The World Health Organization estimates 10.6 million new cases of syphilis occur each year with long-term consequences if untreated, particularly for the sexual and reproductive health of women.1 Studies conducted in Brazil indicate that STIs, particularly syphilis, constitute a serious public health problem among indigenous people. Although control of the disease is relatively more effective in the United States and Western Europe, the endemic rates of syphilis transmission have been stubbornly persistent in countries with limited resources in Latin America, Asia, and Africa.2 These regions also focus syphilis control on female sex workers, men who have sex with men, persons who inject drugs, and specific ethnic groups.3 South America ranks among the highest for incidence of syphilis, accounting for 2.8 million of the annual global cases.4 Sexually transmitted infections among indigenous populations are also an emerging public health concern.5
Paraguay is a small South American country with a substantial indigenous population that may experience higher levels of poor reproductive health outcomes. According to the Third National Census of 2008, indigenous ethnic populations of Paraguay represent 1.7% of the total population or approximately 108,600 people.6 They have a high fertility rate, 6.3 children per woman, and low education level with 38.9% of the population older 14 years being illiterate.6 Furthermore, many indigenous communities have difficulty in accessing health care.7 Indigenous populations may be at particular risk for syphilis because they are geographically and socially marginalized and receive little information on STIs in their own languages.
There are few scientific studies on STIs in indigenous populations in Paraguay and in the world, making it difficult to understand the magnitude of the problem and the vulnerability of these populations to these infections.8,9 The present study builds on a previous survey which found syphilis prevalence at 9.5% in 3 geographical areas that included indigenous populations.10 Despite representing a small segment of the population of Paraguay, indigenous populations may experience higher burden of STIs while being excluded from the prevention and treatment services due to inequity of access to universal health care. The aim of the present study was therefore to determine the prevalence of syphilis and its associated risk factors in several distinct populations of indigenous women in Paraguay.
MATERIALS AND METHODS
Study Design and Population
This study was a cross-sectional survey to measure the prevalence of syphilis among indigenous women in Paraguay, South America, in 2016. The country of Paraguay has approximately 7 million inhabitants divided into 2 major regions, Oriental and Occidental. There are 5 distinct language families spoken by indigenous persons: Guaraní, Maskoy, Mataco, Guaicurú, and Zamuco. These languages families comprise 112,848 persons, including 54,473 women, distributed in 493 communities according to the Paraguayan census.6
The survey used a multistage, probabilistic design to approximate a representative sample based on the Third National Census.6 The first stage stratified the country into 10 areas by the 2 geographic regions and 5 languages families. From each stratum, a random sample of communities was selected with probability proportionate to size. Within the selected communities, all women age 15 to 49 years old were eligible and invited to participate in a brief interview and provide a sample for syphilis testing. The number of communities selected was based on an a priori sample size calculation of 1734 gauged to measure syphilis prevalence at approximately 6% ± 1.2% accounting for 15% nonresponse. In the survey, 1732 eligible women provided specimens to syphilis testing, although nonresponse rates for sensitive questions on sexual behavior ranged from 9.1% to 16.1%.
Data Collection and Informed Consent
Before data collection, a consultative process was carried out with leaders from the communities selected. This process consisted of presenting the proposal to the leaders and traditional authorities of each community. The visit was made with the support of an “interculturality consultant” to help translate the indigenous worldview approach and adequately communicate the principles of informed consent. After obtaining permission at the community level, field workers bilingual in Spanish and each of the 5 language groups were employed to translate the consent process, interviews, counseling, and referrals to treatment. After obtaining written informed consent, a face-to-face interview following a structured questionnaire was done and a blood sample was obtained. For women aged 15 to 17 years, informed consent of the parents or guardians was obtained and the assent of the minor. The questionnaire was adapted from an instrument used for repeated surveys of human immunodeficiency virus (HIV)-related behavior developed by Family Health International.7 The current study focuses on demographic factors, including language, family, and hypothesized sexual risk factors for syphilis, including age of initiation of sex, number of sexual partners, alcohol use, and transactional sex (defined as exchanging sex for money, goods, or other needs).
A rapid test for syphilis antibodies was done on site within the indigenous communities. Additionally, a blood sample was drawn for confirmation of syphilis reactivity and quality control. Specimens were transported to the HIV/acquired immune deficiency syndrome/STI National Program reference laboratory in the capital, conserved at 2°C to 8°C. The test to detect antibodies against Treponema pallidum was performed using the rapid treponemal test (Advanced Quality Intec Products, Inc., Xiamen, China), followed by the Venereal Disease Research Laboratory (VDRL) test (Wiener, Wiener Laboratories SAIC, Rosario, Argentina). Our classification to define a syphilis case for analysis followed the Paraguayan national guidelines for screening and treatment of populations in the context of eliminating congenital syphilis and in the context where follow-up may be difficult and as in previous local studies.10–12 Syphilis cases were rapid test positive plus a VDRL dilution equal to or greater than 1:4, or if the VDRL was 1:1 to 1:4 with a positive TPHA (HUMAN, Diagnostics Worldwide). Information about prior syphilis was also included in the interview.
The ethical principles of confidentiality, equality, and fairness were respected. The signing of an informed written consent was requested and in the case of those younger than 18 years, authorization was requested of the parent or guardian along with assent of the minor. The research protocol of the study was approved by the Committee of Ethics in Research, of the Institute of Tropical Medicine under the protocol 117/2016. All syphilis-positive cases were referred to the national HIV and STI treatment network (PRONASIDA, for its acronym in Spanish) and its affiliated clinics for treatment and corresponding follow-up.
Analysis is descriptive and analytic. The primary measure of interest was the prevalence of syphilis as defined above, overall, and within each of the 5 language families. Associations between syphilis and demographic and risk behaviors were examined using the χ2 test for differences in proportions. P values less than 0.05 were considerate statically significant. Analysis was done using STATA 14.0 (Stata Corporation, College Station, TX).
A total of 1732 indigenous women enrolled in the study; all women who were invited completed the interview and syphilis testing. A large proportion (44.5%) were aged 15 to 24 years; 25.8% were teenage women age 15 to 19 years (Table 1). The distribution of women in the 5 language families were: Guaraní (53.7%), Maskoy (20.8%), Mataco (16.9%), Guaicurú (6.2%), and Zamuco (2.5%).
Table 1 presents sexual risk behaviors among women who responded to these questions. Sexual debut was young, with 61.3% reporting first vaginal intercourse by 14 years or younger. Over 1 (11.5%) in 10 reported multiple sexual partners (2 or more) in the last year, with 4.7% reporting multiple partners in the last month. Alcohol use at last sex was reported by 11.5%; exchanging sex for money, goods, or other needs was reported by 2.0% of women.
Overall, 117 cases were classified as syphilis-positive among the 1732 indigenous women participants, resulting in an overall prevalence of 6.8% (95% confidence interval [CI], 5.6–8.0). Of note, 38 (2.2%) were TPHA-positive with VDRL reactivity of 1:1. Prevalence did not vary significantly by age, education, region, age of sexual debut, number of partners in the last month, and alcohol use during last sexual episode. Syphilis prevalence did vary by language family/ethnic group (P = 0.010), with Mataco having the highest prevalence (8.2%; 95% CI, 5.3–11.9) and Maskoy having the lowest (2.5%; 95% CI, 1.1–4.7). Women reporting multiple partners in the last year had significantly higher prevalence of syphilis (11.3%; 95% CI, 6.9–17.1). Transactional sex in the last year was associated with the highest prevalence of syphilis of any variable examined (18.7%; 95% CI, 7.2–36.4; P = 0.010). In multivariate analysis, transactional sex and language group remained significantly associated with syphilis.
The prevalence of syphilis in indigenous women in our survey in Paraguay was high. About 1 in 15 women in a population-based survey had evidence of syphilis. We also demonstrated variation in syphilis across the different languages family populations, with elevated levels among Mataco, Guaicurú, and Guaraní groups. According to a previous study in Paraguay, in 2013, the prevalence of syphilis among parturient women in areas with high numbers of indigenous persons was 4.41%12; our higher estimate in the current study of 6.8% suggests a worrisome increase. Even compared with other indigenous populations in the region, the prevalence of syphilis in this study is high. For example, a large survey of indigenous people in Brazil found prevalence of syphilis at 1.82%.13 Our figure is also high compared with syphilis prevalence among pregnant indigenous women (1.60%) in Peru.14
Our study corroborates transactional sex and multiple partners as risk factors for syphilis as noted elsewhere in the region and globally.15–17 We recognize that the conceptualization of transactional sex varies according to cultural contexts. In indigenous communities, the practice may be related to the acquisition of food or other goods, differentiated from “sex work” as a primary source of cash income. The context may also include boyfriends, friends, and other acquaintances as the negotiators of the transaction with the exchange being implicit while not formally agreed upon.18,19
Studies of STIs among indigenous populations have suggested low knowledge and poor access to prevention play a role in the increased vulnerability. In the Peruvian study noted above, knowledge of any preventive measure showed a protective role.14 According to a study in the indigenous population in Paraguay, only slightly over one third of indigenous women reported using any preventive practice.20 Researchers in Brazil point to vulnerability to STIs among indigenous people stemming from social inequalities, cultural oppression, and interethnic friction in a complex sociopolitical environment.13 We believe these same factors may pertain to the indigenous population of Paraguay and merit closer examination.
The findings of this study should be interpreted in light of the following limitations. First, the level of missing data or refusal to answer sensitive questions was high, ranging from 9.1% for alcohol use with sex to 16.1% for multiple partners. We posit there is likely underreporting of these factors due to social desirability response bias. Our study also suffers from small sample size and sufficient power for analyses within language groups. We believe that our findings are not consistent with endemic nonvenereal treponemal infections in Paraguay with respect to age-specific prevalence and associations with sexual behaviors.
Despite these limitations, our study provides evidence of high prevalence of syphilis among indigenous populations who may be marginalized in Paraguay and elsewhere in the region. Our data provide support for improved programs and active interventions, such as partner notification and large-scale screening for syphilis. Variation by languages groups may help target the latter interventions. Broader education on reducing the number of partners and harm reduction with transactional sex are also needed in the appropriate languages. Finally, research is critically needed among indigenous populations throughout the world, as they are an especially vulnerable group, suffering from ongoing colonialization, racism, social exclusion, and the lack of political self-determination—factors which frame structural determinants of disparities in indigenous health.21
1. World Health Organization. Strategies and laboratory methods for strengthening surveillance of sexually transmitted infection. Switzerland: WHO, 2012.
2. Loureiro MDR, Cunha RV, Ivo ML, et al. Syphilis in pregnancies and vertical transmission as a public health problem. Rev Enferm UFPE on line 2012; 6:2971–2979.
3. Kitayama K, Segura ER, Lake JE, Perez-Brumer AG, Oldenburg CE, Myers BA, et al. Syphilis in the Americas: A protocol for a systematic review of syphilis prevalence and incidence in four high-risk groups, 1980-2016. Syst Rev [Internet] 2017; 6:195. Available from: http://www.ncbi.nlm.nih.gov/pubmed/29017552
4. Ortayli N, Ringheim K, Collins L, et al. Sexually transmitted infections: Progress and challenges since the 1994 International Conference on Population and Development (ICPD). Contraception 2014; 90:S22–S31.
5. Minichiello V, Rahman S, Hussain R. Epidemiology of sexually transmitted infections in global indigenous populations: Data availability and gaps. Int J STD AIDS 2013; 24:759–768.
6. General Directorate of Surveys, Statistics and Census: Main results EHI / 2008. Survey of indigenous homes. 2008. Available from: http://www.dgeec.gov.py/Publicaciones/Biblioteca/EHI2008_Boletin_Principales%20Resultados/EHI%202008.pdf
Accessed July18, 2018.
7. Amon J, Brown T, Hogle J, et al. Encuestas de Vigilancia del Comportamiento EVC. Directrices para encuestas del comportamiento repetidas en poblaciones en riesgo al VIH. In: Family Health International. 2000.
8. Carvalho NS, Cho R, Flores LP. DST em populações indígenas no Brasil: Análise crítica e revisão da literatura. DST J Bras Doenças Sex Transm 2011; 23:142–145.
9. Domingues RMSM, Szwarcwald CL, Souza Júnior PRB, et al. Prevalência de sífilis na gestação e testagem pré-natal: Estudo Nascer no Brasil. Rev Saude Publica 2014; 48:766–774.
10. Ministerio de Salud Publica y Bienestar Social. Informe Situación Epidemiológica del VIH Paraguay 2016 [Internet]. 2016 [cited 2018 Mar 20]. Available from: http://www.pronasida.gov.py/images/documentos/inf.epi.vih.2016.pdf
11. Ministry of Public Health and Social Welfare (MSP and BS), National HIV / AIDS / STI Control Program. Guía Clínica para la Eliminación de la Transmisión Materno infantil del VIH y de la Sífilis Congénita en el Paraguay 2016–2017. Asuncion, Paraguay, 2011.
12. Ministry of Public Health and Social Welfare (MSP and BS), National HIV / AIDS / STI Control Program. Report on the epidemiological situation of HIV AIDS and syphilis Paraguay/Internet. MSP and BS 2013; Available from: http://www.mcp.org.py/documentos/situacion_epidemiologica1314.pdf
. Accessed July18, 2018.
13. Benzaken AS, Sabidó M, Brito I, et al. HIV and syphilis in the context of community vulnerability among indigenous people in the Brazilian Amazon. Int J Equity Health 2017; 16:92.
14. Ormaeche M, Whittembury A, Pun M, et al. Hepatitis B virus, syphilis, and HIV seroprevalence in pregnant women and their male partners from six indigenous populations of the Peruvian Amazon Basin, 2007–2008. Int J Infect Dis 2012; 16:e724–e730.
15. Galban E, Benzaken A. Situación de la sífilis en 20 Países de Latinoamérica y el Caribe: año 2006. DST J Bras Doenças Sex Transm 2007; 19:166–172.
16. Hernández CA, Cruz A, Figueroa LJ, et al. Prevalencia y factores de riesgo asociados a sífilis en mujeres. Rev Saúde Pública 1998; 32:579–586.
17. Rouner D, Long M, Bubar R, et al. Communication about sexually transmitted infections among rural and urban native American youth. Howard J Commun 2015; 26:172–192.
18. Wamoyi J, Stobeanau K, Bobrova N, et al. Transactional sex and risk for HIV infection in sub-Saharan Africa: A systematic review and meta-analysis. J Int AIDS Soc 2016; 19:20992.
19. Bamgboye EA, Badru T, Bamgboye A. Transactional sex between men and its implications on HIV and sexually transmitted infections in Nigeria. J Sex Transm Dis 2017; 2017:1810346.
20. Alfonso RM, Paiva CL, Giselle M, et al. Conocimientos, Actitudes y Prácticas sobre Prevención de Sífilis y VIH de Indígenas, Distrito Dr. Juan Eulogio Estigarribia, año 2014. Med Trop 2016; 35.
21. Rios-Gonzalez CM. Evaluation of the scientific production on HIV in indigenous people, from 1989 to 2016. Travel Med Infect Dis 2017; 18:83–84.