Uptake of HIV testing and counseling, risk perception and linkage to HIV care among Thai university students

Background HIV testing and counseling (HTC) with linkage to care after known infection are key components for HIV transmission prevention. This study was conducted to assess HTC uptake, HIV risk perception and linkage to care among Thai university students. Methods An outreach HTC program was conducted in a large public university in Thailand from January 2013 to December 2014. The program consisted of brief HIV knowledge assessment, free HTC, HIV risk assessment and education provided by the healthcare personnel. Students were categorized into low, moderate and high-risk groups according to the pre-defined HIV risk characteristics. Results One-thousand-eight-hundred-one students participated in the program, 494 (27 %) underwent HTC. Independent characteristics associated with no HTC uptake included female sex (P < 0.001), lower HIV knowledge score (P < 0.001), younger age (P < 0.001) and students from non-health science faculties (P = 0.02). Among the 494 students undergoing HTC, 141 (29 %) were categorized into moderate or high-risk group, of whom 45/141 (32 %) had false perception of low HIV risk. Being heterosexual was independently associated with false perception of low HIV risk (P = 0.04). The rate of new HIV infection diagnosis was 4/494 (0.8 %). Of these 4 HIV-infected students, 3 (75 %) were men who have sex with men and only 2 of the 4 students (50 %) showed up for HIV continuity care. Conclusions An outreach HIV prevention program with HTC was feasible and beneficial in detecting HIV risk and infection among the university students. However, interventions to improve HTC uptake, HIV risk perception and linkage to care are needed.


Background
Human immunodeficiency virus (HIV) infection and acquired immune deficiency syndrome (AIDS) have been major public health problems in Thailand with the prevalence of HIV infection of 1.1 % and 8200 newlydiagnosed HIV-infected individuals in 2013 [1]. The highest number of AIDS cases was observed in the age group of 30-34 years (24.97 %) followed by the age group of 25-29 years (21.73 %) [2]. Given the lag period of 5-15 years between the estimated time of acquiring HIV and the time of AIDS diagnosis observed among Thai HIV-infected patients at our hospital, individuals in adolescence and early adulthood may have high rates of HIV acquisition in Thailand.
University students are amongst populations in the age groups with the highest probability of acquiring HIV. Our previous study conducted among university students indicated that despite their high level of knowledge, HIV risks and risk behaviors were commonly reported and some of the students were not aware of their HIV risks [3]. Nonetheless, uptake of HIV testing and counseling (HTC), the impact of HIV risk perception on HTC acceptance and linkage to care after diagnosis of HIV infection have not been evaluated in Thai university students.
Universal HTC has been recommended in the communities where HIV prevalence is 0.1 % or higher to increase awareness of HIV status, HIV diagnosis and linkage of HIV-infected persons to care, and prevent HIV transmission [4]. During the HTC program, HIV risk perception should be assessed and targeted education to improve risk perception and reduce risk behaviors should be provided. In Thailand, HIV testing is available free of charge and can be done twice a year, as a part of an HIV prevention campaign conducted by The Ministry of Public Health. However, specific guidelines and protocols regarding how to implement HTC in key populations, especially adolescence and young adults have not been recommended. We conducted this study to evaluate the feasibility of an outreach HIV prevention program that incorporates HTC and linkage to care after an HIV positive test result. In addition, this study aimed to assess HIV risks, risk behaviors and HIV risk perception and its impact on HTC uptake and to determine the rate of and factors associated with HIV infection among Thai university students.

Study population, setting and design
This is a prospective study conducted between 1st January 2013 and 31st December 2014 among Thai students from six different faculties of a large public university, including Science, Engineering, Medicine, Medical Technology, Journalism and Mass Communication, and Laws. These 6 faculties were chosen as they are representative of university students from major faculties in medical science, science, and social science fields. This study was conducted in accordance with the amended Declaration of Helsinki and was approved by the Faculty of Medicine, Thammasat University Ethics Committee.

Study protocol
An outreach HIV prevention program that incorporated HTC was conducted during the study period by the HIV care team of Thammasat University Hospital. This team consists of 3 Infectious Diseases doctors, 2 HIV specialist nurses, 2 non-physician medical assistants and 2 HIV-infected volunteers, to promote HIV prevention and provide relevant education for the students. The program was conducted in designated open-space areas of the main building of each faculty from 10.00 a.m. to 2.00 p.m. weekly. Private rooms for HTC were available within the designated areas. Students in each faculty were approached and asked to participate in the program. Brief HIV knowledge assessment questionnaire, free HTC and education on HIV transmission prevention by the HIV care team were provided in the program. The brief questionnaire asked the participants to answer whether the 12 different statements about HIV transmission were true, false or they did not know the answer. HIV knowledge score was calculated based on the number of correct answer to these 12 statements. Demographics data, HTC acceptance and reasons for accepting or declining HTC were collected in the brief questionnaire form.
The students who voluntarily accepted HTC underwent pre-test counseling conducted by the HIV counselors. Data about demographics, HIV acquisition risks and risk behaviors, and HIV risk perception of the students were collected using the counseling form. The questions in the counseling form were derived from the survey form validated in previous studies [3,5]. The students who reported history of HIV infection were excluded from the HIV testing. A anti-HIV blood test was performed after the counseling. Primary and secondary telephone numbers of each student were recorded by the counselors. These contact numbers were used for HIV test result notification.

Study definitions
Sexual orientation and HIV risk perception were selfidentified by the students. The students identified their own HIV risks by answering "No risk at all", "A little risk (low-risk)", "More than a little (moderate-risk)" and "A lot of risk (high-risk)" to the HIV counselors. Actual HIV risk of the students was defined as "low-risk", "moderate-risk" and "high-risk" based on the prespecified risk characteristics and risk behaviors according to previous studies' criteria (Table 1) [3,5]. Students who were categorized as moderate or high-risk but perceived their risks as no or low-risk were classified as having false perception of low HIV risk.

HIV testing result notification
Notification of the test results was done via telephone within 72 h. The HIV counselors called all students to inform the negative results. However, if the test result was positive, they would inform the students to come to the hospital for post-test counseling and result notification, in accordance with Thai laws. A total of 3 calls (1 week apart) were attempted to notify the students' results and addition 3-week duration was allowed after that for the students to call back before contact failure was considered. Plans for their HIV continuity care were discussed with the HIVinfected students. The counselors called the students every 1 month after notification of the test results and asked whether the participants had already initiated HIV care and when they did so. If the participants had not initiated HIV care, the HIV counselors would assess and identify any problems/obstacles faced by the HIV-positive participants every time they did the follow-up calls and help to alleviate those problems/obstacles and further support the referral for care.

Data analyses
All statistical analyses were performed using SPSS version 15.0 (SPSS, Chicago, Illinois). Categorical variables were compared using Pearson's χ 2 or Fisher's exact test as appropriate. Continuous variables were compared using Mann Whitney U test. All P values were 2 tailed; P values less than .05 were considered statistically significant. Variables that were present at a significance level of P < .20 in univariable analysis of factors associated with no HTC acceptance, false perception of low HIV risk, and HIV infection were entered into logistic regression models. These variables were subsequently removed from the models in backward stepwise fashion if their P values were >0.05 until the final model had reached. Adjusted odd ratios (aORs) and 95 % confidence intervals (CIs) were determined for independent risk factors associated with no HTC acceptance, false perception of low HIV risk, and HIV infection.

Characteristics of the study participants and HIV transmission knowledge
A total of 2250 university students from 6 different faculties were approached, of which 1801 students (80 %) agreed to participate in the HIV prevention outreach program (Fig. 1). Demographic characteristics of the 1801 students are shown in Table 2. The mean age was 20.12 years (range 17-35 years). About a half of the students were female and the majority of them were from faculties in the Social Science field. The median score for HIV transmission knowledge was 10.64 (range 4-12). More than 80 % of the students correctly stated in the survey that "AIDS is caused by a virus", "You can get HIV from sexual contact with an HIV-infected individual", "Mosquitoes cannot transmit HIV", "Condon use can prevent HIV", "You cannot get HIV from having meal with  an HIV-infected individual", "HIV-infected individuals may not have symptoms for several years". "Asymptomatic HIV-infected individual can transmit HIV to other people", "Persons who look clean and healthy can already be infected with HIV", "One can know his/her HIV status by getting HIV blood test" and "Anti-HIV drugs can increase lifespan of the infected individual". Less than 80 % of the students could correctly state that "There is currently no vaccine that can prevent HIV infection" and "Having multiple sexual partners increases risk for getting HIV".    (Table 3). Of these 494 students, 484 (98 %) were reachable for HIV result notification within the median time of 3 days (range 2-44 days) while 10 (2 %) had contact failure. Among the 10 students with contact failure, the median age was 22 years (range 19-26 years), 5 (50 %) were male, 7 (70 %) were from faculties in the Health Science field, 3 (30 %) were from faculties in the Social Science field, 1 (10 %) had prior HIV test, 10 (100 %) were heterosexual, 2 (20 %) were categorized into high-HIVrisk group and none had false perception of low HIV risk. When comparing characteristics between students from different faculties (Table 3), students from faculties in the Health Science field were older, had higher score for HIV transmission knowledge and more likely to have prior HIV test. Higher proportion of students in the Health Science and Social Science fields reported to be homosexual compared to those in the Science field. Health Science students were more likely to perceive their HIV risk higher than their actual risk while Science and Social Science students were more likely to perceive their risk lower than actual risk. However, the proportions of students who had false perception of low HIV risk were not significantly different between students in the three groups.

Reasons and characteristics associated with declining HTC
HIV risk perception and characteristics associated with false perception of low HIV risk

Characteristics associated with HIV infection
Among the 494 students undergoing HIV test, 4 (0.8 %) were HIV-infected. All of these 4 students were newly diagnosed with HIV infection. Of these 4 HIV-infected students, 4 (100 %) were male, 3 (75 %) were homosexual, 3 (75 %) had moderate to high HIV risk and 1 (25 %) had low risk perception. All of these 4 students were contacted and informed the result within the median time of 8 days (range 3-13 days). Comparing between HIV-positive and HIV-negative students (Table 5), HIV-positive students were more-likely to be homosexual, have higher median number of different sexual partner within the past 3 months and have ever had injected drug with needle. In the multivariable logistic regression analysis, characteristics independently associated with HIV positivity were being homosexual men (aOR 12.75; 95 % CI 1.30-125.06: P = 0.03). Of the 4 HIV-infected students, only 2 (50 %) showed up for continuity care within 3 months after the diagnosis while the other 2 could not be further contacted after the first result notification call.

Discussion
Our study findings have important implications for implementation of HTC program among university students. First, our outreach HIV prevention program was successful in attracting many students to participate in during the 2-year study period. This provided opportunities to increase awareness about HIV/AIDS prevention among the students and to educate them on specific    issues about risk perception and risk behaviors reduction. Second, to our knowledge, this study was the first to assess the actual rate of HTC acceptance during the outreach program for university students. This "actual" rate of HTC acceptance was significantly lower than the rates of "willingness" to have HTC assessed through a study questionnaire in previous studies (63-72 %) [6,7]. This implies that students who indicate that they are willing to have HTC may not really have HTC in their real lives, which is an important barrier for HIV transmission prevention. Third, we identified several factors associated with no HTC acceptance among the students. Female were less-likely to accept HTC than male possibly due to perception of lower risk, being more afraid of blood/pain/needles when getting tested and stigmatization of having HIV tests. The other factors associated with no HTC acceptance included lower HIV transmission knowledge score, younger age and being students from non-health science faculties. These factors are relevant to less knowledgeable and experience about HIV/AIDS and were previously reported to be associated with no previous HIV testing and/or no willingness to have HTC among university students in other settings [6][7][8][9][10]. Altogether, our findings suggest the importance of HTC acceptance assessment and interventions to improve HTC acceptance including education about HIV/ AIDS and HTC for the students, use of cost-effective non-blood and painless HIV testing and strategies to reduce HIV stigmatization. The incorporation of validated HIV risk perception assessment in our outreach program was unique. This enabled the HIV counselors to identify students with false perception of low HIV risk and provide education to correct their risk perception. Based on the study risk categorization tool, 29 % of the students undergoing HTC had moderate to high risk for HIV acquisition; 69, 76 and 89 % used condom inconsistently for vaginal, anal and oral sex, respectively; 22 % of the students used to have or were not sure that they had STIs in the past year, and about one fifth to one third were not sure about their sex partners' risk behaviors. Although the proportion of students with moderate to high HIV risk was not as high as other high-risk populations including individuals attending an STI clinic (83 %) [5], participants attending a black gay pride event (67 %) [11] and men who have sex with men (MSM) attending a gay sauna (58 %) [our unpublished data], false perception of low HIV risk was prevalent. Being heterosexual was the independent factor associated with false perception of low HIV risk in this study consistent with reports from studies among STI clinic attenders and AIDS Help-Line users [12,13]. This may be explained by the belief that associates HIV risk with particular risk-recognized groups, i.e., MSM, injecting drug users and commercial sex workers rather than their risk behaviors [5,14,15]. The underlying mechanisms for false perception of low HIV risk among the students despite the high level of knowledge may include their risk assessment in light of remote or past low-risk behaviors despite current highrisk behaviors, optimistic bias that the risk behaviors they engaged in were at no or low-risk, denial or suppression mechanism and bias that they did not use facts in their judgment about risk perception but used certain cues inherent in the questions asked [16].
Previous studies demonstrated that 10-55 % of individuals undergoing blood-based HTC did not return for HIV results [17,18]. However, our study demonstrated the high rates of result notification (98 % for all students and 100 % for HIV-infected students). The higher rate of result notification in our study compared to those in the previous studies could be due to the use of HIV counselor-initiated confidential telephone contact with 2 weekly-follow-up calls rather than having the participants calling in for the results. Although the rapid HIV testing and result notification within 1 h is ideal strategy, these findings suggest that our test result notification protocol may be used in resource-limited settings where the rapid testing is not available. The lower rate of HIV infection among the university students compare to that of Thai general population is due to the overall lower risk of HIV acquisition among the students. Being homosexual men was independently associated with HIV positivity. This finding was consistent with reported high incidence of HIV infection among Thai MSM [19]. Despite being notified with the test result and receiving post-test counseling, only 50 % of HIV-infected students had engaged in HIV continuity care. Interventions such as point-of-care CD4 testing at the time of HTC [20], on-site HIV care providers to perform focused opportunistic infection screening and immediate antiretroviral therapy initiation if eligible, use of non-cash financial incentives for linkage to care [21], more emphasis and clear message to the students on the importance of linkage to care, antiretroviral therapy adherence and care retention, addressing plan for long-term care based on the student's medical coverage, preference and financial status may improve the students' linkage to care.
There were limitations in this study. First, the results may have limited generalizability to university students from a large public university. However, the findings of challenges in HTC acceptance and linkage to care, the importance of HIV risk perception assessment and targeted education based of the risk perception and the result notification protocol should be applicable to implementation of HTC in other settings. Second, the face-to-face interview during the pre-and post-test counseling might impact the disclosure of HIV risks and risk behaviors of the participants. However, this limitation was minimized since the counseling was done in a private room and the counselors were well-trained to build trust between the students and them. Lastly, the small number of HIV-infected students may limit identification of other factors associated with HIV infection. Nonetheless, the result can be a reference rate of HIV infection among university students in our setting.

Conclusions
Implementation of an outreach HIV prevention program incorporating HTC was feasible and provided opportunities to educate the students about HIV transmission, risk perception and risk behavior reduction. HIV risk perception assessment along with interventions to correct risk perception are necessary and should be included in the program. Rapid HIV testing and result notification, point-of-care CD4 testing and HIV care and educational interventions in both healthcare and community settings are needed to increase access to HIV testing and successful linkage to care.
Abbreviations AIDS, acquired immune deficiency syndrome; aOR, adjusted odds ratio; CI, confidence interval; HIV, human immunodeficiency virus; HTC, HIV testing and counseling; MSM, men who have sex with men; STIs, sexually-transmitted infections