Are vaginal swabs comparable to cervical smears for human papillomavirus DNA testing?

Liselotte Coorevits, Ans Traen, Luc Bingé, Jo Van Dorpe, Marleen Praet, Jerina Boelens, Elizaveta Padalko, Liselotte Coorevits, Ans Traen, Luc Bingé, Jo Van Dorpe, Marleen Praet, Jerina Boelens, Elizaveta Padalko

Abstract

Objective: Human papillomavirus (HPV) testing is widely incorporated into cervical cancer screening strategies. Current screening requires pelvic examination for cervical sampling, which may compromise participation. The acceptance could be raised by introducing testing on vaginal swabs. We explored the interchangeability of vaginal swabs and cervical smears for HPV testing, by means of a prospective study conducted in female sex workers (FSWs). Besides, we report on the occurrence of 32 different HPV genotypes in FSW with low-grade squamous intraepithelial lesion (LSIL) or high-grade squamous intraepithelial lesion (HSIL).

Methods: Paired physician-collected vaginal swabs and cervical smears from 303 FSW were tested for HPV using the Abbott RealTime High-Risk HPV assay. Cervical cytology was examined on cervical smears. In case of HSIL/LSIL cytological classification (n=52), both samples were genotyped using INNO-LiPa HPV Genotyping Extra II.

Results: The overall prevalence of high-risk (HR)-HPV was 51%. In FSW with HSIL/LSIL cervical cytology, the sensitivity and specificity of vaginal samples for the detection of HR-HPV was 100% and 70% and for probable HR-HPV 100% and 91%. The mean number of genotypes identified in vaginal samples (mean=3.5; 95% confidence interval [CI]=2.8-4.2) was significantly higher than in cervical smear samples (mean=2.6; 95% CI=2.1-3.0) (p=0.001). The most frequently encountered HR-HPV genotypes were HPV16, 31, 51, and 52.

Conclusion: As our study shows that vaginal swabs are equivalent to cervical smears for the detection of (probable) HR-HPV, vaginal swabs can be used for HPV testing in cervical cancer screening strategies. Given the acceptance of vaginal sampling, this finding offers an opportunity to boost screening coverage.

Keywords: Chlamydia Trachomatis; Mycoplasma Genitalium; Neisseria Gonorrhoeae; Papillomaviridae; Sexually Transmitted Diseases; Trichomonas Vaginalis.

Conflict of interest statement

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

Copyright © 2018. Asian Society of Gynecologic Oncology, Korean Society of Gynecologic Oncology

Figures

Fig. 1
Fig. 1
Flowchart of inclusion of FSWs and number of positive results for HR-HPV on CS in function of the result of cervical cytology. ASC-US, atypical squamous cells of undetermined significance; CS, ThinPrep cervical smear; FSW, female sex worker; HPV, human papillomavirus; HR, high-risk; HSIL, high-grade squamous intraepithelial lesion; LSIL, low-grade squamous intraepithelial lesion; NILM, negative for intraepithelial lesions or malignancy; +, positive; −, negative. *Significantly higher positivity rate than NILM (p=0.001); †Significantly higher positivity rate than ASC-US (p<0.001); ‡Significantly higher positivity rate than NILM (p=0.019); §Significantly higher positivity rate than ASC-US (p=0.001).
Fig. 2
Fig. 2
Paired analysis of HPV positivity for each risk group in VA and CS from 52 FSWs.
CS, ThinPrep cervical smear; FSW, female sex worker; HPV, human papillomavirus; HR, high-risk; LR, low-risk; pHR, probably high-risk; UR, unknown risk; VA, vaginal Abbott swab. *Significant difference between VA and CS (p=0.039).
Fig. 3
Fig. 3
Number of HPV genotypes identified in paired VA and CS samples collected from 52 FSWs. CS, ThinPrep cervical smear; FSW, female sex worker; HPV, human papillomavirus; VA, vaginal Abbott swab.

References

    1. Taylor S, Bunge E, Bakker M, Castellsagué X. The incidence, clearance and persistence of non-cervical human papillomavirus infections: a systematic review of the literature. BMC Infect Dis. 2016;16:293.
    1. Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003;348:518–527.
    1. Lorincz A, Castanon A, Wey Lim AW, Sasieni P. New strategies for human papillomavirus-based cervical screening. Womens Health (Lond) 2013;9:443–452.
    1. Schwebke JR, Hobbs MM, Taylor SN, Sena AC, Catania MG, Weinbaum BS, et al. Molecular testing for Trichomonas vaginalis in women: results from a prospective U.S. clinical trial. J Clin Microbiol. 2011;49:4106–4111.
    1. Fang J, Husman C, DeSilva L, Chang R, Peralta L. Evaluation of self-collected vaginal swab, first void urine, and endocervical swab specimens for the detection of Chlamydia trachomatis and Neisseria gonorrhoeae in adolescent females. J Pediatr Adolesc Gynecol. 2008;21:355–360.
    1. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–174.
    1. Nouws S, Carregosa A, Benoy I, Bogers J, Vanden Broeck D. Epidemiology of human papillomavirus type 67 in Belgian women (OC 05-03); EUROGIN International Symposia 2016; 2016 Jun 15–18; Salzburg, Austria. Paris: EUROGIN; 2016.
    1. Arbyn M, Snijders PJ, Meijer CJ, Berkhof J, Cuschieri K, Kocjan BJ, et al. Which high-risk HPV assays fulfil criteria for use in primary cervical cancer screening? Clin Microbiol Infect. 2015;21:817–826.
    1. Mak R, Van Renterghem L, Cuvelier C. Cervical smears and human papillomavirus typing in sex workers. Sex Transm Infect. 2004;80:118–120.
    1. Depuydt CE, Leuridan E, Van Damme P, Bogers J, Vereecken AJ, Donders GG. Epidemiology of Trichomonas vaginalis and human papillomavirus infection detected by real-time PCR in flanders. Gynecol Obstet Invest. 2010;70:273–280.
    1. Vielot N, Hudgens MG, Mugo N, Chitwa M, Kimani J, Smith J. The role of chlamydia trachomatis in high-risk human papillomavirus persistence among female sex workers in Nairobi, Kenya. Sex Transm Dis. 2015;42:305–311.
    1. Cwikel JG, Lazer T, Press F, Lazer S. Sexually transmissible infections among female sex workers: an international review with an emphasis on hard-to-access populations. Sex Health. 2008;5:9–16.
    1. Ghosh I, Ghosh P, Bharti AC, Mandal R, Biswas J, Basu P. Prevalence of human papillomavirus and co-existent sexually transmitted infections among female sex workers, men having sex with men and injectable drug abusers from eastern India. Asian Pac J Cancer Prev. 2012;13:799–802.
    1. Yin YP, Li HM, Xiang Z, Liang GJ, Shi MQ, Zhou YJ, et al. Association of sexually transmitted infections with high-risk human papillomavirus types: a survey with 802 female sex workers in China. Sex Transm Dis. 2013;40:493–495.
    1. Soohoo M, Blas M, Byraiah G, Carcamo C, Brown B. Cervical HPV infection in female sex workers: a global perspective. Open AIDS J. 2013;7:58–66.
    1. Peng RR, Li HM, Chang H, Li JH, Wang AL, Chen XS. Prevalence and genotype distribution of cervical human papillomavirus infection among female sex workers in Asia: a systematic literature review and meta-analysis. Sex Health. 2012;9:113–119.
    1. Dunne EF, Unger ER, Sternberg M, McQuillan G, Swan DC, Patel SS, et al. Prevalence of HPV infection among females in the United States. JAMA. 2007;297:813–819.
    1. Satterwhite CL, Torrone E, Meites E, Dunne EF, Mahajan R, Ocfemia MC, et al. Sexually transmitted infections among US women and men: prevalence and incidence estimates, 2008. Sex Transm Dis. 2013;40:187–193.
    1. Manhart LE, Koutsky LA. Do condoms prevent genital HPV infection, external genital warts, or cervical neoplasia? A meta-analysis. Sex Transm Dis. 2002;29:725–735.
    1. Harper DM, Longacre MR, Noll WW, Belloni DR, Cole BF. Factors affecting the detection rate of human papillomavirus. Ann Fam Med. 2003;1:221–227.
    1. Arbyn M, Haelens A, Desomer A, Verdoodt F, Thiry N, Francart J, et al. Cervical cancer screening program and Human Papillomavirus (HPV) testing, part II: update on HPV primary screening. Brussels: Belgian Health Care Knowledge Centre (KCE); 2015.
    1. Baldwin S, Santos C, Mendez Brown E, Nuño T, Giuliano A, Davis J, et al. Comparison of type-specific human papillomavirus data from self and clinician directed sampling. Gynecol Oncol. 2005;97:612–617.
    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. Petignat P, Hankins C, Walmsley S, Money D, Provencher D, Pourreaux K, et al. Self-sampling is associated with increased detection of human papillomavirus DNA in the genital tract of HIV-seropositive women. Clin Infect Dis. 2005;41:527–534.
    1. Winer RL, Lee SK, Hughes JP, Adam DE, Kiviat NB, Koutsky LA. Genital human papillomavirus infection: incidence and risk factors in a cohort of female university students. Am J Epidemiol. 2003;157:218–226.
    1. Moscicki AB, Widdice L, Ma Y, Farhat S, Miller-Benningfield S, Jonte J, et al. Comparison of natural histories of human papillomavirus detected by clinician- and self-sampling. Int J Cancer. 2010;127:1882–1892.
    1. Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD. Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med. 1998;338:423–428.
    1. Else EA, Swoyer R, Zhang Y, Taddeo FJ, Bryan JT, Lawson J, et al. Comparison of real-time multiplex human papillomavirus (HPV) PCR assays with INNO-LiPA HPV genotyping extra assay. J Clin Microbiol. 2011;49:1907–1912.

Source: PubMed

3
Sottoscrivi