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Abstract
Objectives Early sexual debut is a behaviour that has been associated with acquiring sexually transmitted infections. Higher schooling may delay sexual debut, thus the university population is categorised with low-risk sexual behaviours. The rate ratio of herpes simplex virus type 2 (HSV-2) seroincidence according to demographic characteristics and sexual behaviour was estimated for a cohort of university students.
Methods A dynamic cohort of university students was followed at the Autonomous University of Morelos, in central Mexico, during the years 2001–5. After obtaining informed consent, information was gathered annually regarding demographic characteristics and sexual behaviour and blood samples were obtained to determine HSV-2 antibodies. Seroincidence was estimated and the incidence rate ratio was evaluated using the Poisson regression model.
Results A total of 404 students participated, with 669.2 person-years of follow-up. An incidence of 4.2 cases per 100 person-years was estimated. The variables delayed sexual debut (≥18 years) and multiple sexual partners (two or more sexual partners during the past year) had a rate ratio of 4.1 (95% CI 1.2 to 14.3) and 2.5 (95% CI 1.1 to 5.6), respectively. Incidence for students with delayed sexual debut and multiple partners is estimated to be 10.3 cases per 100 person-years.
Conclusions Delayed sexual debut was a risk factor for acquiring HSV-2, due to a subgroup with sexual debut at 18 years of age or older that had multiple sexual partners; therefore, in the university population that tends to delay sexual debut, it is necessary to implement prevention programmes to promote the decrease of other risky sexual behaviours, as well as the promotion of the consistent use of condoms.
- College students
- delay sexual debut
- HSV-2
- seroincidence
- seroepidemiology, students
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Early sexual debut is a behaviour that has been associated with a variety of sexually transmitted infections (STI).1–4 This association has had different explanations that are not mutually exclusive: (1) biological: in women there is a predisposition to infections due to immaturity of the cervix5 6; (2) temporal: a longer period of exposure to different STI agents exists at an earlier age of sexual debut7; (3) conduct: early sexual debut has been associated with a greater number of sexual partners, the use of illicit drugs, alcohol and not using a condom.7–9 In Mexico, the median age for sexual debut among women with high school education or higher was 20.4 years compared with 18.2 years for women who did not complete elementary school.10 Research in poor urban areas found that attending school and achieving an educational level comparable with age are factors that delay sexual debut.11 In addition, to confirm the influence of age at sexual debut on the risk of acquiring STI, the use of biomarkers in longitudinal studies has been proposed.12 Herpes simplex virus type 2 (HSV-2), has been used as a biomarker for sexual behaviour at the population level.13 Studies conducted in Mexico on HSV-2 confirm its usefulness as a biomarker of sexual behaviour, including both high-risk and low-risk population groups.14 15 The objective of the present paper was to estimate HSV-2 seroincidence as well as to determine relative risk factors, demographics and sexual behaviour among a cohort of university students in Mexico, with particular emphasis on age at sexual debut.
Materials and methods
This study was approved by the internal review board of the National Institute of Public Health. Classes were visited to carry out the study at the Morelos State Autonomous University in Cuernavaca, Mexico, in the Schools of Medicine, Pharmacy and Psychology after obtaining authorisation and support from the authorities. A cohort design was employed to deal with the recruitment of new participants every year as well as with losses to follow-up normally expected in a student population. Baseline measurements were taken in the years 2001, 2002 and 2003 and follow-up was conducted during 2002, 2003 and 2005. No measurements were taken in 2004 due to a labour conflict at the university.
Before the start of the study a pilot with 100 subjects was conducted to standardise the methods followed. The research team visited each classroom and invited all students 18 years or older who were present to join the survey. During each measurement (baseline and follow-up) and after obtaining informed consent, an intravenous blood sample was drawn and self-completed surveys were administered regarding demographic characteristics and sexual behaviour. Baseline surveys contained information about first sexual relations, past sexual relations and lifetime sexual behaviour; follow-up surveys included information about past sexual relations and sexual behaviour during the past 12 months. The blood obtained was centrifuged, separating the serum and freezing it at −20°C until processing. The detection of HSV-2-specific antibodies was conducted using an established anti-HSV-2 (gG2) ELISA (IgG) method (Euroimmun, Lübeck, Germany), with 95.8% sensitivity and 86.1% specificity.16This test was employed in the National Health Survey performed during 2000 in Mexico.17 According to the manufacturer, the cut-off for negative samples was less than 0.8, and for positive samples it was 1.1 or greater. Samples between 0.8 and 1.1 were re-tested with the same ELISA, a value of less than 1.1 in the second ELISA rendered a negative result and a value of 1.1 or greater was finally positive.
The variable age at sexual debut was stratified into two categories based on the lower quartile for the variable age at sexual debut: early debut included students who had their first relations at the age of 17 years or younger and delayed debut included those initiating sexual life at 18 years or older. Multiple sexual partners was defined as students with two or more sexual partners during the past year, concurrent partners were students with two or more sexual partners in the same month, casual partners were individuals who had sexual intercourse with people they had just met. Time having known first relationship was evaluated by 1 day, 2 days to 1 week, 2 weeks, 3 weeks, 1 month, 2–3 months, 4–6 months, 6–12 months, 1–2 years, 3–5 years, 5 years or more, we stratified using the lower quartile: 1 day to 12 months and 1 year or more. Baseline demographic and sexual behaviour variables were stratified according to sex, and differences between women and men were evaluated with the χ2 test. The incidence of HSV-2 infection was estimated according to time, in person-years, that each individual contributed during the study. The incidence rate ratio of the variables analysed was calculated using the Poisson regression analysis with bivariate and multivariate models and 95% CI. The multivariate model was adjusted by sex, age, report of genital ulcers, sexual debut, sexual partners and condom use during the last sexual relationship, because these sexual behaviours are theoretically correlated with STI; the time variable used was the follow-up years. The statistical analysis was conducted using SPSS 10.0 and STATA 9.0 software.
Results
All the students invited to participate answered the survey, 368 in year 2001, 394 in year 2002 and 230 in year 2003, for a total of 992 subjects. From these, 705 were sexually active but 113 refused to provide the blood sample, thus the basal measurement was carried out with 592 college students who were sexually active. Basal HSV-2 seroprevalence was 2.2%, women had 2.8% and men 1.0% (OR 2.9; 95% CI 0.6 to 13.3); students 21 years old and older had 4.6% of HSV-2 infection and 0.8% among students 18–20 years old (OR 5.9; 95% CI 1.6 to 21.8); students with self-report of genital ulcers had 9.9% of HSV-2 and 1.3% without genital ulcers reported (OR 8.0; 95% CI 2.6 to 24.7). Students with delayed sexual debut had 2.1% of HSV-2 infection, students with early sexual debut had 2.4% (p=0.789).
The cohort study was conducted with 404 sexually active students who participated in at least two measurements and were HSV-2 seronegative at baseline, of whom 128 were men and 276 were women. Together, these students totalled 669.2 person-years of follow-up with an average of 1.7 years. The percentage of the population with early sexual debut (≤17 years) was 27.4% and 76.4% had multiple sexual partners (two or more during the past year). Characteristics such as age, marital status, tobacco consumption and self-reported history of genital ulcers did not show any difference between sexes, whereas men had higher percentages than women for characteristics related to risky sexual behaviour (table 1). During follow-up of the cohort, 28 new cases of HSV-2 infection were detected, resulting in an estimated incidence of 4.2 cases per 100 person-years (95% CI 2.7 to 5.7); women had an incidence of 4.5 per 100 person-years (95% CI 2.6 to 6.4) and men 3.4 per 100 person-years (95% CI 0.9 to 6.0); this difference was not statistically significant (p=0.518).
Sociodemographic variables and sexual behaviour in the cohort of university students, stratified by sex
The multivariate analysis (table 2) showed that the university students who had delayed sexual debut had nearly a four times greater rate ratio of HSV-2 infection than those with early sexual debut (RR 4.1; 95% CI 1.2 to 14.3). Students with multiple sexual partners presented a 2.5 times greater rate ratio of infection compared with those with only one sexual partner (RR 2.5; 95% CI 1.1 to 5.6). When stratifying HSV-2 incidence by age at sexual debut and number of sexual partners (table 3), it was observed that students who had early sexual debut and one partner during the past year presented an incidence of 0.9 cases per 100 person-year, whereas students with delayed sexual debut and multiple sexual partners had an incidence of 10.3 cases per 100 person-years. This subpopulation, with late sexual debut and multiple partners, was the same age as the rest of the population (21.17 vs 21.21; p=879), but presented risky behaviours according to the following indicators: tobacco consumption (60% vs 33.89%; p<0.001), cocaine consumption (8.5% vs 1.7%; p<0.001), history of STI (42.0% vs 24.0%; p=0.001), having known last sexual partner less than 1 year (45.7% vs 27.0%; p<0.001), casual partners (40.8% vs 11.4%; p<0.001), concurrent partners (41.2% vs 8.8%; p<0.001), not using condoms (49.3% vs 37.0% p<0.043) and use of emergency contraception (14.3% vs 5.9%; p=0.008).
Risk factor for HSV-2 infection in the cohort of university students
HSV-2 incidence rate in the cohort of university students, stratified by age at sexual debut and sexual partners during the past year
Discussion
Early sexual debut has been widely associated with a variety of STI; nevertheless, research exists that does not report information about sexual debut and the incidence of HSV-2,18–24 and few longitudinal studies on HSV-2 have found such associations.25 26 In a New Zealand cohort a greater incidence of HSV-2 was found in individuals with sexual debut at the age of 13 years or younger,25 but multivariate models were not conducted to eliminate the effect of potential confounding factors such as the use of condoms and the number of sexual partners. A study of bar and hotel workers in Tanzania found that women with sexual debut at the age of 20 years or less had six times more risk of acquiring HSV-2 than those with debut at 21 years or older.26 Contrary to expectations, individuals in the cohort of university students in Cuernavaca, Mexico, who had delayed sexual debut had a four times greater relative risk of HSV-2 infection; this greater risk is due to a subgroup with delayed debut and multiple sexual partners that also presented other high-risk behaviours (use of legal and illicit drugs, not using condoms, casual and concurrent partners). Therefore, delayed sexual debut among individuals with higher schooling10 11 27 was not sufficient to avoid high-risk sexual behaviours.12 Primary prevention of STI has been described as emphasising three factors (ABC strategy): delayed sexual debut (abstinence); be faithful (reduced number of sexual partners) and the use of condoms.28 Therefore, although in the university sample studied there was spontaneous delayed sexual debut, intervention steps must be taken that primarily focus on reducing the number of sexual partners.29 Early sexual debut has been associated with STI in older adolescents (18 years of age) but not in young adults (24 years of age), thus it has been suggested that delayed sexual debut has little impact on the acquisition of STI over the long term,12 as may possibly be the case among the students analysed in this study.
The cohort of university students in this work is not the only group for which delayed sexual debut is not a protective factor for STI. A study in Zimbabwe found that men with delayed sexual debut (≥21 years) were more likely to be HIV positive, this subgroup reported inconsistent use of condoms.8 Similarly, in the Mexican university population analysed it was found that students with two sexual partners and delayed debut used a condom 49.4% of the time in their last relationship, which was less than 66.2% reported for students with two sexual partners and early debut, a statistically significant difference (p=0.0357). Students with more risky sexual behaviour used a condom more often.
The number of sexual partners has been described to be the primary risk factor in the acquisition of STI; a greater number of sexual partners represents a greater probability of finding an infected partner.30 Among the women in the New Zealand cohort, those with six or more sexual partners had three times more risk of infection than women with one or no sexual partner,25 and the risk was similar to that found among students in Cuernavaca, although in our case for two or more sexual partners. Among men who worked in a factory in Zimbabwe, those who had between two and four sexual partners presented 1.3 times more risk of infection than those with one or no sexual partners,22 less of a risk than that found for students analysed in Morelos. In the Cuernavaca cohort, students with multiple sexual partners had more than twice the risk of acquiring HSV-2; however, 17 of 28 new cases detected were among students with one sexual partner during the past year, and no high-risk factor for the acquisition of HSV-2 was found in this subpopulation (data not presented). Future studies thus need to explore more fully the sexual behaviour of sexual partners in this monogamous population, who might actually be those having risky behaviours.
The incidence of HSV-2 in the university student population addressed is high considering their low-risk behaviour and schooling level, and was exclusively associated with delayed sexual debut and having multiple sexual partners. As delayed sexual debut is apparently not sufficient to avoid HSV-2 acquisition and maybe other STI, a decreased number of sexual partners and consistent use of condoms could be promoted.
Key messages
HSV-2 incidence among Mexican college students analysed was 4.2 cases per 100 person-years.
Students with delayed sexual debut and multiple sexual partners had 10.3 HSV-2 cases per 100 person-years, this subgroup showed other risky sexual behaviours.
Delayed sexual debut is not sufficient to avoid HSV-2 acquisition and probably other STI.
References
Footnotes
MASA was the recipient of a doctoral scholarship CONACyT 130569.
Funding This work was supported by the National Institute of Public Health. Grant 88-6235.
Competing interests None declared.
Ethics approval This study was conducted with the approval of the National Institute of Public Health from Mexico.
Provenance and peer review Not commissioned; externally peer reviewed.