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Attitudes Toward Pre-Exposure Prophylaxis Against HIV Infection Among Individuals Seeking Voluntary Counseling and Testing for HIV in Taiwan: A Cross-Sectional Questionnaire Survey
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Manuscript ID Article Type:
Date Submitted by the Author:
bmjopen-2016-015142 Research 12-Nov-2016
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Complete List of Authors:
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Lee, Yi-Chieh; Lotung Poh-Ai Hospital, Medical Lo-Hsu Foundation, Department of Internal Medicine Chang, Sui-Yuan; National Taiwan University College of Medicine, Department of Clinical Laboratory Sciences and Medical Biotechnology; National Taiwan University Hospital and National Taiwan University College of Medicine Lin, Kuan-Yin; National Taiwan University Hospital Jin-Shan Branch, Department of Internal Medicine Chang, Lan-Hsin; National Taiwan University Hospital and National Taiwan University College of Medicine, Department of Internal Medicine Liu, Wen-Chun; National Taiwan University Hospital and National Taiwan University College of Medicine, Department of Internal Medicine Wu, Cheng-Hsin; National Taiwan University Hospital and National Taiwan University College of Medicine, Department of Internal Medicine Sun, Hsin-Yun; National Taiwan University Hospital and National Taiwan University College of Medicine, Department of Internal Medicine Hung, Chien-Ching; National Taiwan University Hospital and National Taiwan University College of Medicine, Department of Internal Medicine; National Taiwan University College of Medicine Chang, Shan-Chwen; National Taiwan University Hospital and National Taiwan University College of Medicine, Department of Internal Medicine
Keywords:
Sexual health, Sociology
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Secondary Subject Heading:
HIV/AIDS
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Primary Subject Heading:
HIV prevention, men who have sex with men, tenofovir disproxil fumarate, emtricitabine, chemsex, sexually transmitted infection
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Attitudes Toward Pre-Exposure Prophylaxis Against HIV Infection Among Individuals Seeking Voluntary Counseling and Testing for HIV in Taiwan: A Cross-Sectional Questionnaire Survey
Yi-Chieh Lee1, Sui-Yuan Chang2,3, Kuan-Yin Lin4, Lan-Hsin Chang5, Wen-Chun Liu5, Cheng-Hsin Wu5, Hsin-Yun Sun5, Chien-Ching Hung5,6,7,8, Shan-Chwen Chang5
1
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Department of Internal Medicine, Lotung Poh-Ai Hospital, Medical Lo-Hsu
Foundation, I-Lan, Taiwan 2
Department of Clinical Laboratory Sciences and Medical Biotechnology, National
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Taiwan University College of Medicine, Taipei, Taiwan, 3
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Department of Laboratory Medicine, National Taiwan University Hospital and
National Taiwan University College of Medicine, Taipei, Taiwan 4
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Department of Internal Medicine, National Taiwan University Hospital Jin-Shan Branch, New
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Taipei City, Taiwan 5
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Department of Internal Medicine, National Taiwan University Hospital and National
Taiwan University College of Medicine, Taipei, Taiwan 6
Department of Parasitology, National Taiwan University College of Medicine, Taipei,
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Taiwan 7
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Department of Medical Research, China Medical University Hospital, Taichung,
Taiwan 8
China Medical University, Taichung, Taiwan
*Corresponding author: Chien-Ching Hung, MD, PhD Department of Internal Medicine, National Taiwan University Hospital, 7 Chung-Shan 1
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South Road, Taipei, Taiwan E-mail:
[email protected] Fax: +886-2-23707772 Telephone: +886-2-23123456 ext. 67552
Alternative corresponding author: Hsin-Yun Sun, MD
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Department of Internal Medicine, National Taiwan University Hospital 7 Chung-Shan South Road, Taipei, Taiwan E-mail:
[email protected] Fax: +886-2-23707772
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Telephone: +886-2-23123456 ext. 63557
Abstract: 250 words
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Word Count:
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Text: 2543 words
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Running title: Attitudes towards PrEP and HIV infection
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Abstract Objectives: We aimed to investigate the attitudes towards pre-exposure prophylaxis (PrEP) among individuals who sought voluntary counseling and testing (VCT) for HIV in Taiwan, where PrEP is not reimbursed by the insurance. Methods: Between April and October, 2016, an anonymous questionnaire interview
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was conducted among VCT clients to inquire about the attitudes towards PrEP against HIV infection. Multivariate logistic regression analysis was performed to identify the associated factors with willingness to initiate PrEP.
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Results: During the 6-month period, 1173 VCT clients completed the survey, with
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67.3% being homosexual or bisexual male. 79.7% of clients reported having 1 to 5
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sexual partners within 3 months, 38.3% experienced condomless anal sex within 1
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year, and 7.5% ever used recreational drugs before or during sexual activity. While
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67.2% of clients knew of post-exposure prophylaxis, 40.2% heard of PrEP before this survey. Overall, 546 clients (46.5%) were willing to initiate PrEP and 89.5% of them
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would choose event-driven PrEP strategy. In multivariate analysis, male gender (OR,
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1.655, 95% CI, 1.025-2.671), one-night stand (OR 1.381, 95% CI 1.046-1.824), condomless anal sex (OR 1.403, 95% CI 1.055-1.865), ever using recreational drugs before or during sexual activity (OR 2.520, 95% CI 1.507-4.214), and knowledge of PrEP (OR 1.451, 95% CI 1.085-1.941) were associated with willingness to initiate PrEP. Conclusions: A substantial percentage (46.5%) of VCT clients were willing to initiate 3
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PrEP against HIV in Taiwan, which was associated with male gender, engagement in one-night stand and condomless anal sex, use of recreational drugs, and awareness of PrEP.
Key words: HIV prevention; men who have sex with men; tenofovir disproxil
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fumarate; emtricitabine; chemsex; sexually transmitted infection
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Strengths and limitations of this study (up to five short bullet points) 1. This is the first study in the Asia-Pacific region to address the willingness of using pre-exposure prophylaxis (PrEP) among individuals seeking voluntary counseling and testing services, particularly men who have sex with men (MSM). 2. This study provides important information on factors associated with the
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willingness of PrEP use, which will be helpful in implementation of PrEP among individuals at risk for HIV infection in Asia-Pacific region, where PrEP is not
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reimbursed by insurance.
3. The study is limited by the fact that the findings in this single-center study with a
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HIV incidence rate among MSM being 5.5 per 100 person-years may not be
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generalized to other centers or countries.
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Introduction Pre-exposure prophylaxis (PrEP), with the use of antiretroviral agents by HIV-negative individuals before potential exposure to HIV to prevent transmission, has been proven to be efficacious in the reduction of HIV transmission in clinical trials in certain populations, such as men who have sex with men (MSM), heterosexual men
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and women, and injection drug users (IDU).1-4 The efficacy of PrEP depends on the adherence to daily doses of tenofovir disoproxil fumarate (TDF) and emtricitabine
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(TDF/FTC).5 A daily dose of oral PrEP could reduce the risk of HIV transmission by up to 99% if adherence was high (taking 7 tablets or more per week).5 The United States
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(US) Food and Drug Administration (FDA) has approved daily TDF/FTC as PrEP in July,
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2012.6 The US Centers for Disease Control and Prevention (CDC) published a
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comprehensive clinical practice guideline of PrEP for the prevention of HIV infection
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in May, 2014.7
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Although the results of the clinical trials of PrEP are promising and a significantly
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increasing trend in the utilization of TDF/FTC for PrEP among commercially insured persons in the US between 2010 and 2014,8 implementation of PrEP among high-risk populations needs an understanding of sociocultural relationship, knowledge and acceptability of intervention, and appropriate risk assessment. Several studies have explored attitudes and willingness of PrEP in different high-risk populations.9-12 The
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percentage of willingness and acceptability of PrEP ranged from 49.9% to 60.8% in these studies, which was associated with lower levels of education, regular gay scene attendance, high-risk unprotected anal intercourse, and testing for HIV or sexually transmitted infections (STIs) in the previous 12 months.11 In Asia-Pacific region, PrEP using TDF/FTC has not been widely implemented or
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reimbursed by the health insurance. Understanding how PrEP is perceived by individuals at risk for HIV transmission is important before implementation of PrEP as
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one of the HIV prevention strategies. This cross-sectional questionnaire survey aimed to investigate attitudes toward PrEP among individuals seeking anonymous voluntary
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counseling and testing (VCT) services for HIV in Taiwan.
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Methods Setting of the voluntary counseling and testing services VCT services for HIV and syphilis have been offered free-of-charge in Taiwan, with grant support from the Taiwan Centers of Disease Control (CDC).13 The National Taiwan University Hospital (NTUH) has provided VCT services since 1999, which was
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expanded in 2006. The number of attendees of the VCT program at NTUH accounted for ~14% of the total number in Taiwan in recent years.14,15 Each client seeking VCT
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services would have a unique identification code for test results, and completed a standardized anonymous, self-administered questionnaire interview (available as
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Supplementary data at BMJ Open Online), designed by Taiwan CDC. After completion
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of counseling by trained counselors, a blood sample was obtained for testing for HIV,
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syphilis and other STIs.13 The VCT clients gave written informed consent by using the unique code before participating in this survey.
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Among the VCT clients, the overall prevalence and incidence was 3.5% and 3.4
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per 100 person-years (PY) for HIV infection, 2.2% and 1.6 per 100 PY for syphilis, and 0.3% and 0.34 per 100 PY for HCV infection, respectively; and the prevalence was 4.2 to 4.7% for chlamydia, 1.0% for amoebiasis, and 0.7% for gonorrhoea.13,15,16 Among MSM population, the incidence of HIV infection was 10-fold higher than that of heterosexuals.17
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In Taiwan, the number of HIV-positive patients reported to Taiwan CDC was 33,018 as of 31 October, 2016, with an estimated HIV prevalence of 1,353 per 100,000 populations. MSM remain the leading risk group of HIV infection, accounting for 60.0% of reported cases of HIV infection.18 HIV care, including combination antiretroviral therapy and monitoring of plasma HIV RNA load and CD4 count, is
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provided free-of-charge at designated hospitals around Taiwan. The National Health Insurance does not reimburse the cost related to PrEP, though Taiwan CDC and
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Taiwan AIDS Society have issued PrEP guidelines.
Questionnaire interview of PrEP
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The content of this questionnaire for VCT and PrEP comprised 4 parts: first, the
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general and basic data of age, gender, level of education, current employment status,
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and current monthly income status; second, frequency of seeking VCT for HIV testing,
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and activities clients engaged in; third, risk assessment, number of sexual partners in
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the past 3 months, condomless anal intercourse, and use of recreational drugs in the past 1 year; fourth, the knowledge of HIV post-exposure prophylaxis (PEP) and PrEP, willingness to use PrEP, concerns about using PrEP, and reasons of no intention to use PrEP. The pilot questionnaire interview was conducted among the first 66 VCT clients
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to identify the validity and comprehensibility of the questionnaire from March 9 to April 7, 2016. After modification of the questionnaire, 44 clients piloted questionnaire interview from April 8 to 13, 2016 and no changes were made to the questionnaire thereafter. Before the questionnaire interview, PrEP was briefly described and information on two current PrEP strategies were provided: oral PrEP
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with TDF/FTC administered on a once-daily basis and with TDF/FTC on an on-demand (event-driven) basis.19,20
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Statistical analysis
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Statistical analyses were performed using SPSS software version 17.0 (SPSS Inc.,
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Chicago, IL, USA). Continuous variables were reported as mean ± standard deviation
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(SD), and compared with Student’s t test. Categorical variables were expressed as
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percentage of the total number of patients analyzed, and compared with Chi-square
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test. To identify factors associated with willingness of PrEP use, the variables with a P
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value less than 0.05 in univariate analysis were entered into the multivariate logistic regression analysis. A P value of less than 0.05 was considered statistical significance. Missing data were excluded for analysis.
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Results From 8 April to 8 October, 2016, a total of 1175 clients sought VCT services at NTUH and 1173 of them agreed to participate in this study and completed questionnaire interview. The demographic and clinical characteristics of the participants are shown in Table 1. The participants had a mean age of 29.7 years (standard deviation, 7.9
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years), 88.2% were of male gender, 67.3% were homosexual or bisexual male, 88.3% had diploma more than high school, 61.6% had full-time job, and 57.2% had monthly
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income more than 30,000 New Taiwan Dollars (NTD) (approximately 950 U.S. dollars).
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Regarding the activities that VCT clients were engaged in, 57.5% of the clients
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reported having sex with someone online from apps, and 27.5% had one-night stand
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sex. Up to 80% of the clients (79.7%) reported having 1 to 5 sexual partners in the
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past 3 months; 38.3% had condomless anal sex within the past 1 year and 11.1% had
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partners with HIV infection or other STIs. While 45.2% of the clients had a committed
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sexual partner, 69.0% had a casual sexual partner. Around 8.0% of the clients (7.5%) admitted to use of recreational drug use during sexual activity or attending a drug party within 3 months before this survey. With respect to knowledge on HIV testing and prevention, 52.8% of participants had used to attend regular screening for HIV. About two thirds of the clients (67.2%)
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knew of PEP while 40.2% heard of PrEP before this survey. While 3.4% of participants tested positive for HIV, 2.9% tested positive for syphilis in the survey during the study period. Overall, 546 (46.5%) participants expressed their willingness to use PrEP. Comparisons of the baseline data and characteristics between the clients with and
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without willingness to use PrEP are shown in Table 1. Compared with the clients without willingness to consider PrEP, those with willingness to use PrEP were more
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likely to be male (93.4% vs. 83.7%, P < .0001) and homosexual or bisexual male (75.8% vs. 60.0%, P < .0001), and report having sex with someone online from apps
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(61.5% vs. 53.9%, P = 0.0092), having sex with someone by dating at places like a pub,
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bathhouse or gym (11.5% vs. 7.8%, P = 0.0362), and having one-night stand sex
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(32.6% vs. 23.1%, P < .0001). The VCT clients with willingness to use PrEP had a
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higher proportion of having full-time job (66.5% vs. 58.2%, P = 0.0112) and current
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monthly income more than 30,000 NTD (60.9% vs. 54.0%, P = 0.0203).
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When the risk behaviors were concerned, individuals with willingness to use PrEP were less likely to have zero sexual partners within the past 3 months (13.8% vs. 19.7%, P = 0.0295) and have a casual sex partners (53.7% vs. 65.6%, P < .0001), but were more likely to have condomless anal intercourse within 1 year (46.2% vs. 31.4%, P < .0001) and ever used recreational drug during sexual activity or attending a drug
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party (11.7% vs. 3.8%, P < .0001). Regarding the knowledge of HIV testing and prevention, the clients with willingness to use PrEP were more likely to regularly screen for HIV (60.3% vs. 46.4%, P < .0001), have awareness of PEP (73.1% vs. 62.0%, P < .0001) and PrEP (48.0% vs. 33.3%, P < .0001), and receive a diagnosis of HIV infection during the current VCT
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visit (5.7% vs. 1.4%, P < .0001) In multivariate analysis, factors associated with willingness to use PrEP are
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shown in Table 2. Independent factors associated with willingness to start PrEP included male gender (odds ratio [OR], 1.655, 95% confidence interval [95% CI],
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1.025-2.671, P = 0.0391), one-night stand (OR, 1.381, 95% CI, 1.046-1.824, P =
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0.0230), condomless anal sex (OR, 1.403, 95% CI, 1.055-1.865, P = 0.0197), ever using
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recreational drugs during sexual activity or attending a drug party (OR, 2.520, 95% CI,
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1.507-4.214, P = 0.0004), and knowledge of PrEP (OR, 1.451, 95% CI, 1.085-1.941, P =
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Of the 546 clients who reported willingness to use PrEP, 89.5% preferred to use TDF/FTC on an on-demand (event-driven) basis. However, the concerns raised about PrEP included higher cost of medications (41.0%), potential side effects (33.5%), and inconvenient location to acquire TDF/FTC (28.7%). The reasons for not considering PrEP for the 627 clients included having adopted protective measures during sex
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(78.5%), and concerns about higher cost of medications (18.5%), potential side effects (11.6%), and inconvenient location to acquire TDF/FTC (8.6%).
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Discussion This is the first study to report on awareness of using TDF/FTC as PrEP against HIV and willingness to use PrEP among individuals seeking for VCT in Asia-Pacific region in recent years. We found that, while PrEP was not reimbursed by the National Health Insurance in Taiwan, 46.5% of VCT clients were willing to use PrEP and 89.5%
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of them preferred to use PrEP on an event-driven basis. VCT clients who were male with knowledge of PrEP, and had been engaged in condomless anal sex and use of
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recreational drugs were more likely to report willingness of initiation of PrEP. Given the demonstrated efficacy in MSM who were engaged in risky behaviors of HIV
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transmission,19,20 these findings suggest that there is a substantial unmet need for a
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new prevention strategy against HIV transmission among individuals who perceived
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themselves at risk for HIV and STIs and sought VCT in Taiwan.
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Regarding risky behaviours, we found that the associated factors with
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willingness to use PrEP included male gender, engaged in one-night stand and
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condomless anal sex, ever use of recreational drugs before or during sexual activity or attending to a drug party, and awareness of PrEP use. These factors identified were similar to those reported in other studies,10,11,21-24 which implies that engagement in risky sexual behaviours and knowledge of PrEP use may potentiate the willingness to use PrEP. However, factors related to risky sexual behaviors,
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particularly ever use of recreational drugs before or during sexual activity, have not been identified in previous studies. Recreational drug use before or during sex, also termed “Chemsex”, was associated with increased odds of unprotected anal intercourse by encounter-level analysis,25,26 which was a risk factor for acquisition of HIV infection.13,27,28 The published guidelines also identified those persons having
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chemsex as potential candidates to initiate PrEP.7 The finding that willingness to take PrEP was associated with prior knowledge of
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PrEP in our study is in line with those of previous studies. Goedel WC and colleagues identified correlates of awareness and willingness to use PrEP in gay, bisexual, and
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other MSM in New York City.29 In Spain, MSM who had heard of PrEP were more
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forceful in their options on willingness to use PrEP.30 Therefore, the more awareness
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of PrEP, the higher acceptability the population at risk will have. Populations at risk
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for HIV infection should be provided with information, education and counseling of
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PrEP use, which could facilitate implementation of PrEP use.
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Among VCT clients with willingness to use PrEP, almost 90% of them preferred event-driven strategy to prevention against HIV infection in our study. However, the VCT clients were concerned about inconvenient location to acquire TDF/FTC (28.7%), higher cost of medications (41.0%) and potential side effects (33.5%). In the Dutch study, Bil and colleagues found that the benefits of intermittent versus daily PrEP use
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included the lower cost and potential risk of side effects, and lower threshold to decide to start using intermittent PrEP, while the barriers to PrEP included the perceived need to plan their sex life and adhere to multiple prevention strategies among MSM.31 Another qualitative investigation identified preference of on-demand PrEP over daily PrEP, injectable PrEP, and free or standardized access through
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community organizations or government hospitals among MSM in India.32 The greatest consensus regarding more acceptable PrEP attributes has been in the mode
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of delivery and its cost.30 Therefore, provision of information on PrEP efficacy and potential side effects, a convenient location of PrEP service, and reimbursement of
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PrEP are necessary to make implementation of PrEP successful among VCT clients at risk.
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The cost of PrEP medications has been a major concern and barrier to wide
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implementation of PrEP among persons at risk for HIV infection. Several
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mathematical models investigated the cost-effectiveness or impact of PrEP on the
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HIV epidemic among MSM in North America,33-37 Australia,38 the United Kingdoms39 and the Netherlands.40 All these studies demonstrated targeting PrEP to MSM at high risk of HIV infection to be cost-effective. The variable level of cost-effectiveness in studies could be due to the differences in the HIV epidemic among MSM, direct and indirect costs, and the percentage of MSM targeted for intervention. Therefore, the
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demonstration of the cost-effectiveness of PrEP and the potential impact on HIV epidemic when PrEP is used along with other HIV treatment and prevention programmes should be able to provide evidence and rationale for the policy makers to commit to the implementation of affordable PrEP for persons at risk for HIV infection.32,33
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This study has several limitations. First, the study was conducted using anonymous questionnaire interview to collect information on sexual risk behaviors
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and all data were self-reported; therefore, it is difficult to avoid recall bias of VCT clients and we were not able to verify the information provided. Second, this is a
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single-center study including mainly MSM with an HIV incidence rate of 5.5 per 100
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PY and all the study participants are of Asia ethnicity. Therefore, our findings may not
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be generalized to patients of other ethnicities and countries.
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Conclusions
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Among individuals seeking for VCT service in Taiwan, a substantial portion (46.5%) of participants had willingness to take PrEP against HIV infection, which were independently associated with risky sexual behaviors and awareness of PrEP use. The barriers to PrEP included cost, side effects, and accessibility issue. The implementation of PrEP could be facilitated through providing with information on
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PrEP and reimbursement of PrEP.
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Acknowledgements We would like to thank the VCT clients for their participation in this survey and Taiwan Centers for Disease Control for the research grant support.
Contributors
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YCL, SYC, HYS, and CCH designed the study; KYL, LSC, WCL, and CHW performed the questionnaire interview and data collection; YCL, HYS, KYL, and WCL contributed to data analysis; and SCC oversaw the study. First draft was written by YCL with
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substantive revisions and input from all authors. All authors have read and approved the final manuscript.
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Funding: This study was supported by grants from Taiwan Centers for Disease
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Control (MOHW105-CDC-C-114-000104 to Chien-Ching Hung). The funding source
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played no role in study design and conduct, data collection, analysis or interpretation, writing of the manuscript, or the decision to submit it for publication.
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Conflict of interests
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Chien-Ching Hung has received research support from Janssen and ViiV and speaker honoraria from Bristol-Myers Squibb, ViiV, Abbvie, and Gilead, and served on advisory boards for Gilead and Abbvie. Other authors, none to declare.
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transmitted drug resistance of HIV-1 strains among persons seeking voluntary counselling and testing in Taiwan. J Int AIDS Soc. 2014; 17: 19758. 18. Taiwan CDC. Statistics of HIV/AIDS. 2016. Available at: http://www.cdc.gov.tw/english/downloadfile.aspx?fid=61F11C253AE76DEA (Accessed 29 Oct 2016). 19. McCormack S, Dunn DT, Desai M, et al. Pre-exposure prophylaxis to prevent the
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study of drug use and sexual outcomes in multipartner encounters reported by men who have sex with men. AIDS Behav. 2016; 20: 646-54 27. Plankey MW, Ostrow DG, Stall R, et al. The relationship between methamphetamine and popper use and risk of HIV seroconversion in the multicenter AIDS cohort study. J Acquir Immune Defic Syndr 2007; 45:85–92. 28. Chen X, Li X, Zheng J, et al. Club drugs and HIV/STD infection: an exploratory
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Supporting information Additional Supporting Information available may be found in the online version of this article as Supplementary material for the questionnaire about attitudes towards PrEP against HIV infection among individuals seeking for voluntary counselling and testing for HIV.
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Table 1. Univariate analysis of factors associated with the willingness to use pre-exposure prophylaxis (PrEP) among 1173 individuals seeking for voluntary counseling testing for HIV in Taiwan Variables
Individuals
Individuals
Statistics
willing to use
unwilling to use
P value
PrEP
PrEP
Patient number, n (%)
546 (46.6)
627 (53.5)
Age, mean (± SD), years
29.7 (±7.2)
29.8 (±8.6)
0.8883
Male, n (%)
510 (93.4)
525 (83.7)