Compliance and approach to voluntary HIV testing in a high-risk region for HIV transmission in Europe

Background The Kosovo province is being considered as a high-risk region for the spread of HIV. Objective To estimate the prevalence and factors associated with HIV testing in a sample of university students from the Serbian northern Kosovo province. Material and Methods A questionnaire examining socio-demographic characteristics, HIV-related knowledge, attitudes towards people living with HIV (PLHIV) and HIV testing was used in data collection. A total of 1,017 students from the University of Priština temporarily seated in Kosovska Mitrovica completed the questionnaire. Results Only 5.4% of students have previously been tested for HIV, even though the majority (70.9%) had a positive approach to HIV testing. Factors associated with having been tested for HIV were being male and younger, having interest in HIV testing and having previous contact with PLHIV. Being more knowledgeable about HIV and having stronger positive attitude towards PLHIV, being older, receiving information about HIV through friends and special educational programs, using condom at last sexual intercourse, having positive opinion on gays/lesbians and previous contact with PLHIV were associated with positive approach to HIV testing. Conclusion Having a positive approach to HIV testing does not suggest that students would take the HIV test. However, students who have low HIV-related knowledge, negative approach or lack of interest in HIV testing (believing that there is no need to take it) would likely never take the HIV test. Increasing HIV-related knowledge, acceptance of PLHIV and access to testing facilities should be public health priorities to raise HIV testing rates.


Introduction
Only 2.5% of the population aged 15-49 years (1.4% ≤24 years) in Serbia had ever been tested for HIV 1 . The rate of voluntary (i.e., client-initiated) HIV counselling and testing is almost five times lower than that initiated by health care providers 2 . Moreover, during the past decade, the HIV testing frequency in Serbia has declined, even though an apparent increase in the HIV incidence was reported [3][4][5] . By the end of 2019, there were 2,780 people living with HIV (PLHIV) in the Republic of Serbia and the estimated prevalence in the population aged above 15 was less than 0.1% 5 . The highest age-specific HIV incidence rate was registered among people aged 30-39 years (7.99 / 100,000) and 20-29 years (6.38 / 100,000) 5 . Unprotected sexual contact was registered as the most common mode of transmission of HIV in Serbia, and 11 infected men were registered per one infected woman 5 . Because timely testing facilitates the initiation of adequate treatment of HIV, the low testing rate presents a major obstacle to the effective control of the HIV spread [6][7][8] . The Serbian province of Kosovo has had numerous socio-economic, educational and health challenges as a result of previous armed conflict between the Serbian (predominantly living in North Kosovo) and the Albanian community (predominantly living in the remainder of Kosovo). While the scale of the HIV epidemic in Kosovo is deemed small, the prevalence of new HIV diagnoses in high-risk groups (men who have sex with men, injecting drug users and sex workers) is five times higher than that in the general population 9 . Factors such as the overall young adult population, limited business opportunities and high rates of unemployment, ongoing ethnic tensions, migrations, availability of inexpensive illicit substances and alcohol as well as developed sex industry due to the presence of foreign military and non-governmental organizations facilitate the HIV spread 5, 10 . Finally, the only counselling center for sexually transmitted diseases (STDs) and HIV available in this area has low visitation rates 11 . As a result, the Kosovo province is being considered as a high-risk region for the spread of STDs including HIV 5, 10 . The aims of this study were to: 1) estimate the prevalence of HIV testing in a sample of university students from the Northern Kosovo province; 2) examine factors associated with compliance and positive approach to HIV testing.

Methods Setting
The study was carried out from February 1 to June 1, 2014 at the University of Pristina temporarily seated in Kosovska Mitrovica, Northern Kosovo province. Kosovska Mitrovica has approximately 30,000 Serbian ethnicity residents. The University of Pristina temporarily seated in Kosovska Mitrovica is the only educational institution in Kosovo that provides high education in Serbian language. The University is composed of 10 schools with more than 5,000 undergraduate students. This setup allows for a unique opportunity to study university student population in the Serbian Kosovo province.

Participants
Students in the first and fourth study year were enrolled. Such selection enabled the recognition of different approaches to voluntary HIV testing at the beginning and at the end of university schooling. It also presented an indirect impact of education and growing up on testing approach over time. Participants were approached in all available classrooms during mandatory lessons on two randomly selected working days (Mondays and Thursdays). All ten schools were listed alphabetically and study recruitment lasted for one week in each school. The principal investigator (PI, the first author of this paper) in this research made contact with all the schools to arrange for the time of questionnaire distribution. The questionnaires were distributed after the compulsory classes have ended, while students were still in the classroom. The PI provided a detailed explanation about the questionnaire and the study purpose, highlighting that the survey was voluntary and anonymous. In case of refusal to complete the questionnaire, the students were allowed to leave the classroom and no coercion was in place. The PI was at students' disposal for any questions related to the study topic, survey and questionnaire. The informed consent was provided before the paper questionnaire was handed over to the potential participant by the PI inside the classrooms. Out of the invited 1,225 students, the response rate was 82.0%. The Ethics Committee of the Faculty of Medicine, University of Pristina temporally seated in Kosovska Mitrovica approved the study (No. 09-1608-1, issued on October 29, 2013).

Instrument
We distributed a questionnaire, developed within the 8th round of the Global Fund for the Fight against AIDS, Tuberculosis and Malaria of the European Union (GFATM) project (UNAIDS) and then modified for the Serbian set- lifestyle were added based on data from literature suggesting that young people are more likely to engage in risky behaviours because of sensation-seeking 13 . The final version of the questionnaire had 58 items (Appendix). The questionnaire was tested in a pilot study after which the acceptability and clarity of the questionnaire were confirmed suggesting that the study was feasible. The questionnaire explored participants' socio-demographic characteristics (six items), sources of information about HIV infection (six items), knowledge about HIV infection and transmission (14 items), previous HIV testing experiences, awareness and interest in HIV testing and self-perception of HIV risk (five items), attitudes towards PLHIV (17 items), opinions about high-risk groups for HIV (gays/lesbians, injecting drug users and sex workers), having had STDs in the past year and practice of risky behaviours (seven items). Only one answer per question was previewed.
Responses to items about HIV-related knowledge were scored as follows: one point for an incorrect answer; two points for not knowing or not being sure about a correct answer; and three points for a correct answer. The raw continuous Knowledge Score (KNS) was calculated as the sum of points obtained for all knowledge-related items. Higher scores suggested better HIV-related knowledge. Students' attitudes towards PLHIV were also scored. One point was assigned for having negative feelings; two points were assigned for feeling indecisive i.e., not sure what to think or feel; and three points were assigned for expressing positive attitudes and support to PLHIV. The Attitude Score (ATS) was obtained by summing the assigned points per item. Higher scores represented a stronger positive attitude towards PLHIV.

Main outcome measures
Participants were asked whether or not they had ever been tested for HIV (yes vs. no). We also evaluated their testing experiences and potential reasons for not having been tested (possible answer options: no, due to fear / no, due to finances / no need to get tested / does not know where to get tested). Awareness and interest in HIV testing were assessed by asking the students about their position in case they wanted to take the test (possible answers: I know where to take the test / I do not know where to take the test, but I know whom to ask / the test cannot be taken in our country / I do not know, I do not care). Circling one of former two answers was classified as positive approach to HIV testing. Circling one of latter two answers was classified as negative approach to HIV testing.

Statistical analysis
All analyses were performed in SPSS, version 21. Differences were tested using the ANOVA (F) and Kruskal-Wallis test (KW χ2). Spearman's correlation was used to investigate the associations between students' characteristics and different aspects of HIV testing. To analyse association between the variables, we used digital acyclic graphs (DAG) using an open-source platform www.dagitty.net. In DAG we considered "Knowledge about HIV" as the exposure was and "Been tested for HIV" as the outcome. We observed that the independent variables accounting for the socio-demographic characteristics of students were the main confounders, while the independent variables accounting for health behaviour were mediators of this association (Supplemental Figure  S1). Therefore, a binary logistic regression was performed to evaluate factors associated with having been tested for HIV (yes/no) and having a positive vs. negative approach to HIV testing (dependent variables). All models included KNS and ATS. The independent variables were classified in five models based on the questionnaire sections: 1) Socio-demographics; 2) Information sources; 3) Awareness and interest in HIV testing; 4) Mindsets and 5) Lifestyle.

Results
Description of the study sample Of 1,017 participants, 44.6% were males. The mean ± standard deviation (SD) age of students was 21.34 ± 3.51 years. One third (30.3%) studied health-related disciplines, and the majority (62.3%) were in the first study year. The internet was the main source of information about HIV (81.4%). The students generally visited nightclubs on weekends (58.3%), hardly ever used illicit drugs (4.6%), drank alcohol in moderation (64.7%) and had one or less sexual partners in the past year (74%). Approximately one third of students never used a condom. Study participants more often expressed a negative opinion (i.e., desire to protect themselves or avoid contact) when it comes to drug users (64.0%) and gays / lesbians (50.0%), while a smaller percentage of participants had a negative opinion regarding sex workers (42.4%) ( Table 2).

Approach and compliance with HIV testing
A positive approach to HIV testing was registered in 70.9% of the respondents. However, only 5.4% of students have taken the HIV test. Of 721 students who had a positive testing approach, only 53 (7.3%) had taken the test. Almost all (99.3%) students who had a negative testing approach had never taken the HIV test. Among the students who had not previously been tested, 69.4% were well aware of the testing facilities (Table 2). The least frequent reason for non-compliance to HIV testing was financial constraint (0.7%). Fear of testing or receiving the test results prevented 54 (5.3%) students from testing. Three quarters (762, 74.9%) of students believed that they did not need to be tested. In addition, 266 (26.2%) were not interested in testing. Some students (139, 13.7%) did not know where to take the test, while 30 (2.9%) thought that HIV testing was not organized in the Serbitheir an Kosovo province. Most students had adequate knowledge about HIV and expressed a positive attitude towards PLHIV. The mean ± SD KNS of students tested for HIV was 33.42 ± 3.50, while KNS of students who were never tested was 32.75 ± 3.21 (p = 0.12). Contrary, KNS of students who had a positive approach to testing was significantly higher than among those who had a negative approach to testing (tested mean ± SD ATS = 33.04 ± 3.10; not tested = 31.91 ± 3.58; p < 0.01). However, there were no significant differences (p = 0.43) between the tested and non-tested students relative to the ATS (tested students mean ± SD ATS = 39.50 ± 4.55; not tested = 39.06 ± 4.48). On the other hand, ATS of students who had a positive approach to testing was significantly higher compared to those students who had a negative approach (positive mean ± SD ATS = 39.81 ± 4.20; negative = 37.35 ± 4.63; p < 0.01). Students' characteristics, behaviours, mindsets and attitudes are presented in Table 2. Correlations and differences between the assessed variables and various aspects of HIV testing and approach to testing are presented in Supplemental Tables S1 and S2. Figure S1. Initial DAG model of the association between knowledge about HIV and being tested for HIV Supplemental   Logistic regression examining positive approach to HIV testing revealed significant equations (B = -0.89; Wald = 166.32; Exp(B) = 0.411) for all the variable groups (Socio-demographic χ2 = 91.76; p < 0.01; Information sources χ2 = 112.78; p < 0.01; Awareness and interest in HIV testing χ2 = 81.49; p < 0.01; Mindsets χ2 = 82.46; p < 0.01; Lifestyle χ2 = 82.79; p < 0.01) ( Table 4). Factors associated with positive approach to HIV testing were having higher knowledge about HIV and stronger positive attitude towards PLHIV, being older, having received information about HIV through friends and special educational programs, using condom at last sex, having positive opinion on gays/lesbians and previous contact with PLHIV.

Principal findings
This study found that a very small proportion of students had previously been tested for HIV, even though the majority had positive approach to HIV testing. Having better knowledge about HIV and positive attitudes towards PLHIV was associated with having positive approach to HIV testing, but not with previous HIV testing. The results of this study suggest that there is a difference in factors associated with previous HIV testing and having a positive approach to HIV testing.

Comparison with similar studies
Previous studies suggested that a lower level of HIV-related knowledge is often coupled with HIV-related stigma when deciding whether or not to take the test 14 . Fear of stigmatization is a major barrier to HIV testing 3,15,16 . This is commonly related to social labelling, such as being an injecting drug user, sex worker, gay/lesbian, or already being HIV positive. A review of literature conducted in low-and middle-income countries found that adequate HIV-related knowledge decreases the HIV-related stigma, which in turn increases the rates of HIV testing 17 . However, studies conducted in the United States and South African Republic suggested that higher knowledge about HIV did not influence the intention to take the test 18,19 . Feelings of fear and a sense of invulnerability have also been identified as major emotional barriers to HIV testing in college students 15 . Interestingly, only 5.3% of our students reported fear as a reason for non-compliance to HIV testing. This stands in contrast with the results of other studies 15,19 . In a previous study of high school pupils in Serbia, fear was found to be one of the most common reasons for non-compliance, despite having a positive attitude and being willing to take the test. About one-third of students experience less stigmatization in the academic setting compared to their home environment 20 and a greater availability of HIV counselling and testing services facilitates compliance with HIV testing 15,16 . Inconsistent condom use and practice of other risky behaviours have been associated with higher HIV testing rates 21 . Also, persons who do not use condoms consistently and frequently changes sexual partners are more likely to be aware of a higher HIV risk, which, in turn, supports a higher testing compliance 22,23 . Health education programs, especially peer education, had a positive impact on one's approach to HIV test-ing 24,25 . The advantages of peer education come from the fact that the audience can relate to their educators who use a similar language and do not have an authoritarian role. The problem of HIV testing could be addressed by bridging the cognitive (knowing that testing is useful and where and how it could be done) and emotional (fear of the consequences of testing and feeling invulnerable to HIV infection) dimensions.

Importance of the study for public health
The findings from this study suggest that knowledge and attitudes towards PLHIV go hand-in-hand, and therefore, peer education programs aiming at increasing HIV-related knowledge should address attitudes and treatment of PLHIV as well. Our results add to the body of evidence that being more knowledgeable about HIV was not associated with a previous HIV testing experience among university students living in a high-risk region for HIV transmission. The finding that most students declared that they did not need to take the test supports the assumption that most students in this study were at a low risk of HIV exposure (never using drugs, not being sexually active, consistent condom use and not having multiple sexual partners) while being knowledgeable about HIV. Based on the results from this study, the contact with PLHIV could help reduce fear of HIV and HIV-related stigma, and therefore, facilitate the increase in HIV testing uptake. We observed that special education about HIV was associated with having a positive approach to HIV testing, and that interest in HIV testing was associated with previous HIV testing. Involvement of PLHIV in peer education on HIV could help to increase the awareness of HIV testing among young adults. A total of 13.7% of students were misinformed that HIV testing is not available in their country even though HIV testing in Kosovo has been free of charge for many years. A lack of facilities offering confidential counselling and HIV testing in the northern Kosovo province could explain the low HIV testing rates in this study. Specifically, Students' Public Health Centers, where students are obliged to come for periodic health checks, are suitable venues in which students could receive adequate HIV-related information and change their perception of HIV testing.

Cues to action
Low testing rates in students may delay timely diagnosis African Health Sciences, Vol 22 Issue 4, December, 2022 and treatment. This facilitates the transmission of HIV infection as the incidence of HIV in young people rises 26,27 . Therefore, it is essential to enhance the rate of testing. First, accessibility of counselling can strongly influence the change in health-related behaviours that affect the HIV risk reduction 28 . In more urbanized settings calls for testing could be broadcasted through mass media and Internet (short video clips, banners etc.), while people who work with PLHIV (such as health professionals, counsellors, etc.) should publicly discuss the relevance of testing and their experiences from the counselling center. In less urbanized settings, the efforts to increase the HIV testing rates should focus on the trusted members of the local community, such as local health professionals, athletes, artists, academics or representatives of the religious communities, who may publicly discuss the issues surrounding HIV. The channels of communication with young people have evolved along with the technological advancement [29][30][31] . Previous studies indicated that interventions based on the use of new technologies can lead to an increase in HIV testing among young people 29 . In this way users are able to estimate individual risks by filling in a simple online test or understand the risks through video materials or computer games [29][30][31] . Also, this approach helps to overcome barriers to HIV testing in young people such as stigma and discrimination, low perception of personal risk, presence and monitoring of parents, lack of privacy and confidentiality [29][30][31][32] . Use of digital platforms allows for an easier access to counselling. Furthermore, banners, popup windows and reminders about prevention of HIV and testing should be included in dating and socializing apps. Finally, the HIV testing is also related to the availability of the testing kits. To increase the testing rate, it is essential to ensure the availability of HIV tests 29,30 .

Study limitations
This study explored a sensitive topic, and it is, therefore, open to information bias, because all information about students including previous testing experience were self-reported. Due to a cross-sectional study design, the direction of the association cannot be defined. Therefore, the inference on causal pathways can be limited. This study was an integral part of a larger research about knowledge, attitudes and behaviours related to HIV. Because this study was part of a PhD project, the entire investigation had to be completed before the results could be published, which may constitute a limitation due to de-layed reporting. Nevertheless, because the overall social and political circumstances in Kosovo have not markedly changed since the end of the armed conflict in 1999, the obtained results are still novel and relevant. Specifically, policies with regards to sex education have remained similar to that when the study was conducted i.e. sex education has not yet been part of the school program. For this reason, knowledge about HIV and attitudes towards PLHIV observed in this study reflect the current state of affairs.

Conclusion
In conclusion, we report a discrepancy between a large proportion of students who had a positive approach to testing and a small proportion of students who have previously taken the HIV test. Having more knowledge about HIV and positive attitude about PLHIV was associated with having a positive approach to HIV testing, but not with compliance to testing. Given the overall positive approach to HIV testing, access to testing facilities to increase the HIV testing rates should be one of public health priorities in the province. Promotion of education about HIV and contact with HIV positive persons might play an important role in forming positive approach to HIV testing.