Skip to main content
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2013 Aug 12.
Published in final edited form as: Sex Transm Dis. 2012 Jan;39(1):1–7. doi: 10.1097/OLQ.0b013e31823b1922

ONGOING SEXUALLY TRANSMITTED DISEASE ACQUISTION AND RISK TAKING BEHAVIOR AMONG U.S. HIV-INFECTED PATIENTS IN PRIMARY CARE: IMPLICATIONS FOR PREVENTION INTERVENTIONS

Kenneth H Mayer 1, Timothy Bush 2, Keith Henry 3, Turner Overton 4, John Hammer 5, Jean Richardson 6, Kathy Wood 7, Lois Conley 2, John Papp 8, Angela M Caliendo 9, Pragna Patel 2, John T Brooks 2; the SUN Investigators
PMCID: PMC3740591  NIHMSID: NIHMS336712  PMID: 22183836

SUMMARY

A study of HIV-infected persons in primary care in four U.S. found that 13% had a prevalent STD at enrollment and 7% an incident STD six months later.

Background

To better understand the factors associated with HIV and STD transmitting behavior among HIV-infected persons, we estimated STD prevalence and incidence and associated risk factors among a diverse sample of HIV-infected patients in primary care.

Methods

We analyzed data from 557 participants in the SUN study, a prospective observational cohort of HIV-infected persons in primary care in four U.S. cities. At enrollment and six months thereafter, participants completed an audio computer-assisted self interview about their sexual behavior, and were screened for genitourinary, rectal and pharyngeal N. gonorrhoeae and C. trachomatis infections by nucleic acid amplification testing, and for serologic evidence of syphilis. Women provided cervicovaginal samples and men provided urine to screen for T. vaginalis by polymerase chain reaction.

Results

Thirteen percent of participants had a prevalent STD at enrollment and 7% an incident STD six months later. The most commonly diagnosed infections were rectal chlamydia, oropharyngeal gonorrhea, and chlamydial urethritis among the men, and trichomoniasis among the women. Other than trichomoniasis, 94% of incident STDs were identified in MSM. Polysubstance abuse other than marijuana, and having ≥ 4 sex partners in the six months prior to testing were associated with diagnosis of an incident STD.

Conclusions

STDs were commonly diagnosed among contemporary HIV-infected patients receiving routine outpatient care, particularly among sexually active MSM who used recreational drugs. These findings underscore the need for frequent STD screening, prevention counseling, and substance abuse treatment for HIV-infected persons in care.

Keywords: HIV infection, sexual risk, sexually transmitted infections

INTRODUCTION

The HIV epidemic continues unabated in the United States, with men who have sex with men (MSM) accounting for more than half of incident HIV infections, and African Americans being disproportionately affected compared with other racial or ethnic groups 1. Although about half of new HIV infections are transmitted by persons who do not know they are HIV infected 2, the rest are due to contact with individuals who are aware of their infection. HIV disease is now a chronic manageable illness requiring multiple regular contacts with medical care providers for optimal clinical outcomes 3. Thus, HIV clinicians have a unique opportunity to routinely screen their patients for sexually transmitted diseases (STDs), and to assess their risk for HIV and STD transmission. Of particular concern are patients who are not on suppressive antiretroviral therapy, have an STD, or who are engaging in unprotected anal or vaginal intercourse, since each of these factors increases the likelihood of transmitting HIV 4,5. To better understand the factors associated with HIV and STD transmission behaviors among HIV-infected persons, we estimated STD prevalence and incidence, and associated risk factors, among HIV-infected persons enrolled in the Study to Understand the Natural History of HIV and AIDS in the Era of Effective Therapy (the ‘SUN’ Study), a prospective cohort study led by the Centers for Disease Control and Prevention (CDC).

METHODS

The SUN Study

The SUN Study is a prospective, observational cohort study that monitors the clinical course of HIV-infected individuals treated with highly active antiretroviral therapy (HAART) from seven HIV-specialty clinics in four US cities: St. Louis, Missouri (25% of the enrollees); Providence, Rhode Island (27%); Minneapolis, Minnesota (34%); and Denver, Colorado (13%) 6. Of 1346 potential participants who met enrollment criteria, 700 HIV-infected patients were enrolled between March 1, 2004 and June 30, 2006. Reasons for non-enrollment generally focused on perceived study burden. The study’s design, and its data collection and management methods have been described previously 2,6. Participants were generally healthy HIV-infected adults receiving routine outpatient care and were either treatment naïve, or had only been treated with HAART. Patient data, including sociodemographic characteristics, all diagnoses and treatments (including dosage and duration of all medications), and all clinical laboratory data were abstracted from medical charts and entered into an electronic database (Clinical Practice Analyst; Cerner Corporation, Vienna, VA) by trained staff. These data were reviewed for quality and analyzed centrally. Additional data were collected through physical examination, non-invasive imaging, comprehensive testing for STDs, and an audio computer-assisted self interview (ACASI). The ACASI collected behavioral risk data and other health-related information including selected family history variables and use of tobacco, alcohol and non-prescribed (i.e., recreational) drugs. The study protocol was approved and reviewed annually by the CDC and each participating site’s institutional review board.

Testing for sexually transmitted diseases

At study enrolment (i.e., baseline) and every 6 months thereafter, study nurses screened participants for oropharyngeal and rectal Neisseria gonorrhoeae (GC) and Chlamydia trachomatis (CT) infections using swabs provided by the APTIMA COMBO 2® nucleic acid amplification test kits (Gen-Probe, Inc; San Diego, CA). The specimens were tested centrally at CDC. Genitourinary Neisseria gonorrhoeae and Chlamydia trachomatis testing was performed using the FDA-approved commercial method employed at each local clinic’s laboratory. Women were screened for vaginal Trichomonas vaginalis (TV) infection using self-administered swabs and men were screened for TV using centrifuged urine pellets by polymerase chain reaction 6,7; this testing was conducted centrally at Emory University. Site staff were centrally trained to ensure diligence with regard to specimen handling and shipping to optimize the integrity of test results. Sera were tested for syphilis at each site using non-specific assays (e.g., VDRL, RPR) with reflex confirmation assays (e.g., MHA-TP, FTA-ABS) if positive. Medical record abstracted data were reviewed by Infectious Disease physicians, who categorized new infectious from previously treated ones using common clinical algorithms, based on USPHS guidelines. Symptom data for GC, CT and TV infections were collected at the time of specimen collection on specimen collection forms.

Statistical analysis

The outcome variables included prevalent and incident STD diagnoses at baseline and 6 months later, respectively. Assuming all prevalent STDs were treated at baseline, an incident STD was defined as a new STD diagnosis at 6 months. The Mantal Haenszel χ2 or Fisher’s exact test was used to compare categorical variables and Student’s t-test or the Kruskal-Wallis test was used to compare continuous variables in univariate analysis. Multivariate logistic regression models were used to explore associations with the outcome variables. Variables with a p-value < 0.10 in univariate analysis were entered stepwise into a regression model to determine the best multivariate model. P-values were two-tailed and considered significant at p < 0.05. All statistical analyses were performed using SAS, version 9.1 (SAS Institute, Inc., Cary, North Carolina).

RESULTS

Participant Characteristics

The sample consisted of 557 participants for whom complete STD data were available at the baseline and 6-month visits. This sample did not differ demographically from the larger group of participants for only whom baseline data were available. At baseline, the mean age was 42 years (range, 21– 69 years), 79% were men, 61% were non-Hispanic white and 10% were Hispanic. Almost two-thirds of the cohort consisted of men who described themselves per ACASI as men who had sex with men (65%), 21% were women, and 13% were self-described men who had sex with women. The median CD4 cell count of the participants was 479 cells/mm3 and 78% were currently prescribed HAART, of whom 87% had plasma HIV RNA levels of less than 400 copies/mL. Additional characteristics are shown in Table 1.

Table 1.

Baseline Characteristics of Participants, the SUN Study

Baseline Characteristics All Participants
(n=557)(%)
MSM
(n=365)(%)
MSW
(n=73)(%)
Women
(n=119)(%)
Race/ethnicity
  White, non-Hispanic 342 (61) 279 (76) 23 (32) 40 (34)
  Black, non-Hispanic 145 (26) 47 (13) 38 (52) 60 (50)
  Hispanic 57 (10) 34 (9) 9 (12) 14 (12)
  Other/Unknown 13 (2) 5 (1) 3 (4) 5 (4)
Median age at baseline 42 42 43 39
  (IQR) (36 – 47) (36 – 48) (38 – 47) (30 – 45)
High school graduate 467 (88) 326 (94) 55 (85) 86 (73)
Currently employed 327 (60) 249 (70) 35 (50) 43 (38)
Median CD4 cell count 479 485 464 465
  (IQR) (334 – 691) (342 – 696) (294 – 555) (336 – 704)
Viral load < 400 397 (71) 266 (73) 55 (75) 76 (64)
ARV naive 68 (12) 45 (12) 6 (8) 17 (14)
Current cART 436 (78) 288 (79) 62 (85) 86 (72)
Years since HIV diagnosis 4.9 5.1 4.0 4.9
(IQR) (2.2 – 8.1) (2.2 – 8.1) (1.9 – 7.8) (2.5 – 8.3)

IQR= interquartile range; cART=combination antiretroviral therapy; ARV=antiretroviral; MSM=men who have sex with men; MSW=men who have sex with women

STD prevalence and incidence

At baseline, 13% of the participants had at least one STD (Table 2); all were asymptomatic. At baseline, participants from Denver and St. Louis had significantly higher STD prevalence (22% and 21%, respectively) than those enrolled in Minneapolis (10%) or Providence (9%) (p = 0.001). However, the six month follow-up STD rates did not significantly differ by site (data not shown). Rectal CT infection was most common (5%), followed by oropharyngeal GC infection (3%), trichomonas (3%), and urethral CT infection (2%). Approximately 1% of the cohort had syphilis, oropharyngeal CT infection or rectal GC infection. Two participants (one MSW, one woman) had asymptomatic urethral GC infection. Among women, 14% had vaginal TV infection at baseline. No significant differences in STD prevalence were seen when data were stratified by age, race/ethnicity, or level of education (data not shown). All STDs were treated by the participants’ primary care providers according to standard of care. Six months later, 7% of the cohort had developed at least one new STD. Rectal CT infection remained most common (3%), with about 1% of the participants developing each of the other infections. No men were diagnosed with either prevalent or incident urethral TV infections.

Table 2.

Prevalence and Incidence of Sexually Transmitted Diseases (STDs) in the SUN Study

Prevalent Infections (Baseline) Incident Infections (6-Month Visit)

STD MSM
(N=365)
MSW
(N=73)
Women
(N=119)
Total
(N=557)
MSM
(N=365)
MSW
(N=73)
Women
(N=119)
Total
(N=557)
Anorectum:
  - C. trachomatis 27 (7%) 0 (0%) 2 (2%) 29 (5%) 18 (5%) 0 (0%) 0 (0%) 18 (3%)
  - N. gonorrhoeae 7 (2%) 0 (0%) 1 (1%) 8 (1%) 6 (2%) 0 (0%) 0 (0%) 6 (1%)
Oropharynx:
  - C. trachomatis 2 (1%) 1 (1%) 2 (2%) 5 (1%) 7 (2%) 0 (0%) 0 (0%) 7 (1%)
  - N. gonorrhoeae 12 (3%) 1 (1%) 2 (2%) 15 (3%) 5 (1%) 0 (0%) 2 (2%) 7 (1%)
Genitourinary
  - T. vaginalis 0 (0%) 0 (0%) 17 (14%) 17 (3%) 0 (0%) 0 (0%) 3 (3%) 3 (1%)
  - C. trachomatis 8 (2%) 0 (0%) 3 (3%) 11 (2%) 3 (1%) 0 (0%) 0 (0%) 3 (1%)
  - N. gonorrhoeae 0 (0%) 1 (1%) 1 (1%) 2 (< 1%) 2 (1%) 0 (0%) 0 (0%) 2 (< 1%)
Syphilis 5 (1%) 0 (0%) 0 (0%) 5 (1%) 2 (1%) 0 (0%) 0 (0%) 2 (< 1%)
Any STD (≥1) 49 (13%) 3 (4%) 23 (19%) 75 (13%) 34 (9%) 0 (0%) 5 (4%) 39 (7%)
  - excluding T. vaginalis 49 (13%) 3 (4%) 8 (7%) 60 (11%) 34 (9%) 0 (0%) 2 (2%) 36 (6%)
≥ 2 STDs 9 (2%) 0 (0%) 3 (3%) 12 (2%) 7 (2%) 0 (0%) 0 (0%) 7 (1%)

Abbreviations: MSM, men who have sex with men; MSW, men who have sex with women

The majority of the STD diagnoses were in MSM, who accounted for 65% of the prevalent and 87% of all of the incident STDs, and 82% and 94% of all prevalent and incident STD diagnoses excluding trichomoniasis. At baseline, 13% of the MSM in the study had an STD compared to 9% at 6 months. The most common STD among MSM was rectal CT infection, which was present in 7% of the MSM at baseline and 5% at the 6-month visit, followed by rectal GC infection (2% at baseline and 2% at 6 months) and oropharyngeal GC infection (3% and 1% respectively).

Among ten MSM who had at least one STD diagnosed at both the baseline and 6-month visits, seven had infections with either a new organism or infections with the same organism but at different anatomical sites. Of the other three men, two had rectal CT and one had oropharyngeal GC at both visits which were treated at baseline. By the time of the 6-month visit, 20% of the MSM had been diagnosed with one or more prevalent or incident STDs. Most of the GC and CT infections in MSM were detected at extra-genitourinary sites, with 86% and 88% infections at the baseline and 6-month visits, respectively, having been diagnosed at either the rectum or oropharynx.

Factors Associated with Prevalent and Incident STDs

Because the vast majority of the prevalent and incident STD’s were diagnosed among MSM, additional analyses were performed to evaluate the factors associated with STD diagnoses in this population. MSM with prevalent and incident STDs were more likely to report unprotected anal sex, either insertive or receptive, and sex with four or more partners in the six months preceding testing (p<0.05) (Table 3). Of note, 59% of the men with a prevalent STD and 37% of the men without a prevalent STD reported unprotected insertive or receptive anal sex, and 65% of the men with an incident STD and 34% of the men without an incident STD reported unprotected insertive or receptive anal sex. The percentage of MSM reporting unprotected anal sex did not decrease between the baseline and 6-month visits (p=0.257). MSM with a prevalent STD were more likely to report insertive or receptive anal sex compared with MSM without an STD (p=0.006 and p=<0.001, respectively); this difference remained significant for incident cases (p=0.002 and p=0.007, respectively). At least 60% of the men engaged in unprotected oral sex at either visit. Overall, 27% of the MSM in the SUN Study cohort had detectable plasma HIV RNA (Table 1), which included 29% of the 49 men with a prevalent STD and 24% of the 34 men with an incident STD.

Table 3.

Potential Risk Factors for Sexually Transmitted Disease* Acquisition Among Men Who Have Sex with Men, the SUN Study

Prevalent Diagnosis Incident Diagnosis
Behaviors reported in
preceding 6 months, unless
otherwise specified

STD
(n=49)
(%)

No STD
(n=316)
(%)


p-value

STD
(n=34)
(%)

No STD
(n=331)
(%)


p-value
Unprotected receptive anal sex 25 (51) 97 (31) 0.006 18 (53) 90 (47) 0.002
Unprotected insertive anal sex 23 (47) 66 (21) < 0.001 15 (44) 76 (23) 0.007
Any unprotected anal sex 29 (59) 114 (37) 0.003 22 (65) 114 (34) < 0.001
Unprotected receptive oral sex 41 (84) 201 (64) 0.008 26 (76) 213 (64) 0.157
Unprotected insertive oral sex 41 (84) 191 (61) 0.002 26 (76) 199 (60) 0.062
≥ 4 sexual partners 29 (59) 72 (23) < 0.001 19 (58) 76 (23) < 0.001
Marijuana use 16 (33) 112 (36) 0.659 11 (32) 106 (32) 0.969
Cocaine use 4 (8) 34 (11) 0.553 5 (15) 31 (9) 0.233
Use of inhaled nitrite 20 (41) 85 (27) 0.052 15 (44) 88 (27) 0.030
Heroin use 0 (0) 2 (1) 1.000 0 (0) 2 (1) 1.000
Use of club or party drugs
(including methamphetamine)
3 (6) 26 (8) 0.785 7 (21) 19 (6) 0.006
Polysubstance abuse
  (other than marijuana)
4 (8) 23 (7) 0.513 9 (26) 15 (5) < 0.001
Injection drug use 0 (0) 6 (2) 1.000 1 (3) 4 (1) 0.388
Exogenous testosterone use 5 (10) 28 (9) 0.477 4 (12) 47 (14) 0.678
Use of erectile dysfunction agent1 14 (29) 52 (17) 0.045 14 (41) 59 (18) 0.001
Alcohol consumption in last 30
  days (≥ once per week binging
  or ≥ 5 drinks at one time)
17 (35) 100 (32) 0.735 14 (41) 99 (30) 0.184
*

STDs included syphilis, and oropharyngeal, rectal and urine Neisseria gonorrhea and Chlamydia trachomatis

p-value calculated using Mantal-Haenszel chi-square test

Recreational drugs were commonly used by the MSM in the study (Table 3). About one-third of the men (35% at baseline and 32% at 6 months) reported using marijuana in the prior 6 months; 29% reported inhaling volatile nitrites at baseline and 28% at 6 months; 18% used erectile enhancement drugs at baseline and 20% at 6 months; 10% of the men reported cocaine use at baseline and 10% at 6 months. Although heroin use and any drug injection was rare in the cohort (two men reported using heroin at baseline and at 6 months; six men reported injecting drugs at baseline and five men at 6 months), alcohol abuse (at least 5 drinks at one time or binging at least once per week) was common, reported by 32% of the men at baseline and 31% at 6 months.

In univariate analyses, factors associated with having a prevalent STD included unprotected insertive or receptive anal, unprotected insertive oral sex, having four or more partners in the prior 6 months, and use of erectile dysfunction agents (Table 4). In the multivariate analysis, only having four or more partners in the prior 6 months remained significantly associated with diagnosis of a prevalent STD. In the univariate analysis, factors associated with having an incident STD included unprotected insertive or receptive anal, use of inhaled nitrites (i.e., poppers), polysubstance abuse (other than marijuana), use of club or party drugs, and use of erectile dysfunction agents (Table 4). In multivariate analysis, factors independently associated with diagnosis of an incident STD were having four or more partners and polysubstance abuse (other than marijuana) (Table 4). Variables that were not associated with increased risk for a prevalent or incident STD included age, race/ethnicity or educational status (data not shown).

Table 4.

Logistic Regression Analysis of Factors Associated with Prevalent and Incident STDs* among Men Who have Sex with Men, the SUN Study

Univariate Analysis Multivariate Analysis
Risk Factors
OR (95% CI) p value OR (95% CI) p value
For Prevalent STDs
  Unprotected receptive anal sex 2.31 (1.25 – 4.26) 0.007
  Unprotected insertive anal sex 3.30 (1.76 – 6.16) < 0.001
  Unprotected insertive oral sex 3.25 (1.55 – 7.68) 0.003
  ≥ 4 partners 4.81 (2.59 – 9.13) < 0.001 4.81 (2.59 – 9.13) < 0.001
  Use of inhaled nitrites 1.84 (0.98 – 3.41) 0.054
  Use of erectile dysfunction agents 2.00 (0.98 – 3.91) 0.048

For Incident STDs
  Unprotected receptive anal sex 3.01 (1.47 – 6.22) 0.002
  Unprotected insertive anal sex 2.65 (1.27 – 5.45) 0.008
  Unprotected insertive oral sex 2.16 (0.99 – 5.23) 0.067
  ≥ 4 partners 4.54 (2.18 – 9.64) < 0.001 3.44 (1.82 – 7.56) 0.001
  Use of inhaled nitrites 2.18 (1.05 – 4.47) 0.034
  Use of club or party drugs
 (including methamphetamine)
4.26 (1.55 – 10.7) 0.003
  Polysubstance abuse (other than
  marijuana)
7.58 (2.93 – 18.9) < 0.001 5.00 (1.82 – 13.2) 0.002
  Use of erectile dysfunction agents 3.18 (1.49 – 6.62) 0.002

STD = sexually transmitted diseases; OR= odds ratio; CI=confidence interval

*

STDs include syphilis, and oropharyngeal, rectal and urine Neisseria gonorrhea and Chlamydia trachomatis

p-value calculated using Wald chi-square test

Status of partners of MSM with an incident STD

Twenty-nine of the 34 (85%) MSM who had an incident STD reported unprotected anal or oral sex with at least one partner. Among these 29 MSM, 31% reported at least one episode of unprotected insertive anal sex, and 48% reported at least one episode of unprotected receptive anal sex with an HIV-uninfected partner or partner of unknown status (Table 5). The prevalence of unprotected oral sex with HIV-uninfected partners or partners of unknown status was 82% among MSM with an incident STD. Of these 29 men, six of 15 who reported unprotected insertive anal intercourse and four of the 18 who reported unprotected receptive anal intercourse only engaged in these practices with HIV-infected partners.

Table 5.

HIV Status of Partners of Men Who Have Sex with Men with an Incident STD at the 6-Month Visit and Who Reported Unprotected Sexual Activity in the Preceding Last 6 Months (n=29), the SUN Study

HIV Status of Partner
Sex Behaviors Unknown or
Positive Negative Unknown Negative
Anal sex (n=22)
  Insertive(n=15)(%) 10 (67) 1 (7) 8 (53) 9 (60)
  Receptive (n=18)(%) 12 (67) 6 (33) 11 (61) 14 (78)
Oral sex (n=28)
  Insertive (n=26) (%) 16 (62) 13 (50) 15 (58) 23 (88)
  Receptive (n=26) (%) 13 (50) 12 (46) 17 (65) 24 (92)

DISCUSSION

Despite the advent of HAART, which could conceivably slow the spread of HIV by decreasing the infectiousness of those who are treated 8, the annual HIV incidence in the U.S. has remained unchanged during the past decade, with the number of new HIV diagnoses reported to CDC increasing among MSM, most notably among younger African-Americans 1. As reports from community-based samples have documented recent increases in sexual risk taking and STD diagnoses that could increase risk of HIV acquisition and transmission 9-11, our analysis demonstrates that a substantial subgroup of contemporary HIV-infected MSM in regular care have engaged in behaviors capable of transmitting HIV.

Although trichomoniasis was commonly diagnosed among women in this study, the majority of STDs were diagnosed among MSM, who were 65% of the whole sample and had 87% of the incident STDs. The high co-prevalence of STD’s in HIV-infected MSM has been noted in other studies.12 The relative under representation of women (21%) and Black/African-Americans (26%) is a limitation of the study, compromising the ability to make comparisons about differences in STD burden in these populations, compared to Caucasian MSM. Because all study participants received state-of-the-art counseling, and all diagnosed STDs were promptly treated when diagnosed, the incidence of new STDs was attenuated, and would therefore constitute a lower estimate of what might be seen in less controlled environments..

Similar to other studies13,14, the anatomic site where asymptomatic gonorrhea and Chlamydia infections were most frequently detected was the rectum, which can serve as a reservoir potentiating transmission of these infections15,16. The substantial prevalence and incidence of these rectal infections among MSM highlight the need for simpler screening methods of at-risk patients to optimize the likelihood that busy clinical providers will adopt routine rectal screening of sexually active patients. At present however, none of several highly sensitive nucleic acid amplification tests, including the one used in this study, have been granted FDA approval for diagnostic use at rectal or oropharyngeal sites.

Not only did MSM diagnosed with an STD in this study report increased numbers of sexual partners, 29 (8%) were at particularly high risk for transmitting HIV and other STDs insofar as they reported unprotected sex at the time of their STD. Of these men, 9 of 15 who reported unprotected insertive anal intercourse and 14 of 18 who reported receptive anal intercourse had HIV seronegative or status unknown partners, potentially leading to new HIV transmissions (Table 5). The other men reported unprotected anal intercourse exclusively with other HIV-infected partners, which could result in new STD transmission and acquisition, and potential superinfection. Such “serosorting” (the practice of selecting sexual partners who are also HIV-infected) may explain reports that have noted disproportionately increased rates of STD diagnoses among HIV-infected MSM compared with other MSM17,18,19.

MSM with an incident STD were more likely to report polysubstance use than MSM without an STD. These findings support other recent observations that have shown an association between new HIV infections and STDs among substance-using MSM20,21,22. Crystal methamphetamine use has been shown to be particularly highly correlated with increased sexual risk behaviors and correspondingly with the acquisition and transmission of STDs, and has been shown to decrease medication adherence, increasing the risk of virological failure, making users more infectious to their partners 23,24,25. In the current study, more than one fourth of the MSM in care had detectable plasma HIV RNA, including 29% of the 49 men with a prevalent STD and 24% of the 34 men with an incident STD, making them at risk for the efficient transmission of antiretroviral-resistant strains. Some have suggested that increased risk taking behaviors among MSM may reflect treatment optimism; e.g., the belief that the diagnosis of HIV infection is no longer as severe as previously construed26,27.

These findings underscore the important role that primary HIV care providers should play in diagnosing and treating STDs and in providing counseling and referrals that can lead to decreased HIV transmission behaviors.28 From the patient’s perspective, syphilis and possibly other STDs, if untreated, can accelerate the course of HIV disease29,30,31. Thus, current CDC guidelines recommend that providers routinely ask their patients about their sexual behaviors and screen them for STDs annually, and more often (i.e., every three to six months) if they have a past history of any STD or have engaged recently in sexual behavior capable of transmitting HIV or STDs32. The most recent guidelines of the U.S. Department of Health and Human Services note that use of effective antiretroviral therapy regardless of CD4 count is likely to reduce transmission to the uninfected sexual partner. 33

In summary, we found a high prevalence of asymptomatic STDs among HIV-infected patients receiving routine outpatient care, particularly among MSM, corroborating a global trend.34,35 Six months later, following effective treatment, we observed that almost 10% were diagnosed with a new STD and that MSM with STDs and detectable HIV viral loads had continued to engage in high-risk sexual behaviors that could transmit their HIV infection to others. The large majority of STDs among MSM were rectal or oropharyngeal; in the absence of FDA-approved simple methods for their diagnosis (e.g., NAAT) at these anatomic sites, many of these STDs might have gone undiagnosed. Our findings suggest that efforts are needed to ensure that HIV-infected patients in care not only adhere to treatment for their own benefit, but that they be screened and treated for STDs and modify their behavior to decrease their risk of transmitting HIV to others. Sexually active HIV-infected patients should also be offered culturally appropriate risk reduction interventions that address the underlying factors potentiating sexual risk-taking behaviors, including substance use. Further research is needed to develop new clinic-based prevention interventions that can be readily integrated into comprehensive HIV care, that build on existing evidence-based prevention interventions 36,37, in order to limit further HIV transmission by patients in care.

ACKNOWLEDGEMENTS

The authors thank Jean Richardson and Joel Milam, Keck School of Medicine, University of Southern California, Los Angeles, California; Paul Maruff, David Darby, and Angela Caveney, CogState Ltd., Melbourne, Victoria, Australia and Pinckney, Michigan; Suzette Bartley and Dollene Hemmerlein, Division of Scientific Resources, National Center for Infectious Diseases, CDC, Atlanta, Georgia; John Papp, Carol Farshy, and Christi Phillips, Division of AIDS, STDs and Tuberculosis Laboratory Research, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, CDC, Atlanta, Georgia; Elizabeth Unger and David Swan, Division of Viral and Rickettsial Diseases, National Center for Infectious Diseases, CDC, Atlanta, Georgia; Angela Caliendo, Jessica Ingersoll, Tameka Bythwood, and Deborah Abdul-Ali, Emory University, Atlanta, Georgia; Teresa Darragh, Mt. Zion Medical Center, University of California, San Francisco, California; Roger Fielding, Andrea Desilets, and Sara Farnan-Colleary, Gerald J, and Dorothy R. Fiedman Body Composition Analysis Center, Tufts Medical Center, Boston, Massachusetts; John Gottdiener and Shuying Li, Echocardiography Lab, University of Maryland Hospital, Baltimore, Maryland; Howard Hodis and Yanjie Li, Blankenhorn Research Fund, University of Southern California, Los Angeles, California; and Matt Budoff and Angel Salano, Harbor UCLA Research and Education Institute, University of California, Los Angeles, Torrence, California.

Source of Support: Financial support was received from Centers for Disease Control and Prevention contracts 200-2002-00610, 200-2002-00611, 200-2002-00612, 200-2002-00613, 200-2007-23633, 200-2007-23634, 200-2007-23635, and 200-2007-23636. This work was supported in part by the Emory Center for AIDS research (P30 AI050409).

The SUN Study Investigators

John T. Brooks, Pragna Patel, Lois Conley and Tim Bush, Division of HIV/AIDS Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, CDC, Atlanta, Georgia; Kathleen Wood, Rose Baker, and Cheryl Akridge, Cerner Corporation, Vienna, Virginia; John Hammer, Tara Kennedy, Barbara Widick and Billie Thomas, Denver Infectious Disease Consultants, Inc., Denver, Colorado; Ken Lichtenstein and Cheryl Stewart, National Jewish Medical and Research Center, Denver Colorado; Keith Henry, Jason Baker, Edie Gunderson, Miki Olson, and John Hall, Hennepin County Medical Center, Minneapolis, Minnesota; Frank Rhame, Mark Olson, and Eve Austad, Abbott-Northwestern Hospital, Minneapolis, Minnesota; Hal Martin, Meaghan Morton, and Cheri Murch, Park-Nicollet Institute, Minneapolis, Minnesota; Charles Carpenter, Susan Cu-Uvin, Kenneth Mayer, Erna Milunka Kojic, Lynn Taylor, Jennifer Florczyk, Sara Metzler and Patricia D’Aiello, The Miriam Hospital, Providence Rhode Island; and E. Turner Overton, Lisa Kessels, Mariea Snell, Dorothea Dedeaux-Turner, Sara Hubert, and Kenneth Griffie, Washington University School of Medicine, St. Louis, Missouri.

Footnotes

Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

No conflict of interest exists for any of the authors.

Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

REFERENCES

  • 1.Hall HI, Song R, Rhodes P, et al. Estimation of HIV incidence in the United States. Jama. 2008 Aug 6;300(5):520–529. doi: 10.1001/jama.300.5.520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Marks G, Crepaz N, Janssen RS. Estimating sexual transmission of HIV from persons aware and unaware that they are infected with the virus in the USA. Aids. 2006 Jun 26;20(10):1447–1450. doi: 10.1097/01.aids.0000233579.79714.8d. [DOI] [PubMed] [Google Scholar]
  • 3.DHHS, editor. Vol Panel on Antiretroviral Guidlines for Adults and Adolescents. 2009. Guidelines for the Use of Antiretroviral Agents in HIV-1-Infected Adults and Adolescents. [Google Scholar]
  • 4.Quinn TC, Wawer MJ, Sewankambo N, et al. Viral load and heterosexual transmission of human immunodeficiency virus type 1. Rakai Project Study Group. N Engl J Med. 2000 Mar 30;342(13):921–929. doi: 10.1056/NEJM200003303421303. [DOI] [PubMed] [Google Scholar]
  • 5.Gray RH, Wawer MJ, Brookmeyer R, et al. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet. 2001 Apr 14;357(9263):1149–1153. doi: 10.1016/S0140-6736(00)04331-2. [DOI] [PubMed] [Google Scholar]
  • 6.Vellozzi C, Brooks JT, Bush TJ, et al. The study to understand the natural history of HIV and AIDS in the era of effective therapy (SUN Study) Am J Epidemiol. 2009 Mar 1;169(5):642–652. doi: 10.1093/aje/kwn361. [DOI] [PubMed] [Google Scholar]
  • 7.Caliendo AM, Jordan JA, Green AM, Ingersoll J, Diclemente RJ, Wingood GM. Real-time PCR improves detection of Trichomonas vaginalis infection compared with culture using self-collected vaginal swabs. Infect Dis Obstet Gynecol. 2005 Sep;13(3):145–150. doi: 10.1080/10647440500068248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Granich RM, Gilks CF, Dye C, De Cock KM, Williams BG. Universal voluntary HIV testing with immediate antiretroviral therapy as a strategy for elimination of HIV transmission: a mathematical model. Lancet. 2009 Jan 3;373(9657):48–57. doi: 10.1016/S0140-6736(08)61697-9. [DOI] [PubMed] [Google Scholar]
  • 9.Ciesielski CA. Sexually Transmitted Diseases in Men Who Have Sex with Men: An Epidemiologic Review. Curr Infect Dis Rep. 2003 Apr;5(2):145–152. doi: 10.1007/s11908-003-0051-5. [DOI] [PubMed] [Google Scholar]
  • 10.Brewer DD, Golden MR, Handsfield HH. Unsafe sexual behavior and correlates of risk in a probability sample of men who have sex with men in the era of highly active antiretroviral therapy. Sex Transm Dis. 2006 Apr;33(4):250–255. doi: 10.1097/01.olq.0000194595.90487.ed. [DOI] [PubMed] [Google Scholar]
  • 11.Benn PD, Rooney G, Carder C, et al. Chlamydia trachomatis and Neisseria gonorrhoeae infection and the sexual behaviour of men who have sex with men. Sex Transm Infect. 2007 Apr;83(2):106–112. doi: 10.1136/sti.2006.021329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Wolitski RJ, Fenton KA. Sexual health, HIV, and sexually transmitted infections among gay, bisexual, and other men who have sex with men in the United States. AIDS Behav. 2011 Apr;15(Suppl 1):S9–S17. doi: 10.1007/s10461-011-9901-6. [DOI] [PubMed] [Google Scholar]
  • 13.Kent CK, Chaw JK, Wong W, et al. Prevalence of rectal, urethral, and pharyngeal Chlamydia and gonorrhea detected in 2 clinical settings among men who have sex with men: San Francisco, California, 2003. Clin Infect Dis. 2005 Jul 1;41(1):67–74. doi: 10.1086/430704. [DOI] [PubMed] [Google Scholar]
  • 14.Mimiaga MJ, Mayer KH, Reisner SL, et al. Asymptomatic gonorrhea and chlamydial infections detected by nucleic acid amplification tests among Boston area men who have sex with men. Sex Transm Dis. 2008 May;35(5):495–498. doi: 10.1097/OLQ.0b013e31816471ae. [DOI] [PubMed] [Google Scholar]
  • 15.Schachter J, Moncada J, Liska S, Shayevich C, Klausner JD. Nucleic acid amplification tests in the diagnosis of chlamydial and gonococcal infections of the oropharynx and rectum in men who have sex with men. Sex Transm Dis. 2008 Jul;35(7):637–642. doi: 10.1097/OLQ.0b013e31817bdd7e. [DOI] [PubMed] [Google Scholar]
  • 16.Annan NT, Sullivan AK, Nori A, et al. Rectal chlamydia--a reservoir of undiagnosed infection in men who have sex with men. Sex Transm Infect. 2009 Jun;85(3):176–179. doi: 10.1136/sti.2008.031773. [DOI] [PubMed] [Google Scholar]
  • 17.Klausner JD, Wong W. Sexually Transmitted Diseases in Men Who Have Sex with Men: A Clinical Review. Curr Infect Dis Rep. 2003 Apr;5(2):135–144. doi: 10.1007/s11908-003-0050-6. [DOI] [PubMed] [Google Scholar]
  • 18.Buchacz K, Greenberg A, Onorato I, Janssen R. Syphilis epidemics and human immunodeficiency virus (HIV) incidence among men who have sex with men in the United States: implications for HIV prevention. Sex Transm Dis. 2005 Oct;32(10 Suppl):S73–S79. doi: 10.1097/01.olq.0000180466.62579.4b. [DOI] [PubMed] [Google Scholar]
  • 19.CDC. Primary and secondary syphilis--United States, 2003–2004. M. WR Morb Mortal Wkly Rep. 2006. 2006;55(10):269–273. [PubMed] [Google Scholar]
  • 20.Mansergh G, Flores S, Koblin B, Hudson S, McKirnan D, Colfax GN. Alcohol and drug use in the context of anal sex and other factors associated with sexually transmitted infections: results from a multi-city study of high-risk men who have sex with men in the USA. Sex Transm Infect. 2008 Nov;84(6):509–511. doi: 10.1136/sti.2008.031807. [DOI] [PubMed] [Google Scholar]
  • 21.Drumright LN, Little SJ, Strathdee SA, et al. Unprotected anal intercourse and substance use among men who have sex with men with recent HIV infection. J Acquir Immune Defic Syndr. 2006 Nov 1;43(3):344–350. doi: 10.1097/01.qai.0000230530.02212.86. [DOI] [PubMed] [Google Scholar]
  • 22.Fenton KA, Imrie J. Increasing rates of sexually transmitted diseases in homosexual men in Western europe and the United States: why? Infect Dis Clin North Am. 2005 Jun;19(2):311–331. doi: 10.1016/j.idc.2005.04.004. [DOI] [PubMed] [Google Scholar]
  • 23.Spindler HH, Scheer S, Chen SY, et al. Viagra, methamphetamine, and HIV risk: results from a probability sample of MSM, San Francisco. Sex Transm Dis. 2007 Aug;34(8):586–59123. doi: 10.1097/01.olq.0000258339.17325.93. [DOI] [PubMed] [Google Scholar]
  • 24.Buchacz K, McFarland W, Kellogg TA, et al. Amphetamine use is associated with increased HIV incidence among men who have sex with men in San Francisco. Aids. 2005 Sep 2;19(13):1423–1424. doi: 10.1097/01.aids.0000180794.27896.fb. [DOI] [PubMed] [Google Scholar]
  • 25.Purcell DW, Wolitski RJ, Hoff CC, Parsons JT, Woods WJ, Halkitis PN. Predictors of the use of viagra, testosterone, and antidepressants among HIV-seropositive gay and bisexual men. Aids. 2005 Apr;19(Suppl 1):S57–S66. doi: 10.1097/01.aids.0000167352.08127.76. [DOI] [PubMed] [Google Scholar]
  • 26.Dilley JW, Woods WJ, Sabatino J, Rinaldi J, Lihatsh T, McFarland W. Availability of combination therapy for HIV: effects on sexual risk taking in a sample of high-risk gay and bisexual men. AIDS Care. 2003 Feb;15(1):27–37. doi: 10.1080/0954012021000039734. [DOI] [PubMed] [Google Scholar]
  • 27.Marcus U, Bremer V, Hamouda O, et al. Understanding recent increases in the incidence of sexually transmitted infections in men having sex with men: changes in risk behavior from risk avoidance to risk reduction. Sex Transm Dis. 2006 Jan;33(1):11–17. doi: 10.1097/01.olq.0000187224.10428.31. [DOI] [PubMed] [Google Scholar]
  • 28.Mimiaga MJ, Goldhammer H, Belanoff C, Tetu AM, Mayer KH. Men who have sex with men: perceptions about sexual risk, HIV and sexually transmitted disease testing, and provider communication. Sex Transm Dis. 2007 Feb;34(2):113–119. doi: 10.1097/01.olq.0000225327.13214.bf. [DOI] [PubMed] [Google Scholar]
  • 29.Buchacz K, Patel P, Taylor M, et al. Syphilis increases HIV viral load and decreases CD4 cell counts in HIV-infected patients with new syphilis infections. Aids. 2004 Oct 21;18(15):2075–2079. doi: 10.1097/00002030-200410210-00012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Cohen MS. When people with HIV get syphilis: triple jeopardy. Sex Transm Dis. 2006 Mar;33(3):149–150. doi: 10.1097/01.olq.0000204530.19762.e4. [DOI] [PubMed] [Google Scholar]
  • 31.Kofoed K, Gerstoft J, Mathiesen LR, Benfield T. Syphilis and human immunodeficiency virus (HIV)-1 coinfection: influence on CD4 T-cell count, HIV-1 viral load, and treatment response. Sex Transm Dis. 2006 Mar;33(3):143–148. doi: 10.1097/01.olq.0000187262.56820.c0. [DOI] [PubMed] [Google Scholar]
  • 32.Incorporating HIV prevention into the medical care of persons living with HIV. Recommendations of CDC, the Health Resources and Services Administration, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR Recomm Rep. 2003 Jul 18;52(RR-12):1–24. [PubMed] [Google Scholar]
  • 33.Panel on Antiretroviral Guidelines for Adults and Adolescents. Guidelines for the use of antiretroviral agents in HIV-1-infected adults and adolescents. Department of Health and Human Services. 2009 Dec 1;:1–161. Available at http://www.aidsinfo.nih.gov/ContentFiles/AdultndAdolescentGL.pdf.
  • 34.Mayer KH, O'Cleirigh C, Skeer M, et al. Which HIV-infected men who have sex with men in care are engaging in risky sex and acquiring sexually transmitted infections: findings from a Boston community health centre. Sex Transm Infect. Feb 86;(1):66–70. doi: 10.1136/sti.2009.036608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Jin F, Prestage GP, Zablotska I, et al. High rates of sexually transmitted infections in HIV positive homosexual men: data from two community based cohorts. Sex Transm Infect. 2007 Aug;83(5):397–399. doi: 10.1136/sti.2007.025684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Fisher JD, Fisher WA, Cornman DH, Amico RK, Bryan A, Friedland GH. Clinician-delivered intervention during routine clinical care reduces unprotected sexual behavior among HIV-infected patients. J Acquir Immune Defic Syndr. 2006 Jan 1;41(1):44–52. doi: 10.1097/01.qai.0000192000.15777.5c. [DOI] [PubMed] [Google Scholar]
  • 37.Richardson JL, Milam J, McCutchan A, et al. Effect of brief safer-sex counseling by medical providers to HIV-1 seropositive patients: a multi-clinic assessment. Aids. 2004 May 21;18(8):1179–1186. doi: 10.1097/00002030-200405210-00011. [DOI] [PubMed] [Google Scholar]

RESOURCES