Reasons for non-attendance to cervical cancer screening and acceptability of HPV self-sampling among Bruneian women: A cross-sectional study

Liling Chaw; Shirley H F Lee; Nurul Iffah Hazwani Ja’afar; Edwin Lim; Roslin Sharbawi

doi:10.1371/journal.pone.0262213

. 2022 Mar 14;17(3):e0262213. doi: 10.1371/journal.pone.0262213

Reasons for non-attendance to cervical cancer screening and acceptability of HPV self-sampling among Bruneian women: A cross-sectional study

Liling Chaw ^1,^*, Shirley H F Lee ¹, Nurul Iffah Hazwani Ja’afar ¹, Edwin Lim ², Roslin Sharbawi ³

Editor: Oathokwa Nkomazana⁴

PMCID: PMC8920207 PMID: 35287163

Abstract

Objective

Uptake for cervical cancer screening remains well below the 80% target as recommended by Brunei’s National Cervical Cancer Prevention and Control plan. We conducted a pilot study to determine the reasons for non-attendance and explore their acceptance of human papillomavirus (HPV) self-sampling as an alternative to the Pap test.

Methods

A cross-sectional study was conducted at a primary healthcare center in Brunei, from January to December 2019. We recruited screening non-attendees, defined as women who were eligible for Pap test but who either never, or did not have one within the recommended screening interval of 3 years. This recruitment was done conveniently among women attending outpatient care and/or child health services at the primary healthcare center. Participants were first asked to complete a self-administered paper-based questionnaire on their reasons for screening non-attendance, and then invited for HPV self-sampling. Among those who agreed to participate in HPV self-sampling, they were asked to complete a second questionnaire on the self-sampling procedure and their samples were tested for high-risk HPV (hr-HPV). Results were analyzed using descriptive and inferential statistics.

Result

We enrolled 174 screening non-attendees, out of which 97 (55.7%) also participated in HPV self-sampling. The main reasons for not attending Pap test screening were fear of bad results (16.1%, n = 28); embarrassment (14.9%, n = 26) and lack of time due to home commitments (10.3%, n = 18). When compared to those who agreed to participate in HPV self-sampling, those who declined were significantly older (p = 0.002) and less likely to agree that they are susceptible to cervical cancer (p = 0.023). They preferred to receive Pap test-related information from healthcare workers (59.0%, n = 155), social messaging platforms (28.7%, n = 51) and social media (26.4%, n = 47). HPV self-sampling kits were positively received among the 97 participants, where > 90% agreed on its ease and convenience. Nine (9.3%) tested positive for hr-HPV, out of which eight were non-16/18 HPV genotypes.

Conclusion

Our findings suggest that promoting awareness on cervical cancer, clarifying any misconceptions of Pap test results, and highlighting that the disease is preventable and that early detection through screening can facilitate successful treatment would help increase screening uptake among Bruneian non-attendees. Response to HPV self-sampling was highly positive, suggesting the possibility of implementing this strategy in the local setting. Our high detection of non-16/18 HPV genotypes suggest high prevalence of other hr-HPV genotypes in Brunei. Larger studies should be conducted to further validate our findings.

Introduction

Cervical cancer is highly preventable but still remains one of the most common cancers among women worldwide. Globally, an estimated 604,000 women were diagnosed with cervical cancer, and 342,000 women died from the disease in 2020 [1]. Cervical cancer screening has drastically reduced the incidence of invasive cervical cancer in countries that have implemented such screening programs [2], which traditionally involves the use of the Papanicolaou (Pap) test.

Brunei Darussalam (population 459,500) is a small Southeast Asian country with a predominant Muslim population and a crude birth rate of 15.3 per 1,000 population [3]. Within this region, it has one of the highest age-standardized incidence rate (ASR) for cervical cancer: 20.6 per 100,000 women-years in Brunei when compared to 10.5 and 7.7 per 100,000 women-years in Malaysia and Singapore, respectively [4]. Brunei has initiated an organized cervical screening program since 2009, where married or ever married Bruneian women between 20 and 65 years old were invited to attend cervical cancer screening through periodic mail invitations. Pap test is the only screening test used in the country, and currently, liquid-based cytology is being used since 2012. Women with any positive cytology result, defined as with atypical squamous cells of undetermined significance (ASC-US) or worse, are followed up with colposcopy-guided cervical biopsy to diagnose cervical intra-epithelial neoplasia (CIN). The latter refers to premalignant lesions that are mainly caused by infection with certain types of human papillomavirus (HPV) [5], and can be categorized into any one of three stages (CIN1, CIN2, or CIN3) depending on the degree of dysplasia. If untreated, either CIN2 or CIN3 (collectively referred to as CIN2+) can progress to cervical cancer.

Despite this screening service being offered free of charge, the national screening coverage rate remains low at 44% in 2018 (unpublished data). Reasons for screening non-attendance can vary across settings [6, 7], but they can be broadly categorized into two groups: practical and organizational barriers (such as forgot to schedule an appointment, work and childcare commitments) [6], and emotional barriers (such as feeling healthy, lack of time, discomfort associated with gynecologic examination embarrassment, fear of smear test, previous negative experiences and dissatisfaction with their general practitioner) [6, 8–10]. As women who do not attend screening are at increased risk of developing cervical cancer [6], it is thus important to first understand why women chose not to attend screening in the local context.

HPV DNA detection has been recommended by the World Health Organization as the primary screening test for cervical cancer as specific high-risk HPV subtypes (hr-HPV) are known to be a causative agent [1]. In particular, the use of HPV self-sampling kits was suggested to increase screening uptake particularly among screening non-attendees [11, 12], due to its ease of access (where kits could be mailed to women’s homes) and also flexibility for women to perform the test by themselves. Previous studies have shown HPV self-sampling to be highly acceptable among screening non-attendees [13, 14]. In addition, HPV self-sampling results exhibit similar sensitivity and specificity compared to those from samples taken by trained professionals [15]. Repeated HPV self-sampling and testing were shown to increase screening uptake [11, 12, 16], and also resulted in at least two-fold higher detection rate of CIN2+ when compared to the Pap test [17, 18]. In the United Kingdom and Australia, early detection through an organized screening program using HPV testing as the primary screening test was shown to reduce cervical cancer morbidity and mortality [19, 20].

With Brunei’s relatively high incidence of cervical cancer and low screening uptake, we conducted a pilot study to explore the reasons behind non-attendance and to assess the acceptability of HPV self-sampling as a possible alternative to the Pap test among non-attendees (specifically women who are currently not accessing or attending screening). Study findings could be used to strategize ways to improve screening uptake and provide preliminary evidence towards implementing HPV testing as the primary screening test for cervical cancer in Brunei.

Methods

Study design and data collection

A cross-sectional survey was conducted at the Jubli Perak Sengkurong Health Center (JPSHC), from January to December 2019. JPSHC is a government-funded primary healthcare center located at Brunei-Muara District, where the majority (69.3%) of the country’s population resides. This center provides primary health care services to Mukim Sengkurong, a sub-district with about 32,000 people from various socioeconomic backgrounds.

Eligible women attending either the outpatient or child health clinic at JPHSC were conveniently recruited by triage nurses. We defined screening non-attendees as married or ever married women between 20 and 65 years old and have never undergone cervical cancer screening, or did not have one within the recommended screening interval of 3 years. We excluded women who could not comprehend Brunei-Malay or English language, were pregnant, have had total hysterectomy, or with a history of malignancies.

We implemented a two-stage recruitment procedure. In the first stage, participants were first recruited to complete a self-administered questionnaire on the reasons for screening non-attendance (Q1) onsite. Q1 consists of 19 questions on the participant’s socio-demographics, reasons for not getting Pap test, attitude and knowledge on cervical cancer, and lastly, preferred sources to acquire information about Pap test. From a prepared list of 16 possible reasons for not attending the screening program, participants were also asked to select one “Major” reason (defined as the main reason) and one or more “Minor” reason (defined as other reasons for not attending the screening program). Responses for questions on their attitude and knowledge on cervical cancer were recorded using a five-point Likert scale, ranging from “Strongly Agree” to “Strongly Disagree”.

In the second stage, all participants were given an envelope containing information on HPV self-sampling and an instruction leaflet on the procedure, after completing Q1. Within the following two weeks, they were contacted via telephone by a trained nurse, and those who gave verbal consent were given an appointment at JPSHC. On the day, the nurse first explained the procedure using an instructional video and answered any questions. Participants were then given a self-sampling kit and asked to perform the procedure in the clinic. After completion, they were asked to complete the second self-administered questionnaire (Q2) on their acceptability of the self-sampling procedure. Q2 consists of 12 five-point Likert scale questions (ranging from “Strongly Agree” to “Strongly Disagree”) on their experiences and opinions of the self-sampling kit.

Two separate written consents were requested from participants: one for completing Q1 and another for performing self-sampling and completing Q2.

Questionnaires used

The two questionnaires used (Q1 and Q2) were bilingual self-administered paper-based questionnaires in the two languages commonly used in Brunei (namely, Brunei-Malay and English language). Both questionnaires were adapted from similar studies [21, 22]. They were first translated to Brunei-Malay language by native speakers, and then back-translated to check for inconsistencies in comprehension. Both questionnaires were also pre-tested on six eligible women to assess if the questions could be easily understood. Responses from pre-testing were not included in the analysis.

Self-sample handling and laboratory testing

Swabs collected from the self-sampling kits were sent to an overseas laboratory (at BNH hospital, Thailand) for hr-HPV testing. The self-sampling device used was the Evalyn® brush from Rovers Medical Devices. Upon receipt at the testing laboratory, the dry Evalyn® brush was suspended in SurePath medium from which a sample was obtained for the identification of the presence of hr-HPV using the cobas HPV test (Roche, USA). Cobas HPV tests are automated qualitative in vitro tests for the detection of HPV DNA in patient specimens. The tests utilize amplification of target DNA by polymerase chain reaction (PCR) and nucleic acid hybridization for the detection of 14 hr-HPV types (namely genotypes 16, 18, and 12 pooled hr-HPV genotypes 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 66 and 68) in a single analysis. Results obtained from this test can be categorized into four groups: Negative, HPV-16 positive, HPV-18 positive, and positive for non-16/18 HPV genotypes.

Clinical management of hr-HPV positive participants

We adopted the cytology triage strategy for HPV self-sampling participants [23]. Participants with hr-HPV positive results were invited for an immediate clinic-based cytology triage test. Those found to have negative cytology results were invited for a repeat cytology triage test after six months. Those with second negative results were returned to routine cervical screening recall. Participants with any positive cytology result (defined as with ASC-US or worse) were referred for colposcopic examination.

Statistical analysis

Descriptive statistics was conducted to characterize the socio-demographic characteristics of the study population, their reasons for not attending screening, their attitudes and preference for information access on such screening, as well as responses from Q2. Where appropriate, Mann-Whitney and/or Fisher’s exact tests were used to assess significant differences in sociodemographic characteristics, reasons for not attending screening, and attitudes between women who agreed and women declined to join HPV self-sampling. Count responses for questions with the five-point Likert scale were categorized into three categories (agree, neutral, and disagree), and those with missing values were classified as neutral. Statistical analysis was conducted using R ver. 3.6 [24]. Ethics approval was obtained from the Medical and Health Research and Ethics Committee (MHREC), Ministry of Health, Brunei Darussalam [Reference no. MHREC/MOH/2018/9(2)].

Results

A total of 174 eligible women were enrolled in this study from January to December 2019, out of which 97 (55.7%) also participated in HPV self-sampling (Fig 1). Their median age was 45 years, ranging between 23 and 65 years (Table 1). The participants were mainly of Malay ethnicity (92.5%, n = 161), married (90.2%, n = 157), and had ≥ 3 births (60.3%, n = 105). About half of the participants had their last Pap test performed between 4 and 10 years ago (52.3%, n = 91), and have never received the HPV vaccine (54.6%, n = 95). There were significant differences between those who agreed and declined to participate in HPV self-sampling: those who declined were significantly older (p = 0.002) and more likely to have their last Pap test performed > 10 years ago (p = 0.031).

Table 1. Sociodemographic characteristics of the study population, including comparison between groups that agreed and declined to join HPV self-sampling.

Characteristics		Total study population (n = 174)	Joined self-sampling (n = 97)	Declined self-sampling (n = 77)	p-value
Characteristics		n (%)	n (%)	n (%)	p-value
Median age in years (IQR)		45.0 (15.25)	41.0 (17)	49.0 (14.5)	0.002*
Age group (in years)	20–24	3 (1.7)	3 (100)	0 (0.0)	0.018*
	25–29	20 (11.5)	15 (75.0)	5 (25.0)
	30–34	14 (8.1)	10 (71.4)	4 (28.6)
	35–39	28 (16.1)	18 (64.3)	10 (35.7)
	40–44	18 (10.3)	11 (61.1)	7 (38.9)
	45–49	27 (15.5)	12 (44.4)	15 (55.5)
	50–54	35 (20.1)	15 (42.9)	20 (57.1)
	55–59	14 (8.1)	10 (71.4)	4 (28.6)
	> 60	13 (7.5)	3 (23.1)	10 (76.9)
	Missing	2 (1.1)	0 (0.0)	2 (100)
Race	Malay	161 (92.5)	90 (55.9)	71 (44.1)	0.752
	Chinese	6 (3.5)	4 (66.7)	2 (33.3)
	Other	7 (4.0)	3 (42.9)	4 (57.1)
Education level	Primary school	16 (9.2)	10 (62.5)	6 (37.5)	0.396
	Secondary school	96 (55.2)	49 (51.0)	47 (49.0)
	College / University	57 (32.7)	35 (61.4)	22 (38.6)
	Missing	5 (2.9)	3 (60.0)	2 (40.0)
Marital status	Married	157 (90.2)	91 (58.0)	66 (42.0)	0.15
	Divorced	8 (4.6)	2 (25.0)	6 (75.0)
	Widowed	9 (5.2)	4 (44.4)	5 (55.6)
Occupation	Housewife	64 (36.8)	39 (60.9)	25 (39.1)	0.087
	Government employee	67 (38.5)	41 (61.2)	26 (38.8)
	Private employee	31 (17.8)	13 (41.9)	18 (58.1)
	Retired	9 (5.2)	3 (33.3)	6 (66.7)
	Unemployed	1 (0.6)	1 (100)	0 (0.0)
	Other	2 (1.1)	0 (0.0)	2 (100)
Monthly household income	< $500	27 (15.5)	15 (55.6)	12 (44.4)	0.498
	$500 < $999	27 (15.5)	12 (44.4)	15 (55.6)
	$1000-$1999	40 (23.0)	22 (55.0)	18 (45.0)
	$2000-$2999	19 (10.9)	14 (73.7)	5 (26.3)
	$3000-$5000	24 (13.8)	15 (62.5)	9 (37.5)
	>$5000	3 (1.7)	2 (66.7)	1 (33.3)
	Missing	34 (19.5)	17 (50.0)	17 (50.0)
Number of births	0	27 (15.5)	17 (63.0)	10 (37.0)	0.103
	1	19 (10.9)	14 (73.7)	5 (26.3)
	2	22 (12.1)	14 (66.7)	7 (33.3)
	3 or more	105 (60.3)	51 (48.6)	54 (51.4)
	Missing	2 (1.2)	1 (50.0)	1 (50.0)
Last Pap test done	Never	41 (23.6)	29 (70.7)	12 (29.3)	0.031*
	4–10 years	91 (52.3)	48 (52.7)	43 (47.3)
	> 10 years	36 (20.7)	15 (41.7)	21 (58.3)
	Missing	6 (3.4)	5 (83.3)	1 (16.7)
HPV vaccination status	Unvaccinated	95 (54.6)	50 (52.6)	45 (47.4)	0.483
	Fully vaccinated	27 (15.5)	16 (59.3)	11 (40.7)
	Partly vaccinated	41 (23.6)	26 (63.4)	15 (36.6)
	Missing	11 (6.3)	5 (45.5)	6 (54.5)

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IQR = Interquartile range.

Fig 2 and S1 Table show the responses for the major and minor reasons for not attending cervical cancer screening. The top three major reasons reported were that they were “afraid of getting a bad result” (16.1%, n = 28), “feeling embarrassed being examined by a doctor or nurse” (14.9%, n = 26), and “I can’t find the time as I’m too busy at home” (10.3%, n = 18). The top three minor reasons were “feeling embarrassed being examined by a doctor or nurse” (20.7%, n = 36), “I can’t find time as I’m too busy at work” (20.7%, n = 36), and “afraid of getting a bad result” (20.1%, n = 35).

When comparing top 10 major reasons for not attending screening between those who agreed and declined HPV self-sampling (Table 2), those whose major reason was “feeling embarrassed being examined by a doctor or nurse” were significantly more likely to join self-sampling (p = 0.020). Also, those whose major reason was “afraid of getting a bad result” were significantly more likely to decline self-sampling (p = 0.034). Among those who were employed (n = 98), about a quarter (23.5%, n = 23) reported work-related reasons as their major reason for not attending screening (“I can’t find the time as I’m too busy at work” and “Difficult to get permission from employer”).

Table 2. The top ten major reasons of not attending cervical cancer screening at JPSHC, Brunei (Jan–Dec 2019), with comparison between those who agreed and declined HPV self-sampling.

Responses from 146 participants (83.9% of the total study population) were included.

No.	Top ten major reasons of screening non-attendance	Total	Joined HPV self-sampling	Declined HPV self-sampling	p-value
No.	Top ten major reasons of screening non-attendance	n (%)	n (%)	n (%)	p-value
1	I feel embarrassed being examined by a doctor or nurse	26 (14.9)	20 (76.9)	6 (23.1)	0.020*
2	I am scared of pain because of previous bad experience(s)	16 (9.2)	8 (50.0)	8 (50.0)	0.825
3	I am scared of getting a bad result	28 (16.1)	10 (35.7)	18 (64.3)	0.034*
4	I can’t find the time as I’m too busy at home	18 (10.3)	12 (66.7)	6 (33.3)	0.463
5	I can’t find the time as I’m too busy at work	16 (9.2)	10 (62.5)	6 (37.5)	0.759
6	Difficult to get permission from employer	8 (4.6)	5 (62.5)	3 (37.5)	1
7	I have never heard of a Pap Test	7 (4.0)	4 (57.1)	3 (42.9)	1
8	I have forgotten about it	6 (3.4)	5 (83.3)	1 (16.7)	0.229
9	I did not receive any invitation	6 (3.4)	5 (83.3)	1 (16.7)	0.229
10	Others	15 (8.6)	7 (46.7)	8 (53.3)	0.492

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While the responses vary when asked about their health and susceptibility to disease, most agreed on the benefits of undergoing Pap test (92.0%, n = 160), and that cervical cancer is a severe and potentially lethal disease (82.8%, n = 144; Table 3 and S2 Table). Those who agreed that they are more susceptible to develop cervical cancer were significantly more likely to join HPV self-sampling (p = 0.023).

Table 3. Attitudes towards cervical cancer screening among non-attendees at JPSHC, Brunei (Jan–Dec 2019), between those who agreed and declined HPV self-sampling.

No.	Attitude questions		Total study population (n = 174)	Joined HPV self-sampling (n = 97)	Declined HPV self-sampling (n = 77)	p-value
No.	Attitude questions		n (%)	n (%)	n (%)	p-value
1	I believe I am healthy and free of any diseases	Agree	62 (35.6)	34 (54.8)	28 (45.2)	0.984
1	I believe I am healthy and free of any diseases	Neutral/ Disagree	112 (64.3)	63 (56.3)	49 (43.7)	0.984
2	Having Pap test taken is beneficial for my health	Agree	160 (92.0)	91 (56.9)	69 (43.1)	0.464
2	Having Pap test taken is beneficial for my health	Neutral/ Disagree	14 (8.0)	6 (42.9)	8 (57.1)	0.464
3	Like any women, I am susceptible to develop cervical cancer	Agree	110 (63.2)	69 (62.7)	41 (37.3)	0.023*
3	Like any women, I am susceptible to develop cervical cancer	Neutral/ Disagree	64 (36.8)	28 (43.8)	36 (56.2)	0.023*
4	Cervical cancer can be severe and may lead to death	Agree	144 (82.8)	79 (54.9)	65 (45.1)	0.754
4	Cervical cancer can be severe and may lead to death	Neutral/ Disagree	30 (17.2)	18 (60.0)	12 (40.0)	0.754

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Most participants would like to obtain more information about cervical cancer screening (85.6%, n = 149). The top preferred information sources were healthcare workers (59.8%, n = 104), social messaging platforms (28.7%, n = 50) and social media (26.4%, n = 46; S1 Fig).

Among those who participated in self-sampling (55.7%, n = 97), their responses on Q2 (Table 4) were mostly positive. A majority agreed that the instructions were clear (94.8%, n = 92), that it was easy to perform the swab (93.8%, n = 91), and that it was more convenient than the Pap test (91.7%, n = 89). They also reported their confidence in correctly getting the sample (92.8%, n = 90), would prefer to use this method next time (94.8%, n = 92), and would recommend this method to other women (93.8%, n = 91). Notably, 54.6% (n = 53) still prefer a proper Pap test for their subsequent check-up.

Table 4. Acceptability of HPV self-sampling among non-attendees who participated in HPV self-sampling at JPSHC, Brunei (Jan–Dec 2019).

Responses from all Q2 respondents (n = 97) were included.

No.	Self-sampling Questions	Agree	Neutral	Disagree
No.	Self-sampling Questions	n (%)	n (%)	n (%)
1	I thought the instructions were clear	92 (94.8)	0 (0.0)	5 (5.2)
2	It was easy to do the swab	91 (93.8)	1 (1.0)	5 (5.2)
3	Taking the sample with the swab was painful	12 (12.4)	8 (8.2)	77 (79.4)
4	Taking the sample was uncomfortable to do	11 (11.4)	4 (4.1)	82 (84.5)
5	I felt embarrassed doing the self-sampling	9 (9.3)	1 (1.0)	87 (89.7)
6	It was convenient to do without having to undergo a Pap Test	89 (91.7)	3 (3.1)	5 (5.2)
7	I am confident I did it correctly	90 (92.8)	4 (4.1)	3 (3.1)
8	I want to use this method next time	92 (94.8)	2 (2.1)	3 (3.1)
9	I prefer to do this at home	64 (66.0)	15 (15.5)	18 (18.5)
10	I would recommend this method to other women	91 (93.8)	3 (3.1)	3 (3.1)
11	I trust that the result of this self-sampling will be accurate	74 (76.3)	19 (19.6)	4 (4.1)
12	I would like to attend for a proper Pap test in clinic next time	53 (54.6)	23 (23.7)	21 (21.7)

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Among the 97 samples taken, nine (9.3%) tested positive for hr-HPV: one was positive for HPV 16 and eight were positive for non-HPV 16/18 HPV genotype. The HPV 16 positive case was found to have high-grade ASC-US (ASCUS-H) on the initial follow up smear, but found negative after subsequent follow up cervical biopsy. Among the other 8 non-HPV 16/18 HPV genotype positive cases: 2 had negative follow up smears, 4 were reported to have ASC-US on their initial follow up smears, but had subsequent negative follow up smears, 1 was reported to have low-grade squamous intraepithelial lesion (LSIL) on her initial follow up smear, and had a subsequent negative follow up smear, and 1 was found to have CIN 3 with glandular involvement on the follow up smear and cervical biopsy, and has received treatment with a cone biopsy where excision of CIN 3 was confirmed. No significant differences were observed when comparing the sociodemographic characteristics between those who tested hr-HPV positive and those who tested hr-HPV negative (S3 Table).

Discussion

Our study findings highlight three important points to consider for improving cervical cancer screening uptake and detection. First, our findings suggest that it is necessary to provide accurate information among Bruneian women on cervical cancer, the importance of screening and addressing any misconceptions about the Pap test. Important facts to relay include the slow development from pre-cancerous changes to cervical cancer, that pre-cancerous changes are highly treatable, and that screening will help in early detection and thus facilitate successful treatment.

In our study, emotional barriers (fear of unfavorable test results and embarrassment) were the most common major reasons of screening non-attendance. Also, about two-thirds of our participants cited “I am scared of getting a bad result” as their main barrier also declined to take part in HPV self-sampling, possibly due to relating abnormal Pap test results to cervical cancer diagnoses [25]. Although such barriers may play a large role at the onset of screening program, its role diminishes over time with increasing education on the benefits of screening [26]. Educational interventions could also benefit the small group of women who cited menopause, cessation of child-bearing and having had HPV vaccination as reasons for not attending screening (Fig 2 and S1 Table). We also observed that those who agree that they are susceptible to cervical cancer were significantly more likely to participate in HPV self-sampling. This suggests that perceived susceptibility could be an important factor for self-sampling participation, whereby those who do not perceive themselves as susceptible were less likely to engage in preventative behaviors [27–29]. Perceived susceptibility can be increased through education to improve their beliefs on the importance of screening [30]. We suggest that such information could be more effectively disseminated as simple health messages endorsed by Brunei’s Ministry of Health via website and social media platforms.

Second, we observed high acceptability of HPV self-sampling among our participants. Meta-analyses have indicated strong acceptance of and preference for self-sampling over clinician sampling [31], mainly due to logistical reasons [32]. More than half of our participants who joined HPV self-sampling cited embarrassment or lack of time due to home and/or work commitments as their major reason of not attending Pap test screening. This suggest that providing flexibility to accommodate women’s screening method preference [33], such as the option of self-sampling [34], could improve screening uptake.

Thirdly, most of the detected hr-HPV genotypes in our study were non-16/18, with only one out of nine participants tested positive for HPV 16. Although our sample size is small, this result suggests that it may not be accurate to assume HPV 16 or 18 as common hr-HPV genotypes in Brunei, even though this is true in the global context [35]. Other studies have detected a significant percentage of non-16/18 hr-HPV genotypes, suggesting the presence of region-specific heterogeneity in the HPV genotype distribution [35–39]. Also, variation in HPV distribution among different ethnic groups has been reported in an American study [40]. Our finding has potential implication on Brunei’s national school-based HPV vaccination program [41] which currently provides vaccines which do not confer protection against non-16/18 genotypes. Larger population-based studies to understand the distribution of HPV genotypes among Bruneian women will be crucial to determine the efficacy or impact of the current vaccines.

One notable point for the local context relates to the presence of cultural barriers. Being a predominantly Islamic society, religious and cultural modesty could be a contributing factor for embarrassment among Muslim women [42]. Also, having premarital sex is a taboo in Brunei and is generally not openly discussed [43]. This could prevent any unmarried but sexually active women from participating in the screening program. It should be emphasized that only married or ever married females were included in this study; included because it is part of the eligibility criteria for the national cervical cancer screening program in Brunei.

A major limitation for this study is that non-attendees from only one health center were recruited, thus our findings are not representative of the adult female population in Brunei. Secondly, our findings should also be interpreted with caution due to the small sample size and the non-probability sampling approach used. This study was initially conceived as a pilot study due to resource and logistics limitations. There were two reasons for choosing JPSHC as our study site: It is the third largest primary government healthcare center in the country, and that it serves a sub-district with a sizable percentage of residents in the middle- to low-income groups. However, even at this pilot stage, our study findings could encourage stakeholders to conduct similar and larger studies, using random sampling approach. Lastly, as this study relied on the self-reported history of previous Pap test attendance, we might have missed recruiting those who may have forgotten their last Pap test date.

In conclusion, our findings indicate the need to further promote knowledge on cervical cancer, the benefits of screening and clarifying any misconceptions of Pap test results. Reasons of cervical cancer screening non-attendance were mainly related to emotional and logistical factors. As we found high acceptance towards HPV self-sampling, this could be adopted as an alternative for women who refrain from Pap test. Our high detection of non-16/18 HPV genotypes suggest high prevalence of other hr-HPV genotypes in Brunei. Future larger studies involving more Bruneian women should be done to verify our results. Follow-up studies should also be conducted to consider HPV testing as the suitable method for cervical cancer screening.

Supporting information

S1 Table. Responses on their major and minor reasons for not attending cervical cancer screening among non-attendees at JPSHC, Brunei (Jan–Dec 2019).

(DOCX)

Click here for additional data file.^{(15.6KB, docx)}

S2 Table. Attitudes towards cervical cancer screening among non-attendees at JPSHC, Brunei (Jan–Dec 2019).

Responses from the total study population (n = 174) were included.

(DOCX)

Click here for additional data file.^{(13.9KB, docx)}

S3 Table. Socio demographic characteristics and comparison between screening non-attendees who tested positive and negative for hr-HPV at JPSHC, Brunei (Jan–Dec 2019).

(DOCX)

Click here for additional data file.^{(22KB, docx)}

S1 Fig. Preferred sources of information about cervical cancer among non-attendees at JPSHC, Brunei (Jan–Dec 2019).

The x-axis indicates the percentage, and the number next to each bar indicates the number of responses. Multiple responses were allowed and responses from the total study population (n = 174) were included.

(DOCX)

Click here for additional data file.^{(15.5KB, docx)}

S1 Questionnaire. Reasons why women do not participate in the national cervical cancer screening program.

(DOCX)

Click here for additional data file.^{(97.6KB, docx)}

S2 Questionnaire. Acceptability of self sampling for HPV testing among non-attendees of cervical screening program in Brunei Darussalam.

(DOCX)

Click here for additional data file.^{(78.3KB, docx)}

S1 Dataset. Minimal dataset.

(XLSX)

Click here for additional data file.^{(41.3KB, xlsx)}

Acknowledgments

The authors would like to thank the JPSHC staff who have assisted in participant recruitment and questionnaire distribution.

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

Edwin Lim has acquired funding from Ministry of Health, Brunei Darussalam. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS One. doi: 10.1371/journal.pone.0262213.r001

Decision Letter 0

Oathokwa Nkomazana

13 Aug 2021

PONE-D-21-02442

Reasons for non-attendance to cervical cancer screening and acceptability of HPV self-sampling among Bruneian women: A cross-sectional study.

PLOS ONE

Dear Dr. Chaw,

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Reviewer #1: Partly

Reviewer #2: Partly

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Reviewer #1: Yes

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Reviewer #1: The authors have undertaken a questionnaire based small survey in Brunei women about attitude towards cervical screening. Background is that Brunei has a high incidence of cervical cancer and a low screening coverage of 44%.

The results are worth informing the world about. But the manuscript is fair too long for what it contains. It should be shortened considerably:

1. delete most of page 6

2. Delete figure 2

3. Merge Tables 3 and 4

4. Delete figure 3

5. Shorten considerable the three points in the Discussion – really to about two lines each

I miss Discussion about:

1. why is the mean age so high 45 years?

2. Screening coverage is really not so low in participants: 52.3% had been screening within last 4-10 years

3. How does the reported screening coverage in the group correspond to the national coverage of 44%?

4. By for the majority of women answer agree to “having a pap test taken is beneficial for my health” - when why do the authors recommend more education and awareness as their top priority? - women actually seem to be fairly good informed.

5. More comments should be given on potential practical and cultural barriers.

Overall: relevant topic, but not acceptable for publication in its present form. Should be reduced to a max. Of haft the number of words to be of interest for a broader audience.

Reviewer #2: This is an important topic. Please consider how you can make these results of 174 women generalizable to the entire Brunei population. How do you exclude sampling bias? Why did you do this in two parts?

**********

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Reviewer #2: Yes: Diane M Harper

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PLoS One. 2022 Mar 14;17(3):e0262213. doi: 10.1371/journal.pone.0262213.r002

Author response to Decision Letter 0

24 Aug 2021

Point-to-point responses:

From the Journal Author’s Response

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming.

The manuscript has been revised as requested, including the use of American English.

Participants gave written consent for both parts of the study. We have added this point in the Methods section (3rd paragraph under Study design and data collection sub-section):

“Participants who gave written consent to the first part of the study were asked to complete the first questionnaire (Q1) onsite. They were then given an envelope containing information on the second part and an instruction leaflet on the HPV self-sampling procedure. Upon second contact about two weeks later, those who gave verbal consent were given an appointment to JPSHC. On the day, a trained nurse first explained the procedure using an instructional video and answered any questions. Participants who gave another written consent were then given a self-sampling kit and asked to perform the procedure in the clinic. After completion, they were asked to complete the second questionnaire (Q2).”

Both questionnaires used in this study are now attached as Supplementary Information (S4 & S5).

We have attached the minimal dataset as Supplementary Information (S6).

Comments from the reviewers Author’s Response

The results are worth informing the world about. But the manuscript is fair too long for what it contains. It should be shortened considerably:

1. delete most of page 6

2. Delete figure 2

3. Merge Tables 3 and 4

4. Delete figure 3

Thank you for your comments. We have edited the whole manuscript to correct any grammatical mistakes and also make our points shorter and more concise.

As suggested, we have also:

1. Shorten the data collection method in page 6.

2. Merged Tables 3 and 4, whereby the total count column was added into the original Table 4. The original Table 3 is now moved to the Supplementary Information (as Table S2), for readers who want to refer to the breakdown responses (agree, neutral & disagree).

3. Figure 3 was also moved to the Supplementary Information (as Figure S1), for readers who want to know the full breakdown of responses.

For Figure 2, we decided to keep Figure 2 because we think it is the best way to summarize both counts & percentages for both major and minor reasons (and showing the complete picture of our study results). Table S1 shows the same results in the Table version, but it is less intuitive as Figure 2. Also, Table 2 only show the results for the top 10 major reasons (meaning that it is not showing the complete picture, like Figure 2).

5. Shorten considerable the three points in the Discussion – really to about two lines each

I miss Discussion about:

1. why is the mean age so high 45 years?

2. Screening coverage is really not so low in participants: 52.3% had been screening within last 4-10 years

3. How does the reported screening coverage in the group correspond to the national coverage of 44%?

5. More comments should be given on potential practical and cultural barriers.

5.1. The median age of 45 years could be due to the specific population that we have targeted, that is, the screening non-attendees. As mentioned in the Methods section: “The inclusion criteria were married or ever married Bruneian women between 20 and 65 years old, who either never or did not have a Pap test within the last 4 years, and who can comprehend Brunei-Malay or English language”.

While it is possible this could be due the convenience sampling that were conducted in this study, we take note that previous studies from Finland (Virtanen A et al. Ref no.18 in manuscript) and El Salvador (Maza M, et al. Ref no.5 in manuscript), both focusing on screening non-attendees only, also have similar median ages. Although both studies include women between 30-60 years old, our study is still comparable with theirs as the median age of marriage in Brunei is about 26 years from 2014 to 2019 (based on country census data: http://www.deps.gov.bn/SitePages/Vital%20Statistics.aspx )

In the revised manuscript, we decided not to explicitly include this point. Instead, we have added a new paragraph on the potential cultural barriers (please see item 5.5 below) which elude to this point.

5.2. Thank you for your point here. In this study, we want to investigate reasons for both non-attendance to screening at all, as well as for not continuing with screening every 3 years, as recommended. This is why women who had undergone screening within the last 4-10 years were included in this study. To clarify this point and avoid confusion, we have replaced the word “coverage” to “uptake” in our study significance statement (Introduction section, last sentence): “Study findings could be used to strategize ways to improve screening uptake and provide preliminary evidence towards implementing HPV testing as the primary screening test for cervical cancer in Brunei.”

5.3. This point relates to the sampling strategy for this study. Briefly, our study findings could not be generalizable to the whole country population. Please see our response for Reviewer #2 below, who commented on the result generalizability.

5.4. We would like to clarify that we are pushing for promoting knowledge on cervical cancer, the benefits of screening and clarifying any misconceptions of Pap test results. This implies not only on promoting general awareness on the Pap test, but also on why is this important to be conducted periodically and to clarify any misconceptions of the Pap test results. To prevent any misunderstanding, the conclusion paragraph is revised as follows:

“In conclusion, our findings indicate the need to further promote knowledge on cervical cancer, the benefits of screening and clarifying any misconceptions of Pap test results. Reasons of cervical cancer screening non-attendance were mainly related to emotional and logistical factors. As we found high acceptance towards HPV self-sampling, this could be adopted as an alternative for women who refrain from Pap test. Our high detection of non-16/18 HPV genotypes suggest high prevalence of other hr-HPV genotypes in Brunei. Future larger studies involving more Bruneian women should be done to verify our results. Follow-up studies should also be conducted to consider HPV testing as the suitable method for cervical cancer screening.”

5.5. Thank you for your point here. We have added a new paragraph on the potential cultural barriers:

“One notable point for the local context relates to the presence of cultural barriers. Being a predominantly Islamic society, religious and cultural modesty could be a contributing factor for embarrassment among Muslim women [39]. Also, having premarital sex is a cultural taboo in Brunei and is generally not openly discussed [40]. This could prevent any unmarried but sexually active women from participating in the screening program. It should be emphasized that only married or ever married females were included in this study; included because it is part of the eligibility criteria for the national cervical cancer screening program in Brunei.”

Overall: relevant topic, but not acceptable for publication in its present form. Should be reduced to a max. Of haft the number of words to be of interest for a broader audience.

Thank you for your comment. We have edited the manuscript and have reduced the word count to 3049 words (manuscript, excluding references). We hope this revision would be clear and concise enough for the journal readers.

Thank you for your comments.

(a) and (b). It will be difficult to generalize the study results, as there was only one study site, sample size was low & sampling bias was done conveniently. We have emphasized this in the limitations:

“A major limitation for this study is that non-attendees from only one health center were recruited, thus our findings are not representative of the adult female population in Brunei. Secondly, our findings should also be interpreted with caution due to the small sample size and the non-probability sampling approach used. This study was initially conceived as a preliminary study due to resource and logistics limitations. There were two reasons for choosing JPSHC as our study site: It is the third largest primary government healthcare center in the country, and that it serves a sub-district with a sizable percentage of residents in the middle- to low-income groups. It is hoped that even at this preliminary stage, our study findings could encourage stakeholders to conduct similar and larger studies, using random sampling approach.”

(c) Thank you for pointing this out. This study was originally carried out as a two-part study (one on the reasons for non-attendance questionnaire & another on self-sampling). However, we understand that it is irrelevant to mention this, and have therefore removed it entirely from the manuscript: in abstract (first sentence in Methods), and in discussion (first sentence).

Attachment

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PLoS One. doi: 10.1371/journal.pone.0262213.r003

Decision Letter 1

Oathokwa Nkomazana

8 Nov 2021

PONE-D-21-02442R1Reasons for non-attendance to cervical cancer screening and acceptability of HPV self-sampling among Bruneian women: A cross-sectional study.PLOS ONE

Dear Dr. Chaw,

==============================Thank you for reporting on your important work.

Please attend to all the comments by third reviewer. It may be helpful to include, in the method section, "The context of the study". Under this section, briefly outline the national cervical cancer guideline. At what age is screening started? How often should screening be done? What is the screening method? And any other information that will help the reader situate the problem you are addressing through this study.

==============================

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PLOS ONE

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Reviewer #2: Yes

Reviewer #3: No

**********

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Reviewer #2: Yes

Reviewer #3: I Don't Know

**********

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Reviewer #2: Yes

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #2: Yes

Reviewer #3: Yes

**********

6. Review Comments to the Author

Reviewer #2: great work! Continue to probe why older women will not screen after you do an educational intervention that shows the average age of cx ca is about 40 years old without any symptoms.

Reviewer #3: General comments:

Piloting self-testing in various cultural and geographic settings is important, however, I do not believe this adds to the body of literature supporting HPV self-testing. The sample size is also relatively small to make any meaningful comments about HPV prevalence; the authors do cite the need for additional research. The scope of this work would be more appropriate for a regional journal.

Non-attendees needs a clear definition somewhere, as well as clarification as to why a Pap test > 4 years ago was included (is this the recommendation in Brunei?).

Throughout the paper, you contrast HPV self swabs to a Pap test. I think the comparison you are really making is between a self-swab and a provider-collected test (using a pelvic examination). Or do you think there is a patient held belief in the reliability of a Pap test? Do you think it would be appropriate to rather compare HPV testing to any cervical cancer screening? Do you think there was any role of the desire to have a pelvic examination, other contexts have shown that patients feel more secure when a doctor as examined them.

Specific comments:

Abstract:

Objective: specify <80% where? Explain non-attendance – do you mean non-attendance at recommended screening/screening intervals?

Methods: describe the health center – tertiary referral center? You mention 4 years – is this the interval for screening in Brunei? You don’t mention the second survey here. Statistical analysis is not sufficient.

Results: it is hard for a reader to understand how you enrolled “non-attendees”. Perhaps that can simply be clarified. Need to specify in line 46 how many women accepted HPV self-swab.

Discussion: In the results you state that “Fear of bad results, embarrassment and lack of time” are the main causes for non-attendance, I’m not sure your suggested intervention directly tackles those issues. Perhaps specific education/community awareness that cervical cancer is a preventable disease? Line 52 is non-specific and needs clarification.

Introduction: Generally not linear in its progression. First paragraph starts with effectiveness of screening and in particular screening with HPV testing. Second paragraph starts with more effective screening strategies for screening non-attendees. Third paragraph with specifies to Brunei. These are fine themes, but the authors lose focus as they add to these paragraphs. Also, I think there should be a more in-depth dive into screening non-attendance. What are patterns internationally and/or what are factors that cause non-attendance. Specific feedback:

Line 69 and 71: Screening non-attendees: what does this mean. How do you survey screening non-attendees? I assume there is a definition in methods, but some explanation is needed here.

Lines 73-74: need full definition for CIN2+, you have only spelled out CIN

Lines 74-79 seem to belong in the line of thinking of the first paragraph

Lines 89-91 seem out of place and belong in the second paragraph

Lines 95-97 make the statement about the importance/impact of this study more definitive.

Methods: The methods should be clear enough for someone else to repeat the study. It is not clear who was collecting the data, how issues of illiteracy were addressed (or was this an exclusion criteria). It is not stated where data was stored and analysis is not clear enough to be replicable.

Perhaps call this a pilot instead of “preliminary”

Line 115: not clear what “first part of the study is”

Line 117: how was second contact attempted? Why two weeks? I would suggest incorporating what was on the questionnaires with the first reference to the questionnaire, rather than having it as another sectioin

Line 131: could not can

Line 173: It is not clear if frequencies were used to present the questions that were rated on a likert scale for the classifications described. If so, how were these frequencies compared (I notice the p-value in the results below).

Results:

Line 195: drop “major” and “minor” qualifiers or define them.

Line 219: what does this mean they agreed on the “severity of cervical cancer”?

Line 234, would avoid the use of subjective qualifiers

Line 248, It is pretty remarkable that 8/9 women with HPV had abnormal pap smears. Also does this mean only 1 participant had CIN3? What about the rest?

Discussion:

First sentence can be eliminated.

Line 310 – this should be mentioned in the methods section in exclusion criteria of non-married women

Lines 272-274 – this hadn’t come up in the results, so I wouldn’t bring it into the discussion

Lines 319 – 321 – rephrase this, don’t use “hope” to convey this sentiment

Tables:

Table 1: percentages are confusing because you don’t know how many women are in each age group, so you don’t know if the percentage is of the total number of women or the number in the age group. I think the percentages would be more understandable if they were the percentage of women in the age group who joined/declined. What’s the difference between “never” and “no” for HPV vaccination?

Table 4, question 12 – do you think the wording of the question was leading to participants by putting “proper” before Pap test?

**********

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Reviewer #2: Yes: Diane M Harper

Reviewer #3: No

PLoS One. 2022 Mar 14;17(3):e0262213. doi: 10.1371/journal.pone.0262213.r004

Author response to Decision Letter 1

30 Nov 2021

Please see attached the point-by-point response for each comment.

Attachment

Submitted filename: JPSstudy_Rebuttal_Nov2021.docx

Click here for additional data file.^{(23.3KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0262213.r005

Decision Letter 2

Oathokwa Nkomazana

20 Dec 2021

Reasons for non-attendance to cervical cancer screening and acceptability of HPV self-sampling among Bruneian women: A cross-sectional study.

PONE-D-21-02442R2

Dear Dr. Chaw,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Please address two minor issues: 1. Line 77: indicate the unit and period of the incidence rate. Is the unit percentage or per thousand population? Is the period per year or what?

2.Line 85; first mention of Human Papilloma Virus shouldn't use acronym only.

3. Instead of calling your participants non-attendees, it may be better to use a descriptive phrase like: 'those currently not accessing screening'

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Oathokwa Nkomazana, MD MSC PhD

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0262213.r006

Acceptance letter

Oathokwa Nkomazana

5 Mar 2022

PONE-D-21-02442R2

Reasons for non-attendance to cervical cancer screening and acceptability of HPV self-sampling among Bruneian women: A cross-sectional study.

Dear Dr. Chaw:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

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on behalf of

Dr. Oathokwa Nkomazana

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PLOS ONE

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Table. Responses on their major and minor reasons for not attending cervical cancer screening among non-attendees at JPSHC, Brunei (Jan–Dec 2019).

(DOCX)

Click here for additional data file.^{(15.6KB, docx)}

S2 Table. Attitudes towards cervical cancer screening among non-attendees at JPSHC, Brunei (Jan–Dec 2019).

Responses from the total study population (n = 174) were included.

(DOCX)

Click here for additional data file.^{(13.9KB, docx)}

S3 Table. Socio demographic characteristics and comparison between screening non-attendees who tested positive and negative for hr-HPV at JPSHC, Brunei (Jan–Dec 2019).

(DOCX)

Click here for additional data file.^{(22KB, docx)}

S1 Fig. Preferred sources of information about cervical cancer among non-attendees at JPSHC, Brunei (Jan–Dec 2019).

(DOCX)

Click here for additional data file.^{(15.5KB, docx)}

S1 Questionnaire. Reasons why women do not participate in the national cervical cancer screening program.

(DOCX)

Click here for additional data file.^{(97.6KB, docx)}

S2 Questionnaire. Acceptability of self sampling for HPV testing among non-attendees of cervical screening program in Brunei Darussalam.

(DOCX)

Click here for additional data file.^{(78.3KB, docx)}

S1 Dataset. Minimal dataset.

(XLSX)

Click here for additional data file.^{(41.3KB, xlsx)}

Attachment

Submitted filename: Response to Reviewers.docx

Click here for additional data file.^{(23.9KB, docx)}

Attachment

Submitted filename: JPSstudy_Rebuttal_Nov2021.docx

Click here for additional data file.^{(23.3KB, docx)}

Data Availability Statement

All relevant data are within the paper and its Supporting Information files.

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Reasons for non-attendance to cervical cancer screening and acceptability of HPV self-sampling among Bruneian women: A cross-sectional study

Liling Chaw

Shirley H F Lee

Nurul Iffah Hazwani Ja’afar

Edwin Lim

Roslin Sharbawi

Roles

Abstract

Objective

Methods

Result

Conclusion

Introduction

Methods

Study design and data collection

Questionnaires used

Self-sample handling and laboratory testing

Clinical management of hr-HPV positive participants

Statistical analysis

Results

Fig 1. Flowchart of study participants at JPHSC, Brunei (Jan–Dec 2019).

Table 1. Sociodemographic characteristics of the study population, including comparison between groups that agreed and declined to join HPV self-sampling.

Fig 2. Responses on their major and minor reasons for not attending cervical cancer screening, among non-attendees at JPSHC (Jan–Dec 2019).

Table 2. The top ten major reasons of not attending cervical cancer screening at JPSHC, Brunei (Jan–Dec 2019), with comparison between those who agreed and declined HPV self-sampling.

Table 3. Attitudes towards cervical cancer screening among non-attendees at JPSHC, Brunei (Jan–Dec 2019), between those who agreed and declined HPV self-sampling.

Table 4. Acceptability of HPV self-sampling among non-attendees who participated in HPV self-sampling at JPSHC, Brunei (Jan–Dec 2019).

Discussion

Supporting information

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

Oathokwa Nkomazana

Roles

Author response to Decision Letter 0

Decision Letter 1

Oathokwa Nkomazana

Roles

Author response to Decision Letter 1

Decision Letter 2

Oathokwa Nkomazana

Roles

Acceptance letter

Oathokwa Nkomazana

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

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