Nelson, Amy MD*; Press, Natasha MD†; Bautista, Christian T. MSc‡¶; Arevalo, Jorge MD§; Quiroz, Carol‖; Calderon, Maritza**; Campos, Kalina**; Bryant, Amy¶; Shantz-Dunn, Julianna¶; Dahodwala, Nabila¶; Vera, Mario‖¶; Vivar, Aldo MD‖; Saito, Mayuko MD, MPH¶††‡‡; Gilman, Robert H. MD¶††
SEXUALLY TRANSMITTED INFECTION (STI) REPRESENTS a major global health concern with the majority occurring in developing countries; Latin America and the Caribbean account for over 10% of new cases.1 STIs are now widely recognized as a risk factor for the transmission of HIV because they share the same major modes of transmission and the same high-risk behaviors.2 Successful early diagnosis, treatment, and prevention of STIs could lead to a significant decrease in HIV infection in developing countries.3,4
Most epidemiologic studies of heterosexual transmission of STIs have focused on women, and only a few studies have been performed to study the transmission of STIs in heterosexual couples.5,6
Abstinence, mutual monogamy, and condom use are 3 strategies recommended to reduce risk of STI transmission in heterosexual populations.6 Women in stable relationships often do not insist on condom use with their partners because they consider themselves at low risk of acquiring an STI and do not want to “accuse” their partner of infidelity.7 Often, however, their male partners are having sex with other females or males, thus placing the stable female partner at higher risk.8,9 Although women tend to be more monogamous than their male partners, married women who are not monogamous have low rates of condom use during sexual relations with noncohabiting partners, a behavior that increases the STI risk of their stable male partner.10,11
Up to one fourth of female commercial sex workers (CSWs) have a diagnosis of an STI.12–15 Prevalence of HIV has remained low at <1% among general populations in Peru.12,16 In contrast, the HIV prevalence among men who have sex with men (MSM) has been estimated to range between 8% and 23%.11,17,18
This study was conducted in Lima, Peru, to determine the prevalence of STIs (chlamydia, gonorrhea, trichomoniasis, herpes simplex virus [HSV], syphilis, mycoplasma, and ureaplasma) in heterosexual couples without HIV. In addition, we determined potential risk factors associated with these infections. Because of high-risk sexual practices in men and low condom use in men and women in this population, we also expected to find an elevated prevalence of concordant STIs within couples in which one partner was infected with one or more STIs.13,19
Materials and Methods
This epidemiologic study was performed at 2 main hospitals in Lima, the capital city of Peru. The first hospital, Arzobispo Loayza Hospital, is an urban public hospital and serves a largely female patient population. The second hospital, Hospital Dos de Mayo, is a large general and specialty university teaching hospital situated in downtown Lima. Both hospitals function under the Ministry of Health (MoH) and serve the general lower to middle socioeconomic population, which lives in nearby districts and in the Lima metropolitan area. Both of these hospitals have outpatient sexually transmitted disease (STD) clinics.
Subjects who visited one of the STD clinics from February 2001 to March 2003 were invited to participate in this study. If a patient attended the clinic alone without his or her partner, he or she was asked to return with their stable partner to be included in the study. A stable partner was defined as a spouse, a cohabiting partner, or a partner with whom the participant had regular sexual intercourse without financial compensation for at least a 3-month time period. All subjects were included in the study after providing written informed consent. Exclusion criteria were the following: age <18 or >60 years, known HIV-positive status, homosexual couple, treatment with antibiotics within the last 7 days, currently menstruating at the time of presentation, and no history of sexual intercourse in the past 3 months. Baseline demographic and clinical information, as well as sexual and other risk behaviors, were collected by direct interview from each partner using a standardized questionnaire. All participants were interviewed privately without their partner present. A focused physical examination was performed by a trained healthcare worker and included inspection of the pharynx, external genitalia, and anus. In addition, female patients had a pelvic examination, including both speculum and bimanual examination. Patients were initially treated based on syndromic management, but if the results showed another infection that was not treated, they were then offered further treatment according to MoH guidelines. All patients received counseling and education regarding prevention of STIs.
In this study, a “case” was defined as an individual with a newly diagnosed STI of chlamydia, gonorrhea, trichomoniasis, HSV, syphilis, mycoplasma, or ureaplasma. A “control” was defined as an individual in whom no STI was diagnosed. Women with bacterial vaginosis and candidiasis were included in the control group. Newly diagnosed HIV cases and their partners were also excluded from the analysis. To determine potential risk factors associated with STI prevalence and acquisition within heterosexual couples, an unmatched case-control study was performed.
Study protocols were approved by the Institutional Review Board in each hospital, the Asociación Benéfica PRISMA, Lima, Peru, and the Johns Hopkins School of Hygiene and Public Health, Baltimore, Maryland.
Specimen Collection and Laboratory Testing
Clinical specimens included pharyngeal and rectal swabs as well as a clean-catch urine sample and serum samples. Vaginal and endocervical swabs were obtained from female participants, and urethral swabs were collected from male participants. Any genital lesions detected during clinical examination were also tested. Polymerase chain reaction (PCR) testing was performed on all specimens for Chlamydia trachomatis,20,21 Neisseria gonorrhoeae,22 Trichomonas vaginalis,23 HSV,24 Mycoplasma genitalium,25 and Ureaplasma urealyticum.26 All samples for PCR were collected in HCl (0.01 mol/L) buffer. Specimens were stored at 4°C and were transported and tested at the Universidad Peruana Cayetano Heredia laboratory. For the detection of N. gonorrhoeae, in addition to PCR, specimens were cultured on Thayer Martin media at the time of collection and incubated in 5% CO2 at 37°C for 72 hours. Positive N. gonorrhoeae cultures were confirmed using an oxidase test. Gram stains were performed on all vaginal, cervical, and urethral specimens. Specimens for T. vaginalis were cultured in 7 mL Diamond media and incubated at 37°C for 24 to 48 hours. Bedside testing, including pH, whiff test, and wet-mount, was performed on all vaginal samples. Syphilis testing was performed using the rapid plasma reagin test (Immunotrep; Omega Diagnostics, Clacks, U.K.) on serum samples as per the manufacturer. Serum samples were tested for antibodies against HIV-1 by enzyme-linked immunosorbent assay (Genscreen plus HIV Ag-Ab; Bio-Rad, Marnes la Coquette, France) and reactive samples were confirmed with a Western blot test (HIV-1/2; Abbott Laboratories, Abbott Park, IL).
χ2 or Fisher exact test was applied to compare differences in categorical variables between case and control groups. The Mann-Whitney U test was applied to compare differences in continuous variables. Univariate and multivariable logistic regression analyses were performed to compare social and behavioral factors between case and controls. Odds ratios (ORs) were adjusted for age, education level, age at first sexual intercourse, and marital status in the multiple logistic regression analysis. For women’s risk factors, significant ORs were further adjusted for having a partner who is men having sex with men (MSM). Subanalyses were performed for the following groups: excluding MSM for men’s analysis, excluding ureaplasma infection from STI criteria, including only ureaplasma infection as an outcome, and comparing concordant (having the same pathogenic infection within a couple) and discordant infection. Demographic and behavioral factors were compared within groups of high and low condom use and between MSM and non-MSM. All P values were 2-sided. All statistical analyses were performed using Stata 8.0 (Stata Corp., College Station, TX).
Four hundred forty-one individuals (126 couples [126 men and 126 women], 84 men, and 105 women) who met the inclusion criteria were recruited during the study period, of whom 244 individuals (122 couples) accepted participation in the study, 75 individuals accepted to return to the clinic with their respective partners, and 122 (25%) individuals or their partner refused to participate and therefore were excluded from the study. After screening, 2 men were newly diagnosed as having HIV infection and the couple was excluded. In total, 195 heterosexual couples (195 women and 195 men) remained for analysis. Blood tests for syphilis and HIV were refused by 19 people.
The mean age of female participants was 30.8 years (range, 18–55 years) and of male participants, it was 33.9 years (range, 19–60 years). Ninety-one percent of the women presented with STI symptoms or a positive blood test of syphilis. In contrast, 74% of the men came because their partner had an STI symptom or a positive blood test for syphilis (Table 1). The median number of lifetime sexual partners was higher in men than in women (8 vs. 2, P <0.0001). Men had a higher percentage of having multiple partners within the past year compared with women (39% vs. 9%, P <0.0001).
All participants reported vaginal sex with their current or prior partner(s). Anal sex, oral sex, and oral–anal contact with current or prior partner(s) were reported in 62%, 67%, and 27% of women and 71%, 77%, and 30% of men, respectively. Of the 195 men, 25 (13%) reported having had sexual contact with men (MSM) in addition to their female partners.
Prevalence of Sexually Transmitted Infections
The overall STI prevalence in women was 46% (89 of 195) and in men, it was 21% (41 of 195). Of 195 couples, 97 (50%) couples had at least one STI in the man or woman. Of those, 33 (34%) couples had a newly diagnosed STI found in both partners, 56 (58%) couples had a newly diagnosed STI only in women, and 8 (8%) couples had a newly diagnosed STI only in men (Table 2).
The most frequently diagnosed STIs in men were ureaplasma (13.3%), chlamydia (3.6%), and herpes (3.1%) (Table 3). In women, the most frequently diagnosed STIs were ureaplasma (27.2%), trichomonas (8.2%), and herpes (7.7%). Of all the STIs, only trichomonas (P = 0.004) and ureaplasma (P = 0.001) were found significantly more frequently in women than in men. The median age of STI-positive individuals was not significantly different from that of STI-negative individuals (30 years vs. 30 years in women, P = 0.584; 31 years vs. 33 years in men, P = 0.386).
Of the 33 couples with STIs in both partners, 26 (79%) were diagnosed with the same STI, including gonorrhea (n = 1), trichomonas (n = 2), chlamydia (n = 5), ureaplasma (n = 17), mycoplasma (n = 1), and HSV (n = 2). One couple had both ureaplasma and trichomonas and the other couple had both ureaplasma and M. genitalium. Multiple STI infections were found in 8 women and 5 men. Only the 2 couples mentioned previously had multiple STIs.
Of the 56 couples with STIs only in women, the most common STIs were ureaplasma (n = 32), herpes (n = 10), trichomonas (n = 9), syphilis (n = 5), and chlamydia (n = 4). Nine women were diagnosed with multiple STIs, most commonly ureaplasma and herpes (n = 6).
Of the 8 couples with an STI only in men, 6 had ureaplasma and one of these was also coinfected with gonorrhea. In the other 2 men, one was infected with chlamydia and the other with syphilis.
Factors Associated With Sexually Transmitted Infection
For women, the factors associated with STIs in both univariate and multiple logistic regression analysis included Catholic religion, having a television, more sexual partners in the past year or in their lifetime, more stable partners in their lifetime, and having receptive mouth-to-anus contact with their current partner (Table 4). Partner’s factors associated with women’s STI were a partner having an STI or having had oral–vaginal contact with his prior partner(s). Women having a MSM partner had 5% more STIs but the difference was not statistically significant (OR = 1.58; 95% confidence interval [CI] = 0.67–3.75). When significant variables were adjusted for having a MSM partner, significant variables were the same as stated previously. There was no difference between women cases and controls about consumption of alcohol, oral sex, anal sex, and condom use (Appendix A).
For men, the factors associated with STIs in univariate analysis included educational level of less than 11 years, having more number of stable partners or casual partners in their lifetime, having their current partner less than a year, and pain on urination (Table 5). Having the current partner as a stable partner was a preventive factor. All associations found in the univariate analysis remained in the multiple logistic regression analysis with the exception of having their current partner less than a year with marginal significance (OR = 3.07; 95% CI = 0.78–9.63; P = 0.055). Association between STI and having had insertive anal sex with their prior partner(s) became significant in the multiple logistic regression. Although a higher percentage of MSM were found among cases than controls (22% vs. 10%) and was close to significant in the univariate analysis (OR = 2.43; 95% CI = 0.98–5.98; P = 0.054), it was not statistically significant in the multiple logistic regression (OR = 2.15; 95% CI = 0.82–5.65; P = 0.121) (Table 5). There was no significant difference between male cases and controls concerning the number of sexual encounters with CSWs, the number of partners in the last year, oral sex, or condom use (Appendix B). The female partner’s risk factors associated with men’s STI were: a partner having an STI, younger age at first sexual intercourse, more sexual partners within the past year or in their lifetime, and a higher number of stable or casual partners in their lifetime (Table 5).
When we compare 26 concordant couples having the same pathogenic infection with 71 discordant couples (7 infected couples by different pathogens, 8 male-positive couples, and 56 female-positive couples), men’s younger age (OR = 4.86; 95% CI = 1.39–16.98), men who used condoms with their prior partner(s) (OR = 3.95; 95% CI = 1.06–14.70), and having the partner less than 1 year (OR = 7.03; 95% CI = 1.24–9.74) were associated with having the same pathogenic STI(s) within the couple.
Sixty percent of women in both case and control groups reported using a condom during vaginal sex. However, only 7% of cases and 10% of controls reported condom use during anal sex. Lower use of condoms among women during vaginal sex was associated with older age (>35 years; OR = 2.24; 95% CI = 1.21–4.15), lower educational level (OR = 2.37; 95% CI = 1.28–4.39), and their partner’s lower educational level (OR = 2.06; 95% CI = 1.07–3.98). Married women tended to use condoms less during vaginal sex with marginal significance (vs. single; OR = 2.14; 95% CI = 1.00–4.55). In the multiple logistic regression, only older age and woman’s lower educational level remained significant.
Condom use in men was also similar between case and controls with 78% of cases and 79% of controls reporting condom use during vaginal sex. However, only 18% of cases and 22% of controls used condoms during anal sex. In men, older age was also associated with decreased use of condoms during vaginal sex (OR = 4.45; 95% CI = 2.11–9.40).
Men Who Have Sex With Men
When 25 MSM were compared with the rest of the men (non-MSM) (Appendix C), MSM had a higher proportion than non-MSM for the following characteristics: <11 years of education, being circumcised, a higher number of lifetime sexual and stable partners, more sexual encounters for money and with CSWs, having oral–anal contact with their current female partner, and having insertive anal intercourse with prior partner(s) (Table 6). MSM were more likely to have STIs (36% vs. 19%), but, it was not a significant risk factor for either men or women (Tables 4 and 5). More condom use during anal sex (29% vs. 19%, P = 0.270) and vaginal sex (88% vs. 77%, P = 0.097) tended to occur in MSM than in non-MSM.
When only non-MSM were included in the men’s STI risk analysis, the following variables remained significant in the multiple logistic regression: having a current partner as a stable partner, having more lifetime stable partners, having their current partner less than a year, having had insertive anal sex with his prior partner(s), pain on urination, female partner having an STI, female partner’s younger age at first sexual intercourse, and having a female partner with more sexual casual partners in her lifetime.
Exclusion of Ureaplasma
To control for the effect of ureaplasma, we performed 2 additional analyses. When ureaplasma was excluded, the number of cases was 48 in women and 22 in men. The number of couples having STI in both partners decreased from 33 to 15.
Among women, the factors associated with STI infection were pain on urination, having a partner with an STI, partner’s low educational level, and their partner’s not using condoms for vaginal sex (Table 7). The younger the partner’s age, the less likely a women would have a non-ureaplasma STI (OR = 0.33; 95% CI = 0.14–0.79).
For men, after excluding ureaplasma from the analysis, factors associated with STIs were 2 or more current partners, having a partner with STI, a partner who had first sexual intercourse at a younger age, and number of partner’s sexual partners in their lifetime. Having a stable partner was preventive (OR = 0.10; 95% CI = 0.02–0.47). Although 6 (24%) of the 25 MSM were newly diagnosed with ureaplasma, MSM remained as a nonassociated factor for STIs.
Factors associated with having ureaplasma for women were: Catholic religion, having 2 or more partners within a year, having more partners (both stable and casual) in her life, male mouth to anus contact, oral–vaginal contact, oral–penis contact, and nonmenstrual vaginal bleeding. The male partner’s factors of having ureaplasma infection, younger age at first sexual intercourse, more stable partners in his lifetime, and oral sex with their prior partner(s) (oral–vaginal contact and oral–penis contact) were also associated with women’s ureaplasma infection. In men, the following factors were significantly associated with ureaplasma infection: the number of lifetime sexual and stable partners, insertive anal sex with prior partner(s), and their partner’s ureaplasma infection, age at first intercourse, number sexual partners in the past year or lifetime, and number of lifetime casual partners. The association between MSM and having ureaplasma was close to significance (OR = 2.88; 95% CI = 0.98–8.47; P = 0.054).
Although couples in a stable relationship would not be expected to be at high risk for STIs, we found many couples practicing high-risk sexual behaviors both with their stable partner and with casual partners. Although sexual risk behaviors were frequent, the overall prevalence of STIs in this population was lower than expected. Not surprisingly, couples who exhibited high-risk sexual behaviors were more likely to have STIs. The high rate of practicing anal sex and the low rate of condom use during this activity compared with the high rate of condom use during vaginal sex suggest that anal sex is primarily used for birth control and is not considered a high-risk sexual practice. In addition, condom use often is not associated with disease prevention, but rather is used for preventing pregnancy. In a survey of women in a shantytown of Lima, many women considered STIs to be the result of poor personal hygiene rather than sexual contact.27
Within heterosexual couples in which one or both partners had an STI, both female and male partners exhibited well-recognized sexual behaviors that placed them at risk. In our and another Peruvian studies,10,28 men had a higher number of sexual partners than did women. The sexual network of men is a risk factor for their female partners who personally have fewer risks. Interestingly, however, there were no differences between cases and controls for important STI-related factors such as condom use or having sexual contact with female sex workers (men only). In fact, although cases had more STI risk factors, both cases and controls practiced high-risk sexual behavior. This is likely because our study was conducted at STD clinics and therefore participants were already at a higher risk than the general population to have an STI.
Heterosexual couples, in which the man reported himself as an MSM, practiced high-risk behaviors, including paying money for sex and practicing anal intercourse, had a higher proportion of STIs. Tabet et al29 found that MSM in Peru were less likely to have used condoms consistently during the past year for vaginal sex compared with insertive anal sex with men. In Tabet’s study, 80% used condoms during anal sex compared with our study in which condom use was less frequent: only 29% and 18% in MSM and non-MSM, respectively.
In Peru and other Latin American countries, MSM may represent a bridging population between male homosexuals and female heterosexuals. It seems that MSM are not well informed about the high risk of STI transmission by anal sex. Miller et al30 noted that more men reported learning to use a condom for vaginal sex from a female sex worker than from any other source. Interestingly, MSM in our study reported higher rates of visiting CSWs and a slightly higher rate of condom use than non-MSM.
Ureaplasma was the most prevalent organism found in this study’s participants (13% of men and 27% of women). Our study similar to others demonstrates that ureaplasma genital colonization tends to be a marker of sexual experience and increases in relation to the number of sexual partners.31
Ureaplasma colonizes women more commonly than men, but in men, it may be pathogenic, causing acute urethritis. However, even in asymptomatic men attending an STD clinic, there may be a higher carriage rate because tolerance to the organism may occur over time, and it is difficult to eradicate with antimicrobial therapy.32,33 Although this is the first study to report the prevalence of ureaplasma in Peru, ureaplasma was common in both men and women similar to heterosexual populations in other countries.34,35 Interestingly, the subanalysis of ureaplasma infection highlighted the association between ureaplasma infection and oral–genital or oral–anal contacts.
When the analysis was repeated without ureaplasma, the number of STI cases decreased, and the analysis was underpowered to show some of the risk factors for STIs that have been previously identified. However, when ureaplasma was excluded from the analysis, women with a newly diagnosed STI were more likely to be symptomatic with pain on urination. Also, male cases were less likely to use condoms for vaginal sex with casual sexual partners. These additional risk factors were unmasked by excluding ureaplasma, which may represent a colonizer in many of the study participants.
Prevalence of STIs in our population attending an STD clinic was not as high as expected. Compared with a prevalence study performed in a Peruvian family planning and antenatal clinic,34 the prevalence of STIs was similar, although the family planning/antenatal group is a lower-risk population than an STD clinic population.15 For example, in the family planning/antenatal clinic in which approximately 350 women were tested, 5% had trichomoniasis, 5% had chlamydia, 1.4% had gonorrhea, and there were no cases of HIV. In our study, in which HIV cases were excluded, 8% of women had trichomoniasis, 5.5% had chlamydia, and 1.5% had gonorrhea. Perhaps the similar prevalence of STIs occurred because although the STD clinic population is at higher risk, our study participants claimed to be in stable heterosexual relationships, which may place them at a lower risk than the usual STD clinic population. However, the prevalence of syphilis (3%) in our female participants was similar to that observed in previous published studies of Peruvian female sex workers.15,20 In a previous study, patients with HIV in Peru had much higher prevalence rate of gonorrhea (7%) and syphilis (18%).21
M. genitalium has not previously been looked for in a Peruvian population. However, other studies have found M. genitalium in approximately 20% of men with symptoms of urethritis versus 7% of men without urethritis.34 Our study found a relatively low prevalence of 1.5% in men and 3.5% in women. Further investigation is necessary to determine the significance of M. genitalium in this population.
There was less concordance of STIs within couples than we expected. Only 26 of the 97 (27%) couples diagnosed with an STI had at least one concordant STI. This lack of concordance may have occurred for several reasons: difference in sensitivity of diagnostic method between men and women, although men had riskier behavior and cases infected as a result of sexual contacts other than their stable partners. This may be especially true for organisms which are often asymptomatic such as syphilis, chlamydia, and ureaplasma and for which people do not seek timely medical attention.
In another study in Peru, the seroprevalence of HSV-2 in shantytown population was 7% in men and 21% in women.37 In higher risk groups such as socially marginalized individuals and males who had sex only with men (MSOM), prevalence rates were 42% for women, 21% for men, and 72% for MSOM, respectively. Our results for HSV determined by PCR will underestimate the extent of HSV-2 infection because only active disease will be detected.
In conclusion, heterosexual couples attending STD clinics displayed typical high-risk sexual behavior. Couples in which a new STI was diagnosed had more risk factors than those not newly diagnosed. The prevalence of ureaplasma in both men and women was elevated, but the prevalence of M. genitalium was low. Prevalence of other STDs was similar to previous studies. MSM were more likely to have an STI and their condom use was less than 30% during anal sex with their female partner, thus putting their partner at high risk for STIs. It would appear educational effort concerning prevention of STIs in Peru requires more attention.
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