Skip to main content

Agreement of self- and physician-collected samples for detection of high-risk human papillomavirus infections in women attending a colposcopy clinic in Thailand

Abstract

Objective

To study the concordance between vaginal self- and endocervical physician-collected high-risk (hr) HPV testing in Thai women who attended a colposcopy clinic. Vaginal samples were obtained by self-sampling with a dry brush before endocervical samples were obtained by physicians. Both specimens were analyzed for hrHPV by Cobas4800 HPV test.

Results

Of the 247 pairs of samples, overall hrHPV prevalence from self- and physician-collected samples was 41.3 and 36.0%, respectively. The overall agreement between the methods was 74.5% with κ 0.46 (P < 0.001). Our study revealed moderate agreement between self- and physician-collected methods for hrHPV testing.

Introduction

Worldwide trends in incidence and mortality rate of cervical cancer have decreased as a result of effective organized screening programs, however, cervical cancer remains an important health problem in less-developed countries. In Thailand, it is the second most common cancer in women, with an age-standardized incidence rate of 17.8 per 100,000 [1, 2].

The Ministry of Public Health in Thailand launched a national screening program for women aged 30–60 years since 2002 but the coverage rate was 46–67%, which was lower than the target of 75% [3,4,5]. The main reasons for avoiding cervical cancer screening in Thai women were embarrassment and fear of pain or fear of vaginal examination [6, 7].

Human papillomavirus (HPV) testing was approved for primary screening because of its satisfactory sensitivity for detecting high-grade precancerous cervical lesions [8,9,10]. Self-sampling HPV testing has been increasingly adopted for cervical cancer screening [11, 12]. Many studies have shown the advantage of self-sampling in increasing screening attendance and coverage [13,14,15,16,17,18]. Most studies have revealed high agreement between HPV screening results from self- and physician-collected specimens [19,20,21,22,23,24,25] and positive acceptability and preferences among women [26, 27].

Due to the uncommon use of tampon among Thai women, most of them are unfamiliar with inserting the device into their vagina. From our previous study, there was a concern that some women might not use the self-sample device properly [28]. There have been no previous studies compared self-sampling with standard methods for HPV screening in Thailand. We conducted this study to evaluate the agreement between self-sampling vaginal and physician-collected cervical HPV testing in Thai women.

Main text

Study populations

The study protocol was approved by the Institutional Review Board of Chulabhorn Hospital (No. 10/2013). We recruited women aged 30–70 years who visited a colposcopy clinic at Chulabhorn Hospital, Bangkok, Thailand during March 1 to June 30, 2015. Women were eligible for inclusion if they were attending the colposcopy clinic, aged 30–70 years, had no history of cervical cancer, had not undergone a hysterectomy, and were currently not pregnant.

Sample collection

After the participants had given written informed consent to participate in the study, they received instructions by video made by research project’s staffs to explain how to use the vaginal self-sampling brush, verbal and illustrations for vaginal self-sampling. The vaginal specimens were first obtained by self-sampling with the Evalyn Brush (Rovers Medical Devices B.V., Oss, The Netherlands), which is a dry brush. Then, the participants were examined by a gynecological oncologist who obtained an endocervical sample with a Cervex-Brush (Rovers Medical Devices).

Specimen preparation

The self- and physician-collected specimens were both suspended in 10 ml transport medium, SurePath Preservative Fluid (Becton, Dickinson and Company, USA).

High-risk (hr)HPV testing

All self-sampled and physician-collected specimens were sent to the central laboratory of Chulabhorn Hospital for hrHPV testing. All samples were analyzed by Cobas4800 HPV test (Roche Molecular Diagnostics, Pleasanton, CA, USA) within 1 week after collection.

Statistical analysis

Frequency, percentage, mean and standard deviation (SD) were used to calculate the general characteristics. The agreement levels were analyzed by Cohen’s kappa statistics. The statistical significance level was at 0.05. All data were analyzed by STATA/SE version 12.1.

Results

We enrolled 250 eligible women. Two participants were excluded because of a history of cervical cancer and previous hysterectomy. One pair of samples was excluded because of invalid test results. The mean and median ages of the remaining 247 participants were 47.2 and 47.0 years (range 30–70 years; SD 9.8 years), respectively. Table 1 shows the baseline characteristics of the participants. Most participants were Thai (96.8%) and Buddhist (99.2%). Average age at first sexual intercourse was 22.5 years (range 14–47 years; SD 4.9 years).

Table 1 Baseline characteristics of 247 study participants

Overall hrHPV prevalence was 41.3% (102/247) from self-collected specimens and 36.0% (89/247) from physician-collected specimens. The prevalence of hrHPV 16, 18 and non-16, 18 from self- and physician-collected specimens is shown in Table 2.

Table 2 Prevalence of hrHPV from self- and physician-collected specimens

The concordance of hrHPV test results between self- and physician-collected specimens is shown in Table 3. The concordance was 74.5% with moderate agreement and κ 0.46 for overall hrHPV. For hrHPV 16, the concordance was 96.4% with substantial agreement and κ 0.72. For hrHPV 18, there was 96.8% concordance with moderate agreement and κ 0.48.

Table 3 Concordance between hrHPV detection by self- and physician-collected method

Discussion

We found that the prevalence of hrHPV from self-collected specimens (41.3%) was higher than from physician-collected specimens (36.0%). To explain, the self-collected specimens are a combination of cervical and vaginal cells. Additionally, the sampling order first obtained from the self-collected specimens may then collect higher number of exfoliated cells. In particular, the higher prevalence of low-risk HPV in the lower vagina than in the cervix and scanty cross-reactivity of the hrHPV assay to low-risk genotypes can partially explain this finding [18, 29].

Our study revealed 74.5% concordance between self- and physician-collected specimens in detecting overall hrHPV with κ 0.46, which showed moderate agreement. The level of agreement in our study was not as high as that in most previous studies [19,20,21,22,23,24,25]. Most previous studies found 70.6–94.2% concordance with κ 0.6–0.9, which represented substantial agreement between these two methods. However, some studies revealed the same level of agreement as in our study [29,30,31].

One study showed that the agreement between these two methods was lower among older women, which supports our results [30]. The median age of our participants was 47.0 years, which was higher than that in other studies (26.4–41.0 years) [19, 21,22,23,24,25], and ~ 40% of the participants were older than 50 years. This might be the reason why our study showed lower concordance and agreement than the other studies showed. Additionally, some women in this study reported that they were not confident about using the device correctly [28].

Although the agreement level of overall hrHPV between self- and physician-collected samples was moderate, the agreement level of HPV 16 was substantial, with concordance of 93.36% and κ 0.72. This finding for HPV 16 was the same as in the other studies [21, 25]. As mentioned above, the prevalence of HPV from self-collected specimens was higher than from physician-collected specimens. It might be then as a consequence that the concordance levels of other hrHPV were moderate. Whereas, HPV 16 was described in one previous study as the most prevalent HPV type in the cervical specimens, and especially with higher prevalence than in vaginal specimens [32]. Hence, these findings can partially explain about the high agreement and concordance levels of HPV 16.

Limitations

All the participants in our study did the self-collection first then underwent pelvic examination to obtain physician-collected specimens later. This sampling order may have resulted in the self-collected specimens having more exfoliated cells than the physician-collected specimens had.

Our participants were women who attended a colposcopy clinic for various reasons such as abnormal cytology or positive HPV testing, so the prevalence of HPV in this group was higher than in the normal population. The prevalence of hrHPV in our study was 41.3 and 36.0% from self- and physician-collected specimens, respectively. The prevalence of hrHPV in Thai women in previous studies was 3.3–14.0% [33,34,36].

Due to the level of agreement in our study was slightly lower than in most previous studies, more studies with larger populations are needed to explore the reliability and feasibility of self-sampling of HPV as a method for cervical cancer screening in Thai and other Asian women. The molecular and biomarker analyses may be combined to achieve greater accuracy of the test.

Abbreviations

HPV:

human papillomavirus

hrHPV:

high-risk human papillomavirus

References

  1. 1.

    Torre LA, Siegel RL, Ward EM, Jemal A. Global cancer incidence and mortality rates and trends—an update. Cancer Epidemiol Biomark Prev. 2016;25(1):16–27.

    Article  Google Scholar 

  2. 2.

    Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Mukem S, Meng Q, Sriplung H, Tangcharoensathien V. Low coverage and disparities of breast and cervical cancer screening in Thai women: analysis of national representative household surveys. Asian Pac J Cancer Prev. 2015;16(18):8541–51.

    Article  PubMed  Google Scholar 

  4. 4.

    Joseph R, Manosoontorn S, Petcharoen N, Sangrajrang S, Senkomago V, Saraiya M. Assessing cervical cancer screening coverage using a population-based behavioral risk factor survey—Thailand, 2010. J Womens Health. 2015;24(12):966–8.

    Article  Google Scholar 

  5. 5.

    van Ballegooijen M, van den Akker-van Marle E, Patnick J, Lynge E, Arbyn M, Anttila A, et al. Overview of important cervical cancer screening process values in European Union (EU) countries, and tentative predictions of the corresponding effectiveness and cost-effectiveness. Eur J Cancer. 2000;36:2177–88.

    Article  PubMed  Google Scholar 

  6. 6.

    Oranratanaphan S, Amatyakul P, Iramaneerat K, Srithipayawan S. Knowledge, attitudes and practices about the Pap smear among medical workers in Naresuan University Hospital, Thailand. Asian Pac J Cancer Prev. 2010;11:1727–30.

    PubMed  Google Scholar 

  7. 7.

    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(3):945–52.

    Article  PubMed  Google Scholar 

  8. 8.

    Ogilvie GS, Krajden M, van Niekerk D, Smith LW, Cook D, Ceballos K, et al. HPV for cervical cancer screening (HPV FOCAL): complete round 1 results of a randomized trial comparing HPV-based primary screening to liquid-based cytology for cervical cancer. Int J Cancer. 2017;140(2):440–8.

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Wright TC, Stoler MH, Behrens CM, Sharma A, Zhang G, Wright TL. Primary cervical cancer screening with human papillomavirus: end of study results from the ATHENA study using HPV as the first-line screening test. Gynecol Oncol. 2015;136(2):189–97.

    Article  PubMed  Google Scholar 

  10. 10.

    Ronco G, Dillner J, Elfstrom KM, Tunesi S, Snijders PJ, Arbyn M, et al. Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet. 2014;383(9916):524–32.

    Article  PubMed  Google Scholar 

  11. 11.

    Delere Y, Schuster M, Vartazarowa E, Hansel T, Hagemann I, Borchardt S, et al. Cervicovaginal self-sampling is a reliable method for determination of prevalence of human papillomavirus genotypes in women aged 20 to 30 years. J Clin Microbiol. 2011;49(10):3519–22.

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Ting J, Mugo N, Kwatampora J, Hill C, Chitwa M, Patel S, et al. High-risk human papillomavirus messenger RNA testing in physician- and self-collected specimens for cervical lesion detection in high-risk women, Kenya. Sex Transm Dis. 2013;40(7):584–9.

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Lim AW, Hollingworth A, Kalwij S, Curran G, Sasieni P. Offering self-sampling to cervical screening non-attenders in primary care. J Med Screen. 2017;24(1):43–9.

    Article  PubMed  Google Scholar 

  14. 14.

    Enerly E, Bonde J, Schee K, Pedersen H, Lonnberg S, Nygard M. Self-sampling for human papillomavirus testing among non-attenders increases attendance to the Norwegian cervical cancer screening programme. PLoS ONE. 2016;11(4):e0151978.

    Article  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Racey CS, Gesink DC, Burchell AN, Trivers S, Wong T, Rebbapragada A. Randomized intervention of self-collected sampling for human papillomavirus testing in under-screened rural women: uptake of screening and acceptability. J Womens Health. 2016;25(5):489–97.

    Article  Google Scholar 

  16. 16.

    Duke P, Godwin M, Ratnam S, Dawson L, Fontaine D, Lear A, et al. Effect of vaginal self-sampling on cervical cancer screening rates: a community-based study in Newfoundland. BMC Womens Health. 2015;15:47.

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Giorgi Rossi P, Fortunato C, Barbarino P, Boveri S, Caroli S, Del Mistro A, et al. Self-sampling to increase participation in cervical cancer screening: an RCT comparing home mailing, distribution in pharmacies, and recall letter. Br J Cancer. 2015;112(4):667–75.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Haguenoer K, Sengchanh S, Gaudy-Graffin C, Boyard J, Fontenay R, Marret H, et al. Vaginal self-sampling is a cost-effective way to increase participation in a cervical cancer screening programme: a randomised trial. Br J Cancer. 2014;111(11):2187–96.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Obiri-Yeboah D, Adu-Sarkodie Y, Djigma F, Hayfron-Benjamin A, Abdul L, Simpore J, et al. Self-collected vaginal sampling for the detection of genital human papillomavirus (HPV) using care HPV among Ghanaian women. BMC Womens Health. 2017;17(1):86.

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Boggan JC, Walmer DK, Henderson G, Chakhtoura N, McCarthy SH, Beauvais HJ, et al. Vaginal self-sampling for human papillomavirus infection as a primary cervical cancer screening tool in a Haitian population. Sex Transm Dis. 2015;42(11):655–9.

    Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Johnson DC, Bhatta MP, Smith JS, Kempf MC, Broker TR, Vermund SH, et al. Assessment of high-risk human papillomavirus infections using clinician- and self-collected cervical sampling methods in rural women from far western Nepal. PLoS ONE. 2014;9(6):e101255.

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Ortiz AP, Romaguera J, Perez CM, Otero Y, Soto-Salgado M, Mendez K, et al. Human papillomavirus infection in women in Puerto Rico: agreement between physician-collected and self-collected anogenital specimens. J Low Genit Tract Dis. 2013;17(2):210–7.

    Article  PubMed  Google Scholar 

  23. 23.

    Bhatla N, Dar L, Patro AR, Kumar P, Kriplani A, Gulati A, et al. Can human papillomavirus DNA testing of self-collected vaginal samples compare with physician-collected cervical samples and cytology for cervical cancer screening in developing countries? Cancer Epidemiol. 2009;33(6):446–50.

    Article  PubMed  Google Scholar 

  24. 24.

    Sowjanya AP, Paul P, Vedantham H, Ramakrishna G, Vidyadhari D, Vijayaraghavan K, et al. Suitability of self-collected vaginal samples for cervical cancer screening in peri urban villages in Andhra Pradesh, India. Cancer Epidemiol Biomark Prev. 2009;18(5):1373–8.

    Article  Google Scholar 

  25. 25.

    Safaeian M, Kiddugavu M, Gravitt PE, Ssekasanvu J, Murokora D, Sklar M, et al. Comparability of self-collected vaginal swabs and physician-collected cervical swabs for detection of human papillomavirus infections in Rakai, Uganda. Sex Transm Dis. 2007;34(7):429–36.

    PubMed  Google Scholar 

  26. 26.

    Waller J, McCaffery K, Forrest S, Szarewski A, Cadman L, Austin J, et al. Acceptability of unsupervised HPV self-sampling using written instructions. J Med Screen. 2006;13(4):208–13.

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Virtanen A, Nieminen P, Niironen M, Luostarinen T, Anttila A. Self-sampling experiences among non-attendees to cervical screening. Gynecol Oncol. 2014;135(3):487–94.

    Article  PubMed  Google Scholar 

  28. 28.

    Phoolcharoen N, Kantathavorn N, Krisorakun W, Taepisitpong C, Krongthong W, Saeloo S. Acceptability of self-sample human papillomavirus testing among Thai women visiting a colposcopy clinic. J Community Health. 2018. https://doi.org/10.1007/s10900-017-0460-2. (Epub ahead of print).

  29. 29.

    Castle PE, Gage JC, Partridge EE, Rausa A, Gravitt PE, Scarinci IC. Human papillomavirus genotypes detected in clinician-collected and self-collected specimens from women living in the Mississippi Delta. BMC Infect Dis. 2013;13:5.

    Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Khanna N, Mishra SI, Tian G, Tan MT, Arnold S, Lee C, et al. Human papillomavirus detection in self-collected vaginal specimens and matched clinician-collected cervical specimens. Int J Gynecol Cancer. 2007;17(3):615–22.

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Karwalajtys T, Howard M, Sellors JW, Kaczorowski J. Vaginal self sampling versus physician cervical sampling for HPV among younger and older women. Sex Transm Infect. 2006;82(4):337–9.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Castle PE, Rodriguez AC, Porras C, Herrero R, Schiffman M, Gonzalez P, et al. A comparison of cervical and vaginal human papillomavirus. Sex Transm Dis. 2007;34(11):849–55.

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Tangjitgamol S, Kantathavorn N, Kittisiam T, Chaowawanit W, Phoolcharoen N, Manusirivithaya S, et al. Prevalence and associated factors of abnormal cervical cytology and high risk HPV DNA among Bangkok metropolitan women. Asian Pac J Cancer Prev. 2016;17(7):3147–53.

    PubMed  Google Scholar 

  34. 34.

    Kantathavorn N, Mahidol C, Sritana N, Sricharunrat T, Phoolcharoen N, Auewarakul C, et al. Genotypic distribution of human papillomavirus (HPV) and cervical cytology findings in 5906 Thai women undergoing cervical cancer screening programs. Infect Agent Cancer. 2015;10:7.

    Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Phoolcharoen N, Kantathavorn N, Sricharunrat T, Saeloo S, Krongthong W. A population-based study of cervical cytology findings and human papillomavirus infection in a suburban area of Thailand. Gynecol Oncol Rep. 2017;21:73–7.

    Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Marks MA, Gupta S, Liaw KL, Tadesse A, Kim E, Phongnarisorn C, et al. Prevalence and correlates of HPV among women attending family-planning clinics in Thailand. BMC Infect Dis. 2015;15:159.

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Altman DG. Practical statistics for medical research. London: Chapman and Hall; 1991.

    Google Scholar 

Download references

Authors’ contributions

NP study concept and design, participants recruitment and sample collection, statistical analysis, manuscript drafting and revision. NK study concept and design, participants recruitment and sample collection, manuscript revision. WasK participants recruitment and sample collection. TS, NT and GS laboratory method. CT and SS participants coordination and data collection. WarK statistical analysis. All authors read and approved the final manuscript.

Acknowledgements

We thank all participants, Staffs of Women Health Center and Central Laboratory Unit, Chulabhorn Hospital for participating in this study and Cathel Kerr, Ph.D., from Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

The dataset is available upon reasonable request from the corresponding author.

Consent for publication

Not applicable.

Ethics approval and consent to participate

The study protocol was approved by the Institutional Review Board of Chulabhorn Hospital (No. 10/2013). All participants gave written informed consent to participate in the study.

Funding

This study was supported by Chulabhorn Hospital.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Natacha Phoolcharoen.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Phoolcharoen, N., Kantathavorn, N., Krisorakun, W. et al. Agreement of self- and physician-collected samples for detection of high-risk human papillomavirus infections in women attending a colposcopy clinic in Thailand. BMC Res Notes 11, 136 (2018). https://doi.org/10.1186/s13104-018-3241-9

Download citation

Keywords

  • Self-sampling
  • HPV testing
  • Cervical cancer screening
  • Colposcopy
  • Thailand