Article Text

A cross-sectional study on the acceptability of self-collection for HPV testing among women in rural China
  1. YaoYao Guan1,
  2. Philip E Castle2,
  3. Shaoming Wang3,
  4. Belinda Li3,
  5. Changyan Feng3,
  6. Puwa Ci3,
  7. Xue Li3,
  8. Patti Gravitt4,5,
  9. You-Lin Qiao3
  1. 1Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
  2. 2American Society for Clinical Pathology Institute, Washington, DC, USA
  3. 3Department of Epidemiology, Cancer Institute/Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China
  4. 4Department of Epidemiology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Maryland, USA
  5. 5Department of Molecular Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, Maryland, USA
  1. Correspondence to YaoYao Guan, School of Medicine, Johns Hopkins University, 733 N. Broadway, Suite 137, Baltimore, MD 21205-2196, USA; yguan5{at}jhmi.edu

Abstract

Objective To assess the acceptability of using self-collection as a method of sampling for human papilloma virus testing in rural China.

Methods 174 women from the national cervical cancer screening programme in Xiangyuan County, China, were enrolled in our study and underwent self-collection, clinician collection, colposcopy examination and were administered questionnaire. The questionnaire assessed the patients' preference and acceptability of collection method.

Results The mean overall acceptability score for self-collection, although significantly less than the overall score for clinician collection (p<0.01), still is well above 4 (4.33 of 5), indicating high acceptability. The acceptability scores for self-collection and clinician collection were not significantly different on scales measuring comfort and convenience (p>0.05). The scores were significantly lower for self-collection on scales measuring trust, ability to collect specimen and perceived effects of testing compared with clinician collection (p<0.01). 74% of participants preferred clinician collection, and of these participants, 86% preferred it because they thought the results were more accurate.

Conclusions The study shows that self-collection was highly acceptable and that self-collection and clinician collection were equally comfortable and convenient; however, the participants still preferred clinician collection because of lack of trust in the results of self-collection. This indicates that self-collection is an acceptable potential method for screening but education programmes about the validity of self-collection that target general population may be needed prior to implementation.

  • HPV
  • China
  • women
  • cervical neoplasia
  • patients-views
  • children
  • cervicitis
  • testing
  • cervical cancer
  • self-sampling
  • cervix
  • epidemiology

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Introduction

Cervical cancer, the third most common type of cancer in women worldwide, primarily occurs in low- and middle-income countries (LMIC).1 The barriers that contribute to this disparity are inadequate medical infrastructure, poor access to screening programmes and lack of trained practitioners to perform, interpret and evaluate cytology tests.2 In order to address these disparities, there is a need for a sensitive, more cost-effective and systematic population-based screening programme.

Traditionally, women undergo a speculum examination for the collection of cervical specimens for human papilloma virus (HPV) or cytology testing. However, LMIC often lack the clinical infrastructure and healthcare personnel to perform pelvic examinations for general screening. Alternatively, self-collection of cervicovaginal specimens circumvents many of these issues, including obviating the need for a speculum that adds cost to the examination. Self-collected cervicovaginal specimens have been shown to be equally sensitive for detection of HPV DNA and slightly less sensitive for detection of precancerous lesions than clinician-collected cervical specimens.3–5 In LMIC, where clinic-based examinations are impractical and unfeasible, self-collection with HPV DNA testing is an attractive alternative or complementary strategy to the traditional clinician-directed cervical specimen collection.6

The objectives of our study are to assess the acceptability and preference of self-collection among Chinese women who might benefit from self-collection. To increase the feasibility of self-collection, we asked the women to use a novel, dry storage and transportation device (FTA Elute Cartridge; GE Healthcare, Chalfont St. Giles, UK) that avoids some of the pitfalls of liquid-based media such as high storage and transport cost. HPV DNA detection using this transport method for self-collected and clinician-collected specimens is well correlated.7–9

Materials and methods

The institutional review boards of the Cancer Institute/Hospital of the Chinese Academy of Medical Sciences in Beijing, China, approved the study, and the IRB of Johns Hopkins University School of Medicine and National Cancer Institute granted IRB exception for the study because all identifying information was removed.

Study subjects

We target our recruitment among women between the ages of 30–59 living in Xiangyuan County, Shanxi Province, China. Our participants were also offered to participate in the Chinese National Screening programme for Cervical Cancer sponsored by the Chinese government. Eligible women were not pregnant and have not had a hysterectomy. Informed written consent was obtained from all participants. We advertised the screening on TV, radio broadcast, posters and flyers to potentially eligible population of 6100 women in Xiangyuan County based on the national demographic registry, and the first 2500 women (41%) who responded to our advertisement and met our eligibility criteria were enrolled in the screening stage of the study. All 2500 women underwent initial screening in the local clinics, which consisted of gynaecologic examination with visual inspection with acetic acid and Lugol's iodine (VIA/VILI). We nested our feasibility and acceptability study of self-collection using FTA cards in this population by selecting and enrolling all 63 VIA/VILI-positive patients (2.5%) and a random sample of 111 VIA/VILI-negative patients (web-only file—figure 2). The response rates for both groups were 100%. All the VIA/VILI-positive patients received individual phone calls to return to clinic and were also provided with transportation to clinic. For the random selection of VIA/VILI-negative patients, every other woman registered on screening day 5 through 10 with negative VIA/VILI results were selected for the self-collection portion of the study. For this group of patients, self-collection/questionnaires were completed during the same visit as the VIA/VILI screening.

Study procedures

The 174 participants were offered transportation from their local villages to the Xiangyuan County Maternal and Child Health Hospital of Shanxi, where the study was conducted. Each participant had an initial one-on-one interview with a trained health worker, where basic demographic information (age, education, etc), past medical/gynecological history, family history, HPV knowledge assessment and other behavioural factors (transportation method, access to medical care, etc) were collected. The interview was conducted in the local Chinese dialect.

After the initial interview, the participants were given written and verbal instructions for self-collection. The instructions were given in Chinese and each step was also supplemented with descriptive figures (web-only file—figure 1). Instructions were also posted in the self-collection room for reference. Each participant obtained a Qiagen cervical sampler brush (Qiagen, Gaithersburg, Maryland, USA) and a Whatman indicating FTA elute cartridge (GE Healthcare; http://www.whatman.com/FTANucleicAcidCollectionStorageandPurification.aspx) and was sent to a private room for self-collection. The Whatman Indicating FTA Elute cartridge (FTA cartridge) uses a paper matrix chemically treated to denature and stabilise the DNA in the biospecimen and renders the specimen biohazard free. The paper is also infused with an indicator dye that changes colour, from purple to white, when the specimen is applied, thereby confirming that women performed the procedure properly. Upon completion, subjects underwent the clinician collection using the same type of collection materials. After clinician collection, a colposcopy examination was done and biopsy was taken if indicated by the examination. Finally, each participant was invited into another room to complete the questionnaire. In order to eliminate language and literacy barriers, local healthcare workers, who spoke both the local Chinese dialect and Mandarin Chinese, administered the questionnaires via one-on-one interviews. The study team trained the interviewers to make sure that they understood the meaning of the questions in order to accurately explain the questions if asked by the participants.

The questionnaire

A scale assessing acceptability of self-collection and HPV testing among female adolescents in the USA has been developed in a previous study.10 We adapted the general framework of the scale and expanded on some of the categories and changed the wording of the questions so that women living in rural China would more easily comprehend.

In assessing acceptability, we measured the following five categories: trust, ability to collect, comfort, convenience and perceived effects of testing (figure 1) For the category assessing trust, we asked if they believe that (1) the result is accurate and reliable, (2) the test is safe and (3) the procedure is not harmful. For the category assessing ability to collect, we asked if (1) the brush was easy to insert, (2) they are confident that the specimen was collected from the right location and (3) they are confident that the entire procedure was completed correctly. For the category assessing comfort we asked if (1) the procedure was not painful, (2) the procedure was not embarrassing, (3) the procedure provided adequate privacy and (4) they were not nervous during the procedure. For the category measuring convenience, we asked if the test is not time consuming. For the category measuring perceived affect of testing, we asked after the test if (1) they believe that the test is beneficial for their health and (2) they would recommend this test to others. The same set of questions was asked for both self-collection and clinician collection. Participants were asked to score the statement using a 5-point Likert scale (1: strongly disagree; 5: strongly agree) with higher scores corresponding with higher acceptability. In addition to acceptability, we also assessed the clarity of the self-collection instructions and if it was easy to apply specimen onto the FTA cards using the same 5-point Likert scale. Participants were also asked directly about their preference for self-collection or clinician collection and reason for their choices.

Figure 1

Acceptability questionnaire breakdown.

Statistical analysis

STATA V.10.0 was used for all statistical analysis. Paired t test was used to assess the difference between the acceptability scores of self-collection and clinician collection for each individual question. In order to evaluate the association between the acceptability scores and patients profiles, we performed multiple linear regression using mean acceptability score as the dependent variable and age, education, past cervical pathology, family history for cancer, HPV knowledge assessment score and method of transportation as independent variables. We also conducted logistic regression analysis to assess any association between patients' preference for self-collection (dependent variable) and the same set of patient characteristics as listed above. Variables with limited variance (ie, sexually transmitted infection history and travel time to clinic) were not used in the linear regression analysis and the logistic regression analysis.

Results

Participant profile

The demographic information of the participants is listed in table 1. Of the 174 women who were enrolled in the study, one (0.57%) participant was excluded from the study because the questionnaire was not completed. The participants had a mean, median and range of ages of 41.3, 41 and 30–58 years, respectively. Most (88.5%) had an education level of middle school or less. Majority of the women had some knowledge about HPV and cervical cancer: 80.9% (140/173) of the women got four of seven or more correct on the knowledge assessment.

Table 1

Demographics

Acceptability

The acceptability scores for each individual question are listed in table 2. The mean overall acceptability score for self-collection, although significantly less than the overall score for clinician collection (p<0.01), still is well above a 4 (out of maximum of 5), which indicated high acceptability. In terms of relative acceptability for each category of questions, the score for self-collection and clinician collection did not differ significantly on scores for comfort and convenience. However, self-collection scored lower than clinician collection for trust, ability to collect specimen and perceived effects on testing (p<0.01), indicating the lack of confidence in the quality of self-collection. However, the mean score for self-collection in all subcategories are between 3 and 5, with most above a 4. This indicates that self-collection was generally acceptable, although perceived as inferior to the clinician collection. The majority of the participants reported that the instructions to use the FTA cards were clear (98%) and it was easy to use (99%) (web-only file—table 1).

Table 2

Acceptability score: self-collection versus clinician collection

Preference

When asked about preference, 74% preferred clinician to self-collection. Participants were also asked to indicate at least one reason for their preference from a list of five reasons (less embarrassing, more comfortable, results are more accurate, cheaper or more convenient). Data are shown in figure 2. Of those who preferred clinician collection, 86% chose it because they think the results are more accurate. Of those who preferred self-collection, 39%, 26%, 17% and 14%, respectively, chose it because they thought self-collection was more convenient, less embarrassing, cheaper and more comfortable, respectively. By comparison, only 5%, 0%, 0% and 9% of the women who preferred clinician collection thought that clinician collection was more convenient, less embarrassing, cheaper and more comfortable, respectively.

Figure 2

Reason for preferred method of collection. The bars represent the percentage of participants who chose that particular reason for their preference out of all the women who preferred either self-collection or clinician collection.

Modelling

Linear regression analysis revealed little association between participants' mean acceptability score for self-collection and the demographic variables. Women who used buses as the main method of transportation to clinic were more likely to find self-collection acceptable compared with those who walked for transportation but the magnitude of this difference was small. Logistic regression analysis revealed no association between patient's preference for self-collection and demographic variables.

Discussion

Self-collection is a promising alternative to clinician collection of cervical specimens for HPV testing in LMIC where there is a lack of trained medical practitioners, such as the villages of Xiangyuan County, China, where we conducted our research. The acceptability results demonstrate a lack of trust in the self-collection method and the participants' own ability to collect the specimen. And for that reason, the majority of our participants preferred clinician collection to self-collection. There are several possible reasons that could explain the lack of trust in self-collection. One is the lack of higher education. Only 11% of the women in our study completed an education level above middle school, thus these women may prefer a clinician to perform the examination because they feel that they are not as qualified to do it correctly. Another reason is the lack of knowledge about self-collection. The current standard of care is HPV collection by a clinician using a speculum, and self-collection still is a novel idea to the general public. Although the women in our study found our self-collection instructions to be clear, there may not have been enough information about the accuracy and validity of self-collection to convince the participants that it is a sensitive method.

Our finding is consistent with several other prior studies. A study done by Tisci et al 11 in rural China demonstrated that self-collection is an acceptable method and the largest barrier in the study was education level. Another study by Anhang et al 12 in New York City showed that self-collection, although not preferred, is still found to be acceptable by the participants. In addition, a study done in UK found that the participants were concerned about results of self-collection and their ability to perform the procedure correctly.13 In a study of female adolescents in the USA by Kahn et al 10 using similar scales measuring acceptability as our study, the participants found a lack of confidence in their ability to collect the specimen and a lack of trust in the self-collection result. One aspect that differs between the Kahn study and ours is that the women in Kahn's study found self-collection to be less comfortable than clinician collection, whereas our participants found that they were equally comfortable; however, this difference maybe be contributed to the difference in the collection device that was used. There have also been other studies that showed self-collection to be more comfortable, less embarrassing and more private than clinician collection or that self-collection was more preferred.14 ,15 Cultural difference may be the main contributor to the differences between results. In rural China, almost all gynaecologists are women. Therefore, women undergoing screening may feel less embarrassed and more comfortable during a pelvic examination than women who live in cultures where male gynaecologists are more prominent. There may also be a cultural difference in the need for privacy. In rural China, where communal bathrooms and showers are more common, women may have a different threshold for privacy than women from other cultures.

The uniqueness of our study was the use of the Whatman indicating FTA elute card, which addresses a key but underappreciated aspect of using self-collection for cervical cancer screening: the transportation of the specimen from distant location where the specimen might be collected to a more central location where the HPV testing might be done. Compared with the traditional liquid-based transport media, samples are kept dry at ambient temperature on the FTA card, thus avoiding high cost and logistical challenges associated with transporting flammable and bio-hazardous liquid material. Another benefit of the FTA card is that it is very compact. Its small size (7.3 cm×3.8 cm) allowed us to fit many cards in a small box during transport. These benefits make the FTA cartridge suitable to be sent by regular mail, which is not feasible for liquid-based medium. In addition to the benefits of the FTA card, our study demonstrated that 99% of the women thought that it was easy to apply the sample onto the FTA card, making FTA card a highly acceptable new method of transportation. The FTA card offers public heath practitioners a more feasible and cost-effective specimen transport method for population-based cervical cancer screening using HPV testing and allows clinicians to offer their patients an alternative to a speculum examination for the collection of cervical specimens for HPV testing. Patients could collect the specimen at home and easily mail the FTA card back to the clinician by regular mail.

Another strength of our study is that we had very high response rate. Some of the reasons include that the research team made repeated phone calls for VIA/VILI-positive patients to return to clinic, provided reimbursement for transportation and provided multiple locations where patient can come in and participate in the study. For the random group of VIA/VILI-negative patients, self-collections were completed in one visit, which ensured high response rate. Only one participant was excluded from the study due to incomplete questionnaire. The high compliance rate (99.4%) can be mainly due to the fact that the questionnaire was completed via interviews, and the interviewers encouraged participants to answer each question.

Our study has some limitations. One of the limitations was that our study population might not have been representative to other rural communities in China in terms of their awareness of cervical cancer and HPV. The majority of our participants received a score of 4 of 7 or high on the knowledge assessment, when most of the participants only had an education of 9 years or less. This is because Xiangyuan County is one of the main national cervical cancer screening sites in rural China, and there have been several cervical cancer screening projects taking place in the Xiangyuan County over the past 5 years. Women there may have a higher awareness of cervical cancer and HPV compared with other lower resource areas. This also indicate that even with the increased awareness, our participants still demonstrated a lack of trust in self-collection, this again emphasises the importance of addressing the issue of trust, as it may hinder successful implementation of self-collection. Our small sample size was also a limitation. This is mainly because the FTA cartridge is a novel device and is new to China. Our study is one of the first to introduce this new collection device to the clinicians and patients in rural China. With good acceptability results of the FTA card, we plan on incorporating this collection device in future larger studies to confirm our findings. Another limitation of our study was that the self-collection was completed in a clinic setting. Since self-collection can potentially and perhaps ideally be performed at home, future studies should assess women's attitude towards taking the test at home. Our study had a high participation rate because the women who consented to the study were able to complete the collection and return it to the research staff in one visit to the clinic. With home collection, participation and reply rate may differ and should be assessed in future studies.

Despite the limitations of our study, it has several important clinical and public health implications. Our study demonstrates that self-collection was an acceptable method for population-based screening; however, our results also suggest that the issue of trust in self-collection must be addressed before self-collection can be successfully implemented. Public advertisement and patient education about the validity of the self-collection method should be the next step. Possible sites of advertisement are gynaecology clinics and primary care clinics, local healthcare facilities or free cervical cancer screening sites. Since self-collection can potentially be offered as an alternative to clinician collection, especially to reach women who do not attend regular screening, TV advertisements or radio broadcasts may reach broader population. Through education, we may be able to increase the women's confidence to collect their own specimen. Using data from concordance studies on self-collection versus clinician collection, we can prove to the women that self-collection is a suitable alternative to clinician collection for HPV DNA screening. The FTA elute card can aid in this education effort. The FTA card contains an indicating dye, which changes the colour of the filter paper once DNA is detected.9 This provides instant verification of sample capture that is easily visible to the women, providing direct feedback, and thereby may improve their confidence in their own ability to collect the specimen. With easier sample transport method such as the FTA cards and more patient education, self-collection holds great potential to be incorporated in future cervical cancer screenings.

Key messages

  • Self-collection is a promising alternative to clinician collection of cervical specimens for HPV testing in low- and middle-income countries.

  • Education programmes about the validity of self-collection that are designed for the general population may be needed prior to implementation.

  • FTA cartridge, which provides many advantages over liquid-based transport media, is positively accepted by the participants and should be considered for large-scale HPV screening programmes.

References

Supplementary materials

  • Supplementary Data

    This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

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  • Supplementary Data

    This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

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Footnotes

  • Funding This study was supported by the Cancer Institute/Hospital, Chinese Academy of Medical Sciences Department of Epidemiology, the Johns Hopkins University Departments of Epidemiology and Molecular Microbiology and Immunology, and the Chinese National Cancer Screening Project for Cervical Cancer and Breast Cancer Among Rural Women. The FTA cards used in this study were donated by GE healthcare. PEC was previously supported by the Intramural Research Program of the NIH/NCI.

  • Competing interests None.

  • Patient consent Obtained.

  • Ethics approval Ethics approval was provided by the Ethics Committee of Cancer Institute and Hospital, Chinese Academy of Medical Sciences.

  • Provenance and peer review Not commissioned; externally peer reviewed.