Prevalence and determinants of intercourse without condoms among migrants and refugees in Morocco, 2021: a cross-sectional study

With the world's migratory flow, the risk of infection by the human immunodeficiency virus (HIV) among migrants is increasing. The prevalence of intercourse without condoms with a casual or commercial sex partner, a high-risk sexual behavior for HIV infection, is unknown among migrants. The purpose of this study was to determine the prevalence of intercourse without condoms among migrants and the risk factors associated with not using condoms. In Oujda, we conducted a cross-sectional survey of 416 sexually active migrants. We used a multistage sampling method. Face-to-face interviews were conducted with participants to collect socio-demographic information, disease perception, behavioral habits, sexual behavioral habits, and para-clinical parameters. A multivariate logistical regression analysis identified the risk factors associated with high-risk HIV sexual behaviors. The prevalence of intercourse without condoms with a casual or commercial sex partner was 72.8%, with a median age of 25.0 years, and 212 (69.9%) were males. The prevalence of HIV was 0.2%. Being homeless, having difficulty obtaining condoms, and only having a basic education were all risk factors for these sexual behaviors. Migrants with precarious living conditions are at increased risk of having intercourse without condoms. This group must be prioritized by strengthening public health programs targeting the health of migrants as well as the intervention of thematic non-governmental organizations. Vigilant monitoring of the HIV epidemic, with a focus on vulnerable populations, should be a high priority in Morocco.

www.nature.com/scientificreports/ of persecution. However, everyone has the right to access healthcare regardless of their race, religion, political opinions, or economic or social conditions. The large influx of migrants, refugees, and asylum seekers has intensified global focus on the health of vulnerable populations and prompted host countries to address their health needs. Migrants, refugees, and asylum seekers are a population at risk of infection by sexually transmitted diseases such as the human immunodeficiency virus (HIV), a disease that presents a redoubtable challenge to life and human dignity. This high risk is attributed to the pre-migration characteristics of HIV-endemic countries of origin, as well as the post-migration characteristics marked by the impact of the migratory route, social and ecological determinants of health, and linguistic, cultural, financial, and legal barriers related to access to preventive services in host countries 3 .
The HIV pandemic takes a heavy toll on human lives, individuals, communities, and health systems. In 2021, globally, an estimated 37.7 million people were living with HIV, 1.5 million were newly infected, and 680,000 died 4 . However, in the African region, for the same year, the number of newly infected people appears at 880,000 and deaths at 460,000, while in the Eastern Mediterranean region, new HIV infections are estimated at 41,000 and deaths at 17,000 5 . A Canadian study of refugee patients revealed an HIV prevalence of 2% 6 . That of Greece, conducted at the Greek-Turkish border among migrants and refugees, showed an HIV prevalence of 0.3% 7 .
Morocco is one of the few countries in the region that has launched a strong response to the HIV epidemic in recent decades 8 . In 2020, According to the most recent epidemiological surveillance data produced by the Ministry of Health's Directorate, the prevalence of HIV in the general population remains low and stable (0.08%), with an epidemic concentration among the major population groups most at risk of infection, including sex workers (1.7%), men who have sex with men (4.1%), people who inject drugs (7.1%), and immigrants (3.0%) 9 .
HIV is an epidemic concentrated in low-income countries and afflicting vulnerable populations. Migrants, refugees, and asylum seekers are the most affected, in addition to sex workers, men and women who exchange sex for money or goods, people in prison, men who have sex with men, and people who inject drugs. Migration can encourage several of these behaviors, pushing the migrant to join one of these groups with unprotected sexual intercourses. The migrant can thus serve as a bridge and facilitate the transmission of HIV to migrant populations and to the population of the host country 10 . In Morocco, to thwart the spread of sexually transmitted diseases and reduce the risks of epidemics linked to HIV, a circular from the Ministry of Health on monitoring the health of illegal migrants was launched in 2003. This circular authorizes access to care for migrants in an irregular administrative situation 11 . In 2010, the World Health Organization (WHO) encouraged the promotion of screening activities among people at risk and the management of positive cases 12 . Anonymous testing and free treatment, regardless of the legal status of migrants, are essential elements in responding to the "Leave No One Behind" policy, a policy refusing exclusion and fighting it 13 .
Integrating combination prevention with migrant, refugee, and asylum seeker populations into the response to HIV is a public health priority. It is a step towards considering migrants as a resource for the socio-economic development of the host countries and not as a burden. Investing in the health of migrants, refugees, and asylum seekers is a future investment in the health of the whole population. Assessing the level of knowledge of migrants, refugees, and asylum seekers about HIV infection and intercourse without condoms is essential to facilitate the formulation of preventive messages targeted at migrants living in Morocco and to end the HIV epidemic. Hence, the objective of our study is to describe the state of knowledge of migrants, asylum seekers, and refugees about HIV infection and to measure the prevalence of intercourse without condoms and its associated risk factors.

Methods
Study design and population. Oujda occupies a strategic geographical position in Morocco by overlooking Europe to the north and adjoining the Algerian border to the east, which attracts migrant populations 14 . It is one of the three main regions hosting refugees and asylum seekers 2 .
Between November and December 2021, we conducted a cross-sectional study among the sexually active migrant population that have ties with non-profit associations working to improve the health of migrants or the health of vulnerable people. We based the sampling on two stages. The primary unit brought non-profit associations together. The secondary unit was made up of migrants aged 18 and over, sexually active, present in Oujda on the day of the survey and having agreed to participate in the study. A random draw of the order numbers of the migrants was carried out to determine the secondary unit in each chosen primary unit. This method has accelerated the investigation and reduced costs. A simple random draw was used to select sixteen primary units. Each primary unit was made up of 24 people. We excluded pregnant women from the study.
A migrant has been defined as any person of foreign origin, with or without legal status in Morocco, regardless of their date of entry into the country and the more or less prolonged duration of their stay, or even installation 15 . The legal status of migrants was classified into four categories: (i) regular legal status with legal status in the host country; (ii) irregular legal status without legal status in the host country; (iii) asylum seekers who are seeking safety from persecution or harm in a country other than their own and awaiting a response to their refugee claim; (iv) and refugees who are unable or unwilling to return to their country of origin due to a well-founded fear of persecution on account of their race, religion, nationality, membership of a particular social group or opinion policies 16 . The same questionnaire was used and the same trained investigators were involved to limit the measurement bias. The participant received no remuneration due to the limited budget. Data collection was done in a closed room to ensure confidentiality and anonymity.
A rapid screening test for HIV used the HIV 1/2/O Tri-line Human Immunodeficiency Virus Rapid Test Device (Abon Biopharm) and/or self-reported HIV and the results were communicated on site. Participants who had positive HIV tests were referred to the referral center for infectious diseases present in Oujda for confirmation by Western blot tests. Confirmed HIV cases were treated. All treatments were free of charge for the participants 17 (Fig. 1

Data collection.
To collect data in relation to socio-demographic background, perception of the disease by the participant, behavioral habits, sexual behavioral habits, and para-clinical parameters, we used a standardized paper questionnaire during a face-to-face individual interview with the participant. The questionnaire was administered in arabic, french, spanish, or english, which corresponds to the main languages spoken by migrants in Morocco.

Operational definitions. HIV knowledge assessment.
We assessed knowledge about HIV through a 17item questionnaire to which the participant had to answer "yes" or "no". These items were grouped into three subgroups: eight questions on HIV symptoms, six questions on complications, and three questions on preventive measures. If the participant answered "no" to half of the questions in each subgroup, their knowledge of HIV was said to be unsatisfactory. Conversely, when the participant answered "yes" to half of the questions in each subgroup, he was considered to have The instrument's Cronbach's alpha was 0.86, indicating satisfactory internal consistency for the HIV knowledge assessment questionnaire.

Assessment of risk behaviors for HIV infection.
The assessment of HIV risk behaviors was carried out by asking questions about the behaviors adopted during the last six months preceding the survey. These behaviors are related to the consumption of alcohol, drug injections, and the fact of having benefited from a piercing or tattoo.
Assessment of high-risk HIV sexual behavior. We defined high-risk HIV sexual behavior as any intercourse with a casual or commercial sex partner without condom use. Participants were asked about their sexual identity, age at first sexual intercourse, number of sexual partners, difficulty obtaining condoms, practice of vaginal sex, and practice of anal sex.
Data management and statistical analysis. The precautionary measures to respect the confidentiality of the information collected and the anonymity of the participants were rigorously respected. The analysis was done with Epi Info version 7.2.0.1. All tests were two-sided and statistical significance was set at a p-value of less than 5%. Categorical variables were expressed as numbers and percentages, and continuous variables were expressed as mean and standard deviation. The proportions of categorical variables were compared using the chi-square test or Fisher's exact test, where applicable. Continuous variables were compared using the analysis of variance test or the Mann-Whitney test, where applicable. Multiple logistic regression was used to identify risk factors associated with high-risk HIV sexual behaviors as defined above, providing odds ratios (OR) and adjusted OR with 95% CI.   (Table 3).

Discussion
The long latency period of HIV infection in the population makes it difficult to master and control epidemics linked to this disease. Added to this, is the concentrated nature of the epidemic among at-risk groups who are stigmatized and difficult to identify. This stigma reduces access to preventive and curative services. Migrants are among the vulnerable populations at risk for HIV infection. This is a risk exacerbated by a shift in behavior, including sexual behavior, following liberation from relatively rigid societal norms. In our study, the prevalence of migrants who practice intercourse without condoms with a casual or commercial sex partner, a high-sexual risk behavior for HIV infection, was 72.8%. This prevalence was 43% in Kazakhstan in 2015, out of a sample of 422 migrants 18 and 43% of the 553 Mexican migrants with a recent stay in the border region between Mexico and the United States in 2016 in Tijuana, Mexico 19 .
In a study by Zhuang et al. in 2012 on a sample of 1625 migrants in China, young age was associated with high-risk HIV sexual behaviors 20 . This could be explained by the attitudes that young people have towards sexuality and the fact that young people agree to have sex with casual sex partners or in exchange for money 21 . In our study, age was not associated with high-risk HIV sexual behaviors.
Male gender is known to be a factor consistently associated with sexual behaviors that facilitate the transmission of sexual diseases. These behaviors include multiple sexual partners and casual sex or sex with sex workers 22 . The study of 1219 migrants in Mexico showed that married men who do not live with their spouses were more likely to have sex with a casual partner or a sex worker than their counterparts with their spouse 23 . This could be explained by the perception men have of sex. For these men, they assume they have the right to satisfy their sexual and emotional needs when separated from their spouse 24 . In our study however, male sex and marital status were not associated with practicing intercourse without condoms with a casual or commercial sex partner.While a study conducted on 17,377 migrants in China found no link between a low level of education and high-risk sexual behavior for sexually transmitted diseases 10 , our survey found a significant association. This low level of education could be associated with ignorance about HIV, its mode of transmission, and methods for its prevention.
Insufficient general knowledge about HIV is a risk factor associated with increasing the risk of engaging in intercourse without condoms with casual partners. The study conducted by Pan 25 . The literature also reports that migrants who know about prevention methods against sexually transmitted diseases such as HIV adopt safer sexual behaviors 21 . In our study, insufficient general knowledge about HIV was not a risk factor for having intercourse without condoms with casual partners. The difficulty of obtaining condoms was associated with high-risk sexual behavior among migrants in Morocco. This may be associated with difficulties obtaining sexual and reproductive health education as well as migrants' lack of knowledge of places where condoms are distributed for free.
Indeed, a South African study of 943 migrants found that having access to free condoms increased the likelihood of migrants using condoms 26 .
In the current survey, being homeless was listed as a risk factor for intercourse without condoms with casual partners. Indeed, the migratory experience can lead to the absence of a roof, a family, and friends and can engender a feeling of loneliness and a break in social ties to which are added the illegal or legal status, precarious living conditions, absence of work, and barriers to accessing basic services, aggravated by the discrimination of which migrants are victims. All of these conditions lead migrants to seek to compensate for deficits in material and emotional support through sexual behaviors such as intercourse without condoms with sex workers or casual partners 27 . The study by Desgrees du Loû and al. showed that migrants had more unprotected sexual relations during the years when they had no fixed address or irregular legal status 27 . Women, without housing or irregular legal status, were more likely to agree to unwanted sex in exchange for shelter or material support 27 . The precarious living conditions of migrants and the administrative instability in which they find themselves, at least in the first years of their arrival, generate latent anxiety with deleterious effects on their mental health 27 . The symbolic violence imposed by administrative procedures creates instability, insecurity, and situations of discrimination or Table 2. Knowledge, risk behaviors and sexual HIV behaviors among sexually active migrants, Morocco, 2021. sd standard deviation. For qualitative variables, the Pearson chi-2 test estimated the association between the dependent variable and the independent variables when the conditions were valid. For the quantitative variables, we used a comparison test of two means; p-value was considered significant when it was less than 0.05. www.nature.com/scientificreports/ even harassment. It generates stress and anxieties that affect the health of migrants and expose them to sexuality and the risk of sexually transmitted diseases. The administrative stability marked by a legal status, including refugee status, leads to an increase in self-esteem and a feeling of belonging to the host country, which facilitates their integration and makes them capable of benefiting from basic services, including access to care and prevention methods against sexually transmitted diseases. In our survey, refugee status was a protective factor against intercourse without condoms with casual partners.

Limitations
Our study had certain limitations, including its cross-sectional nature, which makes it difficult to establish the causal relationship between exposure and the adoption of intercourse without condoms with casual partners. To which is added the prevarication bias encountered during the collection of data in relation to sexual behavior despite the guarantee of anonymity and the use of community actors during data collection. However, our study made it possible to meet its objectives by measuring the prevalence of migrants having intercourse without condoms with casual partners and proposing public health actions to prevent the spread of sexually transmitted diseases, including HIV.

Conclusion
The results of this research have important implications for maintaining and improving the health of populations in Morocco, especially with regard to human dynamics. After more than 30 years of experience in the fight against sexually transmitted diseases in Morocco, research on HIV among migrants is quasi-absent. The results of this survey show that the homeless, the difficulties of obtaining condoms, and the elementary education level are factors associated with high sexual behavior for HIV. Following these results, it is important to emphasize the need to increase HIV prevention among migrants by taking action on the social and ecological determinants by providing them with shelter and suitable living conditions. In addition, the establishment of community prevention programs against HIV would encourage migrants to adopt healthier and safer sexual behaviors, which would ensure their support for change.
It is important to make migrants aware of the importance of preventing HIV infection through the use of condoms as well as pre-exposure or post-exposure prophylaxis.

Data availability
All data generated or analyzed during this study are included in this published article.