:347-56.
    1. Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, et al. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer 2007;121:621-32.
    1. Trent Cancer Registry. Profile of cervical cancer in england: incidence, mortality and survival. National Cancer Intelligence Network, 2012.
    1. National Cancer Intelligence Network. Cervical cancer incidence and screening coverage. 2014. .
    1. Saslow D, Solomon D, Lawson HW, Killackey M, Kulasingam SL, Cain J, et al. American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. CA Cancer J Clin 2012;62:147-72.
    1. Ronco G, Dillner J, Elfström KM, Tunesi S, Snijders PJF, Arbyn M, et al. Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet 383:524-32.
    1. Rijkaart DC, Berkhof J, Rozendaal L, van Kemenade FJ, Bulkmans NWJ, Heideman DAM, et al. Human papillomavirus testing for the detection of high-grade cervical intraepithelial neoplasia and cancer: final results of the POBASCAM randomised controlled trial. Lancet Oncol 2012;13:78-88.
    1. Kitchener HC, Gilham C, Sargent A, Bailey A, Albrow R, Roberts C, et al. A comparison of HPV DNA testing and liquid based cytology over three rounds of primary cervical screening: extended follow up in the ARTISTIC trial. Eur J Cancer 2011;47:864-71.
    1. Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Palma PD, Del Mistro A, et al. Efficacy of human papillomavirus testing for the detection of invasive cervical cancers and cervical intraepithelial neoplasia: a randomised controlled trial. Lancet Oncol 2010;11:249-57.
    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. Can Med Assoc J 2000;163:513-8.
    1. Vorsters A, Micalessi I, Bilcke J, Ieven M, Bogers J, Van Damme P. Detection of human papillomavirus DNA in urine. A review of the literature. Eur J Clin Microbiol Infect Dis 2012;31:627-40.
    1. Enerly E, Olofsson C, Nygard M. Monitoring human papillomavirus prevalence in urine samples: a review. Clin Epidemiol 2013;5:371.
    1. Chien PFW, Khan KS, Siassakos D. Registration of systematic reviews: PROSPERO. BJOG 2012;119:903-5.
    1. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol 2009;62:e1-34.
    1. Collaboration C. Handbook for DTA reviews. 2014. .
    1. Lijmer JG, Mol BW, Heisterkamp S, Bonsel GJ, Prins MH, van der Meulen JH, et al. Empirical evidence of design-related bias in studies of diagnostic tests. JAMA 1999;282:1061-6.
    1. Whiting PF, Rutjes AWS, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med 2011;155:529-36.
    1. Deeks JJ, Macaskill P, Irwig L. The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol 2005;58:882-93.
    1. Alameda F, Bellosillo B, Fuste P, Musset M, Marinoso ML, Mancebo G, et al. Human papillomavirus detection in urine samples: an alternative screening method. J Low Genitl Tract Dis 2007;11:5-7.
    1. Bissett SL, Howell-Jones R, Swift C, De Silva N, Biscornet L, Parry JV, et al. Human papillomavirus genotype detection and viral load in paired genital and urine samples from both females and males. J Med Virol 2011;83:1744-51.
    1. Cuschieri K, Nandwani R, McGough P, Cook F, Hogg L, Robertson C, et al. Urine testing as a surveillance tool to monitor the impact of HPV immunization programs. J Med Virol 2011;83:1983-7.
    1. Daponte A, Pournaras S, Mademtzis I, Hadjichristodoulou C, Kostopoulou E, Maniatis AN, et al. Evaluation of high-risk human papillomavirus types PCR detection in paired urine and cervical samples of women with abnormal cytology. J Clin Virol 2006;36:189-93.
    1. Daponte A, Tsezou A, Oikonomou P, Hadjichristodoulou C, Maniatis AN, Pournaras S, et al. Use of real-time PCR to detect human papillomavirus-16 viral loads in vaginal and urine self-sampled specimens. Clin Microbiol Infect 2008;14:619-21.
    1. Farnbrini M, Penna C, Pieralli A, Bussani C, Fallani MG, Andersson KL, et al. PCR detection rates of high risk human papillomavirus DNA in paired self-collected urine and cervical scrapes after laser CO2 conization for high-grade cervical intraepithelial neoplasia. Gynecol Oncol 2008;109:59-64.
    1. Forslund O, Hansson BG, Rymark P, Bjerre B. Human papillomavirus DNA in urine samples compared with that in simultaneously collected urethra and cervix samples. J Clin Microbiol 1993;31:1975-9.
    1. Gupta A, Arora R, Gupta S, Prusty BK, Kailash U, Batra S, et al. Human papillomavirus DNA in urine samples of women with or without cervical cancer and their male partners compared with simultaneously collected cervical/penile smear or biopsy specimens. J Clin Virol 2006;37:190-4.
    1. Jong EE, Mulder JW, van Gorp ECM, Wagenaar JKS, Derksen J, Westerga J, et al. The prevalence of human papillomavirus (HPV) infection in paired urine and cervical smear samples of HIV-infected women. J Clin Virol 2008;41:111-5.
    1. Munoz M, Camargo M, Soto-De Leon SC, Sanchez R, Parra D, Pineda AC, et al. Human papillomavirus detection from human immunodeficiency virus-infected Colombian women’s paired urine and cervical samples. Plos One 2013;8:7.
    1. Payan C, Ducancelle A, Aboubaker MH, Caer J, Tapia M, Chauvin A, et al. Human papillomavirus quantification in urine and cervical samples by using the Mx4000 and LightCycler general real-time PCR systems. J Clin Microbiol 2007;45:897-901.
    1. Pieralli A, Bussani C, Andersson KL, Mattei A, Fambrini M. Appendix to: “PCR detection rates of high risk human papillomavirus DNA in paired self-collected urine and cervical scrapes after laser CO(2) conization for high-grade cervical intraepithelial neoplasia”. Gynecol Oncol 2010;116:586-7.
    1. Prusty BK, Kumar A, Arora R, Batra S, Das BC. Human papillomavirus (HPV) DNA detection in self-collected urine. Int J Gynecol Obstetr 2005;90:223-7.
    1. Song E-S, Lee HJ, Hwang TS. Clinical efficacy of human papillomavirus DNA detection in urine from patients with various cervical lesions. J Korean Med Sci 2007;22:99-104.
    1. Stanczuk GA, Kay P, Allan B, Chirara M, Tswana SA, Bergstrom S, et al. Detection of human papillomavirus in urine and cervical swabs from patients with invasive cervical cancer. J Med Virol 2003;71:110-4.
    1. Strauss S, Jordens JZ, McBride D, Sonnex C, Edwards S, Desselberger U, et al. Detection and typing of human papillomavirus DNA in paired urine and cervical scrapes. Eur J Epidemiol 1999;15:537-43.
    1. Tanzi E, Bianchi S, Fasolo MM, Frati ER, Mazza F, Martinelli M, et al. High performance of a new PCR-based urine assay for HPV-DNA detection and genotyping. J Med Virol 2013;85:91-8.
    1. Jacobson DL, Womack SD, Peralta L, Zenilman JM, Feroli K, Maehr J, et al. Concordance of human papillomavirus in the cervix and urine among inner city adolescents. Pediatr Infect Dis J 2000;19:722-8.
    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;52:187-92.
    1. Mendez K, Romaguera J, Ortiz AP, López M, Steinau M, Unger ER. Urine-based human papillomavirus DNA testing as a screening tool for cervical cancer in high-risk women. Int J Gynecol Obstetr 2014;124:151-5.
    1. Munoz M, Camargo M, Soto-De Leon SC, Sanchez R, Pineda-Pena AC, Perez-Prados A, et al. Classical molecular tests using urine samples as a potential screening tool for human papillomavirus detection in human immunodeficiency virus-infected women. J Clin Microbiol 2013;51:3688-93.
    1. Brinkman JA, Jones WE, Gaffga AM, Sanders JA, Chaturvedi AK, Slavinsky J, et al. Detection of human papillomavirus DNA in urine specimens from human immunodeficiency virus-positive women. J Clin Microbiol 2002;40:3155-61.
    1. Leeflang MMG, Bossuyt PMM, Irwig L. Diagnostic test accuracy may vary with prevalence: implications for evidence-based diagnosis. J Clin Epidemiol 2009;62:5-12.
    1. Johnson DJ, Calderaro AC, Roberts KA. Variation in nuclear DNA concentrations during urination. J Forensic Sci 2007;52:110-3.
    1. Sehgal A, Gupta S, Parashari A, Sodhani P, Singh V. Urine HPV-DNA detection for cervical cancer screening: Prospects and prejudices. J Obstetr Gynaecol 2009;29:583-9.
    1. Mendez K, Romaguera J, Perez CM, Soto-Salgado M, Tortolero-Luna G, Palefsky JM, et al. Cervical human papillomavirus infection in a sample of Hispanic women living in Puerto Rico: comparison with cervical cytology reports. P R Health Sci J 2013;32:3-7.
    1. Cook RL, Hutchison SL, Østergaard L, Braithwaite RS, Ness RB. Systematic review: noninvasive testing for Chlamydia trachomatis and Neisseria gonorrhoeae. Ann Intern Med 2005;142:914-25.
    1. Network WHL. 2014. .
    1. Schünemann HJ, Andrew DO, Jan B, Paul G, Roman J, Gunn EV, et al. Grading quality of evidence and strength of recommendations for diagnostic tests and strategies. BMJ 2008;336:1106-10.
    1. Bossuyt PM, Irwig L, Craig J, Glasziou P. Comparative accuracy: assessing new tests against existing diagnostic pathways. BMJ 2006;332:1089-92.

Source: PubMed

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