Sexually Transmitted Diseases:
Prevalence and Risk Factors for Chlamydia trachomatis Infection Among Young Thai Men in 2008–2009
Jatapai, Anchalee PhD*; Sirivongrangson, Pachara MD, MPH†; Lokpichat, Somchai MSc†; Chuenchitra, Thippawan PhD‡; Nelson, Kenrad E. MD§; Rangsin, Ram MD, MPH, DrPH¶
From the *Research and Development Office, Phramongkutklao College of Medicine, Bangkok, Thailand; †Bureau of AIDS/TB/STIs, Department of Disease Control, Ministry of Public Health, Bangkok, Thailand; ‡Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand; §Department of Epidemiology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD; and ¶Department of Military and Community Medicine, Phramongkutklao College of Medicine, Bangkok, Thailand
The authors acknowledge the collaboration of the military hospitals, the Royal Thai Army, and all participants. The authors thank COL Chaiyaphruk Pilakasiri and CPT Wes McCardle for reviewing the manuscript.
Supported by the National Institute of Health (No. 5R01TW006972-04) and Ministry of Public Health, Thailand.
Conflict of interest: The authors have no conflicts of interest to declare.
Correspondence: Ram Rangsin, MD, MPH, DrPH, Department of Military and Community Medicine, Phramongkutklao College of Medicine., 315 Ratchawithi Rd, Ratchathewi, Bangkok 10400, Thailand. E-mail: firstname.lastname@example.org.
Received for publication May 18, 2012, and accepted November 2, 2012.
Background: Asymptomatic Chlamydia trachomatis (CT) infection and other sexually transmitted infections in men potentially contribute significantly in sustaining the spread of the infection. To describe the distribution and related sexual behaviors, we conducted a cross-sectional study among young Thai men using a (1:30) systematic sampling of all newly inducted military conscripts in Thailand.
Methods: In November 2008 and May 2009, participants’ urine and serum samples were tested for CT and Neisseria gonorrhoeae, using a multiplex polymerase chain reaction technique, and serologic testing for Treponema pallidum and HIV-1 was done. Information on demographic data and risk behaviors was obtained by a self-administered questionnaire.
Results: The overall prevalence rates of CT, N. gonorrhoeae, HIV-1, and syphilis infection were 7.9%, 0.9%, 0.5%, 0.05%, respectively. The risk factors for CT infection were living in the upper north region (adjusted rate ratios [95% confidence interval], 2.13 [1.39–3.26]), having had 4 or more sexual partners (2.14 [1.48–3.09]), graduation from a vocational school (1.66 [1.14–2.41]), inconsistent condom use (1.48 [1.05–2.08]), unemployment (1.82 [1.06–3.12]), and age 21 years or younger (1.63 [1.01–2.63]).
Conclusions: The prevalence of CT infection among young male military conscripts was high, especially among men from upper northern Thailand. Multiple sexual partners, graduation from a vocational school, inconsistent condom use, unemployment before the military induction, and younger age were independently associated with the CT infection among young Thai men. These data will be useful to develop more effective public health interventions to prevent, detect, and treat sexually transmitted infections among young men in Thailand.
Sexually transmitted infections (STIs) including Chlamydia trachomatis (CT) infection remain an important global health problem in most countries, particularly in young populations.1 In 1999, the global estimated number of new cases of CT infection occurring each year was 92 million.1–3 Although CT infection is often asymptomatic,4 it can lead to serious sequelae, especially in women.5 Furthermore, infection with certain STIs including CT can increase the risk of acquisition and transmission of human immunodeficiency virus (HIV) by 2- to 5-fold in both women and men.6 Several studies have identified risks for CT infection, related to the complex interrelationship of sociodemographic and behavioral risk factors.7–10 Nevertheless, the core group at risk for CT infection are young men and women.9
Although the HIV epidemic in Thailand has been well characterized, there is less information about the prevalence of infection with other STIs and their related risk behaviors among young adults. Our previous study in 1991 to 1993 showed that the incidence of nongonococcal infection among young Thai men was 3.9 per 100 person-years, which was acquired through sexual contact with female sex workers and associated with other risks including inconsistent condom use, illicit drug use, and low education.11 C. trachomatis infection was more frequently observed among methamphetamine users (22%) in Thailand.12 The prevalence of CT was 2.8% among young Thai men who had graduated from vocational schools.13 From 1999 to 2002, the prevalence of CT infection in northern Thailand increased from 2.5% to 6.0% in adolescent boys and from 3.2% to 7.5% in adolescent girls.14 The increasing prevalence of STIs, especially CT infection, may indicate an increase in unprotected sexual intercourse, in a subset of both men and women in Thailand. Therefore, it is useful to identify potential risk behaviors among this core group of young generally healthy adult men to detect ongoing changes in high-risk sexual behavior, which may also impact these men at increased risk for HIV-1 infection.13,15,16
Our study aimed to determine the distribution and analyze epidemiologic risk factors for acquiring CT infection and other STIs among a sample of men. The recent STIs and sexual risk markers using the integrated behavioral and STIs biomarker information can provide current situation for STI-specific prevention and control programs.
MATERIALS AND METHODS
Men aged 21 years are selected for 2 years’ service in the Royal Thai Army (RTA) using a nationwide random lottery system. The lottery is held in April each year in the district of their family residence. Some exemptions are available for men with a handicap and a few other men. However, in general, nearly all men qualify and participate in the lottery selection. Approximately 1 in 10 (∼60,000) men are selected for service each year. Then, a half of them are inducted into the military service in May, and another half are inducted in November. Since 2001, the RTA began inducting some volunteers aged 18 to 20 years into the military. However, these relatively younger men comprise only approximately 10% to 15% of the cohorts of military conscripts. Those men older than 21 years were also lottery recruited after their delay conscription until graduation. Therefore, the military conscripts are a representative sample of all similar aged men, and their data can be generalized to the entire young male population of Thailand.
We conducted a cross-sectional study on men conscripted in November 2008 and May 2009 to determine the annual prevalence and recent risks for acquiring CT infection and other STIs, including Neisseria gonorrhoeae and syphilis. The study population was a systematic sampling (1:30) from the overall list of the new conscripts in each military camp who participated in the national HIV-1 sentinel serosurveillance program. Although HIV testing is voluntary (i.e., opt-out), participation in the screening at induction into military service is nearly 100%. Therefore, this study population consisted of both HIV-1–positive and HIV-1–negative men. Each participant signed an informed consent form and completed a questionnaire. No compensation was provided to participants.
A standardized self-administered questionnaire developed from the questionnaire used in the previous HIV-1 risk factor studies among Thai conscripts in 1991 to 1998,17–19 was used.
During the first 2 weeks of basic military training of the new conscripts in November 2008 and May 2009, we invited conscripts who were included on the list of the systematic sample to participate in the study after they attended a routine health education session on AIDS and STIs prevention. The sampled conscripts were guided through a self-administered questionnaire process. The questionnaires were sent to the Data Management Unit, Phramongkutklao College of Medicine in Bangkok, Thailand, for entry and analysis.
All participants agreed to submit sera for HIV and syphilis testing and urine samples for testing of gonorrhea and chlamydia infections. HIV antibody was evaluated by enzyme-linked immunosorbent assay (Murex HIVAg/Ab Combination; Murex Biotech Ltd, UK) for screening, and reactive specimens were repeatedly duplicated by Enzygnost Anti-HIV 1/2 Plus assay (Dade Behring Marburg Gmbh, Germany). Syphilis screening was performed using rapid plasma reagin (Newmarket Laboratories Ltd, Kenford, UK), and the reactive specimens were confirmed by the Treponema pallidum hemaglutination test (Serodia-TP; Fujirebio, Tokyo, Japan).
A small volume of first-void urine sample (10–20 mL) was collected and stored at 4°C to 8°C and then transported to the laboratory of Thailand Ministry of Public Health Bureau of AIDS/TB/STIs in Bangkok for CT and N. gonorrhoeae testing using a multiplex polymerase chain reaction test (Cobas Amplicor CT/NG; Roche Molecular Systems, Branchburg, NJ). The polymerase chain reaction sensitivity and specificity of CT test in urine samples have been reported to be 80% and 95.5%, respectively.20
Statistical analyses were performed using the STATA version 9.0 (StataCorp LP, College Station, TX). We evaluated the prevalence and risk factors for CT infection. Bivariate comparisons were made using χ2 test or Fisher exact test for proportion and the Student t test for continuous variables. To estimate the potential effect of various risk factors for CT infection, we constructed a Poisson regression model with robust variance to obtain unadjusted and adjusted prevalence rate ratios (RRs) and 95% confidence intervals (CIs). The criteria for selection of variables for a regression model were a P value less than or equal to 0.2 and other biologically relevant variables. The level of significant was set at P < 0.05.
Ethical Consideration and Treatment
The study protocol was reviewed and approved by the institutional review board of the RTA Medical Department. Written informed consent was obtained from the participants after they read the information sheet and the consent form. HIV voluntary counseling and testing were given to a cohort of conscripts by trained persons. Sexually transmitted infection–infectedand HIV-1–infected men received posttest counseling, treatment, and care at the military hospitals in accordance with the standard of STIs and HIV/AIDS treatment in Thailand.
Between November 2008 and May 2009, 2281 sampled young men were invited to participate, and 2123 (93.1%) men agreed and had completed questionnaires and acceptable test results. The participants were relatively homogenous in terms of age and sex. During the study period, sampled young men were 17 to 29 years old, with a mean (SD) age of 21.09 (±1.39) years and age at first sexual intercourse of 16.65 (±2.05) years. The sampled young men were sexually active (88.46%), single (71.79%), and mostly from the northeastern region of Thailand (35.80%), and almost 90% reported a history of alcohol drinking. Approximately half of them had 4 or more lifetime sexual partners. Almost half of them reported a history of illicit drug use (45.17%) including methamphetamine (34.43%), marijuana (23.39%), and Mitragyna speciosa (10.27%).
Overall, 191 (9.00%) of 2123 (95% CI, 7.81–10.29) young men had evidence of 1 or more STIs. The highest annual prevalence of STIs was CT infection (7.9%; 95% CI, 6.76–9.06), followed by N. gonorrhoeae (0.9%; 95% CI, 0.53–1.35), HIV-1 (0.5%; 95% CI, 0.18–0.76), and syphilis (0.05%; 95% CI, 0.00–0.26) (Table 1). The distribution of prevalence of CT infection is shown in Figure 1, and the sociodemographic risk factors are summarized in Table 2.
The risk behaviors for CT infection are shown in Table 3. Of the sexual characteristics, younger age (≤17 years) at first intercourse was significantly related to CT infection. The sexual risk behaviors significantly associated with CT infection were an increased number of lifetime sexual partners and having had 4 or more sexual partners in the past 6 months and sexual contact with friends, whereas sex with men was not significantly associated with CT prevalence (P = 0.360). Most young men (90%) were aware that condoms are effective in preventing STIs. The proportion of men who reported consistent condom use in the past 6 months with their wives was 39.48%; 77.77%, with causal partners/girlfriends; 97.45%, with sex workers; and 98.86%, with men. Sex without a condom was significantly associated with CT infection (RR, 1.68; 95% CI, 1.23–2.31). In addition, the proportion of condom use during the last sexual intercourse was lower among CT-positive young men. Illicit drug use and HIV-1 infection were not related to CT infection; however, 16.46% of sampled young men had ever used illicit drugs before sex.
Men who were conscripted from the upper northern region of Thailand infection had a higher prevalence of CT infection and reported more frequent sexual behavioral risks for STIs. A total of 28 (12.96%) of 216 (95% CI, 8.45–17.48) young men from this region had CT infection compared with 6.97% (95% CI, 5.79–8.16) among men from other regions. Condom use in the last 6 months was slightly lower (45.08%) among men from the upper northern Thailand, and inconsistent condom use in the last 6 months was related to CT infection (RR, 2.74; 95% CI, 1.15–6.51). The proportion of inconsistent condom use among CT-positive young men having had 4 or more female sexual partners was 42.86% (6/14) in this region. Young men who graduated from vocational schools were more likely to acquire CT infection (RR, 1.12; 95% CI, 0.50–2.52) than the others.
We evaluated multiple risk factors in a multivariate logistic regression analysis to evaluate independent risk behaviors for acquiring CT infection. The following factors were independently associated with CT infection: residence in upper northern Thailand for 2 years before conscription (adjusted RR, 2.13; 95% CI, 1.39–3.26), men who reported having had sex with more than 3 females in the past 6 months (adjusted RR, 2.14; 95% CI, 1.48–3.09), men who graduated from vocational school (adjusted RR, 1.66; 95% CI, 1.14–2.41), those who reported inconsistent condom use with noncausal girlfriends in the past 6 months (adjusted RR, 1.48; 95% CI, 1.05–2.08), and age 21 years or younger (adjusted RR, 1.63; 95% CI, 1.01–2.63).
The most frequent STIs among young Thai men in our study were CT infection. The prevalence of CT infection in this study was slightly less than the reported rates of nongonococcal infection among young conscripts in Northern Thailand in 1991 to 1993 (7.9% vs. 9.2%).11 However, a change in sexual practices over nearly 2 decades was observed. The proportion of male conscripts who reported that they were sexually experienced increased from 34% in 199021 and 48% in 1999 13 to almost 90% in this study. In addition, the proportion of sexual debut among young men 17 years or younger increased from 36.3% to 42% in 1993 to 1995 18 to 66.78% in this study.
Geographically, the prevalence of CT was higher in upper northern Thailand. This region had also experienced the most severe epidemic of HIV/AIDS in the 1990s.22 Our data are similar to previous studies in that the prevalence of STIs among young adults was higher among men from the upper northern provinces12–14 and lower in the southern provinces of Thailand.23 C. trachomatis infection among men living in the upper northern region may result from significant differences in sexual behavior among men from this region of the country.
The sexual behavior analysis in this study showed that the significant risk factors for acquiring CT infection were multiple sexual partners and inconsistent condom use among young men. The men who reported having 4 or more sexual partners in the past 6 months and inconsistent condom use had an increased prevalence of CT infection, which is similar to other studies.9,14 Multiple sexual partners and inconsistent condom use appeared to increase the risk for acquiring CT infection. Consequently, the risk-taking characteristics of sexual partners such as concurrent partnerships, frequency of sex, substance use, number of infected sex partners and duration of infectivity, inconsistent condom use, or social norms likely influence the transmission of CT and other STIs.24,25 Our data suggest that young adult men in Thailand are at high risk for CT infection and that the rate of CT may be increasing in the last decade in this population. Several factors may influence the sexual attitudes and behaviors among Thai teenagers, including ambiguous social roles, leading to confused identity, heightened sexual awareness and curiosity, key gaps in knowledge and life skills, limited parental input, impulsivity, and risk taking.26 We believe that it is useful to follow the prevalence of CT in this randomly selected population of sexually active young men. It is very difficult to obtain data from random populations of healthy sexually active populations of young men in most societies.
Our study has several limitations. First, the cross-sectional design of our study was unable to explicitly demonstrate that some of the sociodemographic and sexual behaviors preceded the CT infection. In addition, some of the questionnaire responses may be affected by recall bias and/or a social desirability bias for sexual risk behaviors.27 To minimize these potential limitations, the trained personnel informed the group of participants to skip some sensitive questions rather than recording incorrect responses in the questionnaire. Second, misclassification may have occurred from underreporting and overreporting of sexual experiences. However, there was only 1.79% (3/168) of men who were CT positive by polymerase chain reaction reported having had no sexual experience. Third, because most of the men were approximately 21 years old, the CT prevalence data cannot be applied to men of different ages from this study population.
In summary, our data indicate a high prevalence of CT infection among a population of healthy randomly selected young men in Thailand. Furthermore, the CT infection among these young men was associated with reports of multiple sexual partners and inconsistent condom use during sex. These data are of considerable public health concern because of the explosive HIV/AIDS epidemic, which affected Thailand during the past decade, which was controlled with the 100% Condom program and other public health programs to reduce high-risk sexual behaviors, especially those associated with commercial sex. These data suggest that unprotected sexual exposures among young men in Thailand may have been frequent, especially with noncommercial partners. Continued surveillance for CT prevalence coupled with behavioral questionnaires is needed to continue monitoring high-risk sex and STI transmission in this young male population in Thailand. This study also identified core groups of men who were at relatively higher risk for CT, namely, men with education at a vocational school and men from the upper northern provinces. Continued surveillance of these populations would be beneficial.
1. Sciarra JJ. Sexually transmitted diseases: Global importance. Int J Gynaecol Obstet 1997; 58: 107–119.
2. Gerbase AC, Rowley JT, Mertens TE. Global epidemiology of sexually transmitted diseases. Lancet 1998; 351: 2–4.
3. WHO. Global Prevalence and Incidence of Selected Curable Sexually Transmitted Infection. Overview and estimates. 2001.
4. Miller WC, Ford CA, Morris M, et al.. Prevalence of chlamydial and gonococcal infections among young adults in the United States. JAMA 2004; 291: 2229–2236.
5. Xu F, Schillinger JA, Markowitz LE, et al.. Repeat Chlamydia trachomatis infection in women: Analysis through a surveillance case registry in Washington State, 1993–1998. Am J Epidemiol 2000; 152: 1164–1170.
6. HIV prevention through early detection and treatment of other sexually transmitted diseases—United States. Recommendations of the Advisory Committee for HIV and STD prevention. MMWR Recomm Rep 1998; 31: 1–24.
7. Boyer CB, Shafer MA, Pollack LM, et al.. Sociodemographic markers and behavioral correlates of sexually transmitted infections in a nonclinical sample of adolescent and young adult women. J Infect Dis 2006; 194: 307–315.
8. Jennings J, Glass B, Parham P, et al.. Sex partner concurrency, geographic context, and adolescent sexually transmitted infections. Sex Transm Dis 2004; 31: 734–739.
9. Navarro C, Jolly A, Nair R, et al.. Risk factors for genital chlamydial infection. Can J Infect Dis 2002; 13: 195–207.
10. Nguyen TV, Van Khuu N, Thi Le TT, et al.. Sexually transmitted infections and risk factors for gonorrhea and chlamydia in female sex workers in Soc Trang, Vietnam. Sex Transm Dis 2008; 35: 935–940.
11. Celentano DD, Nelson KE, Suprasert S, et al.. Epidemiologic risk factors for incident sexually transmitted diseases in young Thai men. Sex Transm Dis 1996; 23: 198–205.
12. Celentano DD, Sirirojn B, Sutcliffe CG, et al.. Sexually transmitted infections and sexual and substance use correlates among young adults in Chiang Mai, Thailand. Sex Transm Dis 2008; 35: 400–405.
13. Paz-Bailey G, Kilmarx PH, Supawitkul S, et al.. Risk factors for sexually transmitted diseases in northern Thai adolescents: An audio-computer–assisted self-interview with noninvasive specimen collection. Sex Transm Dis 2003; 30: 320–326.
14. Whitehead SJ, Leelawiwat W, Jeeyapant S, et al.. Increase in sexual risk behavior and prevalence of Chlamydia trachomatis among adolescents in Northern Thailand. Sex Transm Dis 2008; 35: 883–888.
15. Cohen MS. Sexually transmitted diseases enhance HIV transmission: No longer a hypothesis. Lancet 1998; 351: 5–7.
16. Laga M, Manoka A, Kivuvu M, et al.. Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: Results from a cohort study. AIDS 1993; 7: 95–102.
17. Celentano DD, Nelson KE, Suprasert S, et al.. Risk factors for HIV-1 seroconversion among young men in northern Thailand. JAMA 1996; 275: 122–127.
18. Nelson KE, Celentano DD, Eiumtrakol S, et al.. Changes in sexual behavior and a decline in HIV infection among young men in Thailand. N Engl J Med 1996; 335: 297–303.
19. Nelson KE, Celentano DD, Suprasert S, et al.. Risk factors for HIV infection among young adult men in northern Thailand. JAMA 1993; 270: 955–960.
20. Palladino S, Pearman JW, Kay ID, et al.. Diagnosis of Chlamydia trachomatis and Neisseria gonorrhoeae. Genitourinary infections in males by the Amplicor PCR assay of urine. Diagn Microbiol Infect Dis 1999; 33: 141–146.
21. Sittitrai WPP, Barry J, Brown T. Thai sexual behavior and risk of hiv infeclion. A report of the 1990 survey of partner relations and risk of HIV infection in Thailand: Bangkok Program on AIDS. Thai Red Cross Society. 1992.
22. Brown T, Sittitrai W, Vanichseni S, et al.. The recent epidemiology of HIV and AIDS in Thailand. AIDS 1994; 8: S131–S141.
23. Chandeying V, Skov S, Duramad P, et al.. The prevalence of urethral infections amongst asymptomatic young men in Hat Yai, southern Thailand. Int J STD AIDS 2000; 11: 402–405.
24. Adimora AA, Schoenbach VJ. Social context, sexual networks, and racial disparities in rates of sexually transmitted infections. J Infect Dis 2005; 191: S115–S122.
25. Halperin DT, Epstein H. The role of multiple concurrent partnerships and lack of male circumcision: Implications for AIDS prevention. S Afr J HIV Med 2007; 8: 19–25.
26. Vuttanont U, Greenhalgh T, Griffin M, et al.. “Smart boys” and “sweet girls”—sex education needs in Thai teenagers: A mixed-method study. Lancet 2006; 368: 2068–2080.
27. Aral SO. Sexual behavior in sexually transmitted disease research. An overview. Sex Transm Dis 1994; 21: S59–S64.
© Copyright 2013 American Sexually Transmitted Diseases Association