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Can Human Papillomavirus DNA Self-sampling be an Acceptable and Reliable Option for Cervical Cancer Screening in Female Sex Workers?

Wong, Eliza L.Y. PhD, MPH, BSN, RN, FHKCHSE, FCHSE; Cheung, Annie W.L. MPhil, BBA; Huang, Fenwei MPH, BSc; Chor, Josette S.Y. PhD, MPH, MBBS, BSc, FHKAM (Community Medicine)

doi: 10.1097/NCC.0000000000000462
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Background: The causal relation between human papillomavirus (HPV) and cervical cancer has enabled HPV self-sampling to be envisaged as a possible screening method.

Objectives: The aim of this study is to explore the acceptability and reliability of HPV DNA self-sampling as an alternative option for cervical screening among female sex workers.

Methods: Sixty-eight participants carried out self-sampling for HPV testing, gave a clinician-obtained sample for HPV testing, and a Papanicolaou test. After the samplings, the participants were questioned on the acceptability of the tests.

Results: Most participants (65.6%) preferred to adopt HPV DNA self-sampling in the future; in particular, those without previous experience of Papanicolaou tests marginally significantly preferred self-sampling (86.7%, P = .055). The overall crude agreement in HPV detection rates between clinician and HPV DNA self-sampling was 85.3% (58/68), with a κ of 0.69 (95% confidence interval, 0.51–0.87). The sensitivity and specificity of self-collected samples were 66.7% and 66.1%, respectively, and the positive and negative predicted values were 24.0% and 92.5%, respectively. The prevalence of HPV was slightly higher in self-collected samples (39.7%, 27/68) than in clinician-collected samples (36.8%, 25/68). The participants expressed positive attitudes toward self-sampling but were less confident in their skills of self-sampling compared with clinicians (70.6% versus 91.2%).

Conclusions: The findings showed that self-sampling could be incorporated into current cervical cancer screening approaches.

Implications for Practice: Self-sampling could potentially increase compliance to cervical cancer screening and thus reduce the morbidity and mortality from cervical cancer. Further research and education on self-sampling will be required for women of diverse backgrounds.

Author Affiliations: The Jockey Club School of Public Health and Primary Care, The Chinese University of Hong Kong, Hong Kong Special Administrative Region, China.

The study was funded by Direct Grant of Research, the Chinese University of Hong Kong.

The authors have no conflicts of interest to disclose.

Correspondence: Eliza L.Y. Wong, PhD, MPH, BSN, RN, FHKCHSE, FCHSE, School of Public Health Building, Prince of Wales Hospital, Shatin, New Territories, Hong Kong (lywong@cuhk.edu.hk).

Accepted for publication November 7, 2016.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially.

Cervical cancer is the fourth most common female cancer in the world, and approximately 528 000 new cases and 266 000 deaths were reported worldwide in 2012.1 More than half of the women who develop cervical cancer have never had a Papanicolaou test or have not been screened regularly.2 In the Hong Kong Special Administrative Region (HKSAR) of China, approximately 57% of local women aged 25 to 64 years reported having had a Papanicolaou test screen in the previous 3 years.3 Female sex workers (FSWs), who are at higher risk of human papillomavirus (HPV) infection and developing cervical cancer because of an early age at first sexual intercourse, cigarette smoking, multiple sexual partners, and a high frequency of intercourse, had a lower screening rate of 27.5%.4,5 A local study in Hong Kong reported that the prevalence of atypical squamous cells of unknown significance (ASCUS) was 6.23% and that of low-grade squamous intraepithelial lesion (LGSIL) or worse was 6.23% among FSWs.6 Of the FSWs recruited at an outreach well-women clinic for FSWs, 71.8% were new migrants and 8.9% were nonlocal illegal immigrants or on a temporary visitor visa.7 Because of the expense, the barriers to access to screening, and problems regarding their identities, FSWs are less liable to seek medical help or screening.8 A numbers of studies have also indicated that the low uptake rate for Papanicolaou tests was related to multiple barriers, including the fear of abnormal results, experiencing pain, inconvenience, and embarrassment.9–11 Hence, the exploration of alternative cervical screening methods to increase the coverage and overcome reticence among high-risk and underscreened populations is urgent.

Infection with high-risk types of HPV plays a causal role in the development of cervical cancer.12,13 High-risk types of HPV account for about 90% of precancerous changes, including carcinoma in situ and adenocarcinoma in situ.14 Thus, HPV DNA testing has been recommended as one of the primary screening methods for cervical cancer by the World Health Organization,13 and Kim et al15 suggested that such testing is a more cost-effective triage measure for women with ASCUS than repeated Papanicolaou tests or immediate colposcopy. With the availability of HPV DNA testing, clinical guidelines have been revised in some countries to provide several screening options, including cytology every 1 to 3 years with HPV DNA testing for the triage of equivocal cytology results.16,17 These strategies could enhance the uptake rate of cervical screening, provide greater protection against cervical cancer than cytology-only strategies, and be more cost-effective than other public health interventions.18,19 Further studies abroad have reported that the degree of acceptability of HPV DNA self-sampling was greater than that of clinician sampling and cytology,20,21 but this remains unknown for those at higher risk of HPV infection.

This clinical trial was the first of its kind to explore the acceptability and reliability of HPV DNA self-sampling as an alternative cervical cancer screening method in underscreened populations in Hong Kong. The findings provide an important reference for health policy makers and healthcare providers to better understand various screening options and thus increase the uptake rate of cervical screening by implementing practical and effective screening programs.

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Materials and Methods

This was the first clinical trial in FSWs in the HKSAR of China to investigate the acceptability and reliability of HPV DNA self-sampling as an alternative cervical cancer screening method. Between November 3, 2009, and May 4, 2010, FSWs were recruited from a nongovernment organization (NGO) that provides health services to FSWs in HKSAR, where sexually transmitted disease and gynecology inspections are offered free of charge, regardless of their identities.

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Participants

The eligibility criteria were aged 18 years or older, not currently pregnant, had no known abnormal Papanicolaou test results and not having presented symptoms of cervical cancer, genital cancer, cervical surgery, or immune treatment of the cervix during the 6 months before recruitment into the study. Based on a literature review, a minimum of 30 participants were required for a selected minority group for treatment in a pilot study.22,23 Therefore, a minimum of 30 eligible FSWs were the target for this study.

Eligible participants who consented to participate in the study were given a study identification number. They then carried out HPV DNA self-sampling and underwent clinician sampling, with an interval of about 20 to 30 minutes between the 2 samplings. On completion of each screening method, the participants were invited to a face-to-face individual interview with a research officer using a structured questionnaire to explore the degree of acceptability (attitudes and preference) of HPV DNA self-sampling versus clinician sampling. Consequently, the response to their attitudes toward HPV DNA self-sampling would not be influenced by clinician sampling (Figure 1).

Figure 1

Figure 1

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Interventions

HPV DNA SELF-SAMPLING

For HPV DNA self-sampling, verbal and written instructions with a diagram in Chinese were given to participants so that they fully understood the materials and study procedures. The participants were shown how to insert a Dacron swab at least 2 in into the vagina and make 2 full rotations, then take the swab out of the vagina and place it in a vial of phosphate-buffered saline.

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CLINICIAN SAMPLING

For clinician sampling, ectocervical samples were collected by a clinician using a cytobrush and a Dacron swab for a Papanicolaou test and HPV DNA testing, respectively.

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Laboratory Testing

All 3 cervical screening tests were analyzed in the university laboratory. Fifteen of the HPV types studied, including 16, 18, 26, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 68, and 73, were grouped as high-risk (including those that were probable high-risk) and 21 of the HPV types, including 6, 11, 30, 34, 40, 42, 43, 44, 53, 54, 55, 57, 61, 62, 66, 67, 69, 70, 82, 84, 85, and 97, were grouped as low risk (including those with unknown risk).24 The clinical management of participants followed the routine practice of the clinic according to the Bethesda system.

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Instrument and Outcome Measures

INSTRUMENT

The questionnaire included 16 items under 3 sections: section 1—attitudes to 7 dimensions that included embarrassment, discomfort, anxiety, unpleasantness, degree of fear and relaxation, and confidence in the test being performed correctly by HPV DNA self-sampling versus clinician sampling and a preference for using HPV DNA self-sampling in the future; section 2—behavioral aspects (smoking, alcohol consumption, and experience of Papanicolaou tests) and self-perceived health status; and section 3—sociodemographic information.

The questionnaire was derived from an extensive literature review,20,21,25,26 and a pilot test was carried out with 10 women to ensure its comprehension and readability. Cronbach’s α coefficient was calculated using the items on the attitudes toward the 2 sampling methods to confirm the internal reliability of the construct. The α coefficient for the self-sampling attitudes and Papanicolaou test scales were .68 and .78, respectively, indicating that the questionnaire had sufficient internal consistency.

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OUTCOME MEASURES

The major outcome measures of this study were acceptability and reliability of HPV DNA self-sampling as an alternative cervical cancer screening method. The participants' degree of acceptability, which referred to their attitudes toward HPV DNA self-sampling in 7 dimensions (embarrassment, discomfort, anxiety, unpleasantness, degree of scare and relaxation, and confidence in the test being performed correctly), was explored using a 5-point rating scale (from extremely disagree to extremely agree), together with their preference to use HPV DNA self-sampling in the future. For the reliability of HPV DNA self-sampling, a comparison of the proportion of HPV-positive results in self-collected samples with that in clinician-collected samples and Papanicolaou tests was made. Also, agreements in laboratory results between self-sampling and clinician sampling for HPV and between self-sampling and Papanicolaou test were investigated using the κ coefficient.

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Statistical Analysis

Data were managed and analyzed using PASW version 18. Descriptive results of the characteristics of the respondents are presented. The differences in participants' attitudes toward the 2 sampling methods and in the characteristics of participants who preferred clinician sampling and those who preferred self-sampling or either method were examined using χ2 and t tests. Multiple logistic regression analysis was conducted to determine the factors that might be associated with preferences for self-sampling methods. The agreement between HPV DNA self-sampling and clinician sampling was determined by κ statistics, where the strength of agreement of κ lower than 0 was poor, 0 to 0.20 was slight, 0.21 to 0.40 was fair, 0.41 to 0.60 was moderate, 0.61 to 0.80 was substantial, and 0.81 to 1.00 was almost perfect.27 McNemar test was used to test the significance of unequal distribution of discordant results in the detection of HPV between the 2 tests. To compare the performance of HPV DNA and Papanicolaou testing, the sensitivity, specificity, and positive (PPV) and negative (NPV) predicted values were estimated. A P value < .05 was considered to be statistically significant.

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Results

Recruitment

A total of 69 of 71 FSWs (97%) from an NGO, aged 22 to 59 years, met the inclusion criteria, and 68 potential participants agreed to join the study (response rate, 99%). Among 68 participants; 65 (96%) underwent a Papanicolaou test, with 3 refusing because of unavailability and 64 completed whole set of questionnaire by face-to-face interview, where 4 refused to provide response related to sociodemographics because of personal concern. The mean age of the 64 participants was 38.2 years. Approximately half of the participants had completed upper secondary education or above (43.6 %) and were married or cohabiting (51.6%). Most of the FSWs had at least 1 child (77.4%) and resided in HKSAR (72.6%). None of the participants reported a history of any cancer; however, family members of 28.3% of the participants had a history of cancer. They were mainly nonsmokers (61.9%), were infrequent drinkers (87.5%), had undergone Papanicolaou tests (76.2%), and rated their health as average or above (70.3%). The sociodemographic details are shown in Table 1. No adverse event was reported in the study.

Table 1

Table 1

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Acceptability of HPV DNA Self-sampling as an Alternative Cervical Cancer Screening Method

Among the 68 participants, 65.6% (42/64) indicated a preference for adopting HPV DNA self-sampling in the future or accepting both methods because it was convenient, simple, and less frightening, whereas 34.4% (22/64) preferred clinician sampling at a clinic during a pelvic examination because they had more confidence in the procedure carried out by healthcare professionals; 5.9% (4/68) had no plans for future screening or no opinions on preferences for future cervical screening; 86.7% (13/15) of the women without a Papanicolaou test history stated a preference for using self-sampling at home or at a clinic or either method in the future; and 58.3% (28/48) of the women with a Papanicolaou test history opted for the self-sampling method.

Univariate analysis showed marginally significant differences in some demographic characteristics, namely, age and history of Papanicolaou test, between the groups with different preferences for cervical screening methods (Papanicolaou test vs self-sampling at home or in a clinic or either method). No statistically significant differences in other perceived health status, demographic characteristics, or smoking habits were found (Table 1). Multiple regression analysis showed that older age was significantly associated with a preference for self-sampling (odds ratio, 1.10; P = .035); a history of no Papanicolaou tests was marginally significantly associated with a preference for self-sampling at home or at clinic or either method (odds ratio, 0.18; P = .055).

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Reliability of HPV DNA Self-sampling

COMPARISON OF HPV DNA SELF-SAMPLING AND PAPANICOLAOU TESTS

Of 65 successfully obtained Papanicolaou test samples, 56 tested normal, but 1 (1.5%) high-grade squamous intraepithelial lesion, 2 (3.1%) LGSIL, and 6 (9.2%) ASCUS cases were identified. Among the 9 cases with an abnormal Papanicolaou test, the proportion of positive results found after self-sampling was 66.7% (6/9). Among cases with a normal Papanicolaou test result, 66.1% (37/56) tested negative for HPV in self-collected samples (Table 2). These findings resulted in a PPV of 24.0%, an NPV of 92.5%, a sensitivity of 66.7%, and a specificity of 66.1% for HPV DNA testing of self-collected samples.

Table 2

Table 2

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COMPARISON OF HPV DNA SELF-SAMPLING AND CLINICIAN SAMPLING

The prevalence of HPV was 39.7% (27/68) in self-collected samples and 36.8% (25/68) in clinician-collected samples. The overall crude agreement in HPV detection between the HPV DNA self-sampling and clinician sampling was 85.3% (58/68). The agreement in HPV-positive results was 67.7%, with a substantial agreement κ of 0.69 (95% confidence interval, 0.51–0.87). A total of 10 discordant results were found: 6 positive results in self-collected samples were negative in clinician-collected samples, whereas 4 negative results in self-collected samples were positive in clinician-collected samples. No statistically significant difference in the detection of HPV DNA was found between the 2 types of sample collection (McNemar test = 0.4; P = .527).

Regarding agreement on the HPV genotypes, a total of 17 (17/21) HPV DNA self-sampling and clinician-sampling pairs provided HPV genotypes. There was perfect agreement in 11 of 17 (64.7%) positive sample pairs, partial agreement (at least 1 type detected in both samples) in 3 of 17 (17.6%) positive sample pairs, and complete discordance in 3 of 17 (17.6%) positive sample pairs.

The agreement for high-risk HPV genotypes was considerably greater than that for low-risk HPV genotypes in a comparison of self- and clinician-collected samples (Table 3). Overall, low-risk HPV-84 was the most prevalent type detected in both self- and clinician-collected samples (26.1% and 21.1%, respectively), followed by high-risk HPV-58 (17.4% and 15.8%, respectively) and high-risk HPV-16 (13.0% and 10.5%, respectively) (Figure 2).

Table 3

Table 3

Figure 2

Figure 2

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Perceptions of and Attitudes to HPV DNA Self-sampling

When questioned on their attitudes toward the 2 sampling methods, all participants understood the self-sampling procedure explained by health professionals, and 88% felt the diagrams on collection were clear. Participants felt less embarrassed, anxious, unpleasantness, and frightened and more relaxed with the self-sampling method, although none of these factors were significantly different; 70.6% were confident that self-sampling was performed correctly, and there was significantly more (91.2%) confidence in the clinician-sampling method (P < .05) (Table 4).

Table 4

Table 4

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Discussion

This was the first study to explore the acceptability and reliability of HPV DNA self-sampling in FSWs. The findings provide confirmatory evidence that it is a feasible, easy-to-implement option that could potentially be integrated into conventional cervical screening to increase its uptake rate.

Participants indicated a high acceptance of the use of self-sampling as a screening tool in the future, which reiterated the results of other studies.28–30 Women who had never had a Papanicolaou test especially stated a preference for self-sampling in the future. Thus, HPV DNA self-sampling could be a potential approach to boost up the response rate/compliance to cervical screening in nonattendees.

Women had a more positive attitude toward self-sampling, although this was not statistically significant. Embarrassment was found to be one of the greatest obstacles to Papanicolaou tests,9,11,20 whereas self-sampling ensures privacy in collecting vaginal samples. Dzuba et al20 stated that confidence in the clinician-sampling procedure was the main reason for participants' preferences. Those in our study had a significant preference for clinician sampling over self-sampling with regard to the accuracy of the procedure, possibly because of their unfamiliarity with the method of self-sampling and belief that Papanicolaou tests were a conventional and superior screening program.31 Therefore, offering skill-based education and encouraging self-sampling would be helpful to the public in the future to raise confidence in handling the procedures and acceptance of the test. A further study on the correlation between preference and confidence in handling procedures is thus required.

The agreement in HPV-positive results (67.7% with a κ of 0.69) between self- and clinician sampling was reasonable compared with studies that used vaginal swabs in self-sampling methods, for which the agreement ranged from 0.45 to 0.84.32 The results of the detection of the types of HPV that were positive were highly consistent between self- and clinician sampling. The prevalence of HPV infection was slightly higher in self-collected samples than in clinician-collected samples. One possible reason could be that HPV infection found in tissues in the vaginal areas was not detected in cervical samples. The reported prevalence of HPV after self-sampling and clinician sampling for HPV DNA testing was moderately higher than that in studies in various other geographical regions.33 This could be related to the characteristics of our study participants who were more sexually active with multiple sexual partners and thus had a higher risk of HPV infection and a higher HPV viral load in their cervico-vaginal discharge.

Human papillomavirus DNA testing of clinician-obtained samples had greater sensitivity and specificity than self-collected samples did. The results were similar to those of other studies abroad,32,34 although the sensitivity and specificity varied considerably across these studies.30 The PPV of self-sampling (24%) was relatively low, but the NPV was reasonable (92.5%). The NPV indicated that HPV DNA self-sampling could potentially be incorporated into conventional screening to lengthen the interval between cervical screening and thus make it more cost-effective. Conversely, the small PPV showed the necessity of following up those diagnosed with positive results after a self-sampling HPV DNA test, owing to the large number of false-positives. However, the low cost and convenience of self-sampling overcome the drawbacks.

The main difference between this study and most other self-sampling studies is that our subjects were middle-aged FSWs who were less likely to undergo cervical screening even though they were at a high risk of developing cervical cancer.5 The willingness to sign up for and the acceptability of HPV DNA self-sampling of FSWs could differ from those of non–sex workers.

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Conclusion and Implications

This study has added valuable findings to existing evidence in the field of cervical screening that is either doctor or nurse led. Human papillomavirus DNA self-sampling could potentially be incorporated into conventional cervical cancer screening to boost the screening rate and compliance in underscreened population, in a less invasive and generally acceptable manner, and with relatively simple instructions to reduce the morbidity and mortality of cervical cancer. This study also provides information to assist nurses to counsel underscreened population and encourage them to attend cervical screening by an alternative tool. Access to self-sampling at NGOs that provide related services could also improve the screening rate. Publicity and education in the skills of self-sampling for women are required, and training nurses to offer such services to the public would be helpful in the future. As the results were limited by the small sample size, further study should be conducted on the attitudes toward self-sampling among women of diverse backgrounds in Hong Kong, to confirm the feasibility of using HPV DNA self-sampling as a tool and the possibility of using it as the sole screening tool for the detection of cervical cancer.

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ACKNOWLEDGMENTS

We thank the local NGO (organization name not revealed to ensure the confidentiality of participants) providing us the site of data collection. We also thank Dr Francois Y Fong for conducting gynecological examinations and Dr Krystal CK Lee for carrying out laboratory tests.

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Keywords:

Acceptability; Cervical cancer screening; HPV DNA self-sampling; Reliability; Underscreened population group

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