THERE ARE APPROXIMATELY 1.0 TO 1.2 MILLION persons living with HIV in the United States, of which an estimated one-quarter are unaware of their diagnosis.1 With the recent recommendations promoting universal HIV screening for all adolescents and adults in all healthcare settings, understanding population-based risk factors for HIV acquisition are crucial to designing preventive programs impacting trends in HIV transmission.2 In 2003, strategies at a national level were initiated to assist state and local health departments monitor selected behaviors through face-to-face surveys among groups at highest risk for HIV infection.3 Data from these survey tools may be enhanced when coupled with information from biologic determinants contributing to HIV transmission. Localized infections with sexually acquired bacterial diseases facilitate transmission and acquisition of HIV through several mechanisms, including boosting HIV shedding in genital secretions, increasing recruitment of HIV-susceptible inflammatory cells to the genital tract, and disrupting mucosal barriers to HIV invasion.4 Persons with sexually transmitted diseases (STDs) may constitute a bridge for HIV transmission from high-risk groups to the general population.5,6
In Illinois, public health, institutional, and various community-based clinics offer confidential testing for STDs and HIV. Testing is available to diverse populations throughout the state, including persons seeking evaluation through school-based and neighborhood health clinics, family planning and prenatal clinics, drug treatment centers, correctional institutions, TB and anonymous HIV clinics, county health departments, hospitals and private physicians, and STD clinics. In this study, we used statewide surveillance data in Illinois to determine demographic and behavioral factors associated with newly diagnosed HIV infection among persons with a concomitant STD within the general population attending public health clinics.
Laboratory results, demographic, and risk behavior data from all encounters to Illinois public health providers in 2002 during which both HIV and bacterial STD (Chlamydia, gonorrhea, and/or syphilis) specimens were collected at the same visit and submitted to the Illinois Department of Public Health (IDPH) laboratory for testing were included in the analysis. Urine or urethral specimens with nucleic acid amplified tests positive for Chlamydia or gonorrhea were designated laboratory-confirmed cases. Early syphilis cases were defined as serum specimens reactive for fluorescent treponemal antibody absorbed and a nontreponemal rapid plasma reagin (RPR) or venereal disease research laboratory (VDRL) titer ≥1:8, with a diagnostic code of primary, secondary, or early latent syphilis determined by IDPH or Chicago Department of Public Health (CDPH) STD programs based on field investigation information corroborated by medical record reports of signs and symptoms of infection. Serum specimens with a screening enzyme immunoassay positive for HIV were laboratory-confirmed by Western Blot. Repeat visits by the same patients were included, as HIV or STD status may have changed throughout the year.
At each clinic visit, patients undergoing confidential testing for STD and HIV are asked to fill out a risk behavior survey that includes sexual and social behavior information. At CDPH facilities, physicians, or nurse practitioners administered the behavioral survey to patients through face-to-face interviews and documented responses to the medical record. In IDPH sites outside Chicago, risk assessment surveys were self-administered by patients and reviewed by clinic personnel, and then forwarded to the IDPH STD program. Surveys were required by IDPH for all STD clinics. Behavioral risk surveys obtained information regarding patient sexual orientation, condom use (never, sometimes, always), number of sexual partners during the past 2 to 12 months (none, one, or >1), history of ever been diagnosed with an STD, history of ever being tested for HIV and result, injection drug user (IDU), sex with an IDU, history of snorting drugs, history of exchanging sex for drugs or money, sex while drinking alcohol or using drugs, and history of ever having sex or shared injection needles with a known HIV-positive person.
The IDPH laboratory results for Chlamydia, gonorrhea, and syphilis were merged with HIV laboratory results and matched with behavioral risk data collected during patient visits. To maintain confidentiality, HIV results were reportable by a unique 12-character patient code number (PCN). STD test results were reported by name. Case-specific STD identifier data were converted to emulate the HIV unique PCN in preparation for matching the databases. Risk behavior survey and all laboratory results from IDPH and CDPH surveillance systems were standardized, matched, and merged.
For analysis, “Any STD” was defined as an encounter with a positive Chlamydia, gonorrhea, and/or early syphilis result. All newly diagnosed HIV-positive results are newly recognized cases without a known prior history of HIV in the IDPH or CDPH reporting systems or without an affirmative response to the question in the risk assessment survey to determine if the patient is known to be HIV-positive. Univariate and bivariate analyses using variables derived from demographic and risk factor survey data compared STD-positive and newly recognized HIV-positive cases to STD-positive and HIV-negative cases. An additional bivariate analysis examined distinct STDs as factors associated with newly diagnosed HIV in STD-positive cases. Student t test were used to compare means of continuous variables such as age at clinic visit. The Mantel-Haentzel χ2 test, or Fisher exact test where appropriate, were used to calculate odds ratios (OR) with 95% confidence intervals (CIs) and related P values. Cases for which risk assessment surveys were not collected were excluded from the risk behavior analysis. Unconditional multivariable logistic regression was performed to identify factors independently associated with laboratory-confirmed STDs concomitant with newly diagnosed HIV and to adjust for potential confounding and multiplicative interaction. Variables approaching significance (α ≤ 0.10) in bivariate analysis were considered in the multivariable models. Cases missing values for any variable selected in the multivariate models were excluded in the final analysis. All analysis was performed using SAS version 8.2 (SAS Institute, Cary, NC).
In Illinois in 2002, there were a total of 28,232 patient visits to STD clinics and 15,285 patient visits to non-STD clinic sites. Risk behavior surveys were available for 27,609 encounters, representing 25,575 individual patients (Fig. 1). Among the 43,517 patient encounters during which specimens were collected concomitantly for STDs and HIV, there were 5814 (13.4%) positive STD results.
Patients aged ≥30 years constituted the largest age group (35.2%) among encounters, but represented only 21.8% of visits with positive STD test results. The age group with the highest number of positive STD test results was 20 to 24 years, representing 28.5% of all encounters. The majority (56.3%) of positive STD test results was among men, but women accounted for the majority (57.9%) of all encounters. Nearly one-half (49.5%) of all encounters identified themselves as non-Hispanic black; the majority (70.7%) of positive STD test results were among non-Hispanic blacks. Most (59.0%) of the encounters took place in facilities outside of Chicago, but the majority (55.5%) of positive STD tests were from CDPH-based clinics (Table 1).
Sexual orientation was derived from 61.8% test reports in which risk behavior data were available. Heterosexuals accounted for 88.1% of derived sexual orientation data and 76% of all positive STD test results. A majority (56.6%) of the patients with positive STD test results reported “sometimes” using condoms. The number of sex partners reported within 2 to 12 months of the visit was unknown in 39.0% of the cohort. One sexual partner and >1 sexual partners within 2 to 12 months of the visit were reported in nearly the same proportion of the cohort (29.4% and 29.0%, respectively). Among patients with positive STD test results, 46.3% had >1 sexual partner within 2 to 12 months and 33.2% had one partner within 2 to 12 months (Table 2).
Risk behavior data showed that 30.9% of encounters had a self-reported previous STD and 39.7% had been tested previously for HIV. Forty-four percent of encounters with positive STD test results had reported a previous STD and 50.3% of encounters with positive STD test results had reported been previously tested for HIV. Data were not collected for any of the risk behaviors among 36.6% of all encounters.
There were 308 (0.7%) newly recognized HIV-positive test results. Detection of any STD was associated with newly diagnosed HIV infection (OR = 1.9, 95% CI 1.5–2.5). Among the 308 patients, 71 (22.7% of newly recognized HIV infections and 0.2% of the patient encounter cohort) were coinfected with an STD as defined by a concomitant positive STD test result. Bivariate analysis indicated a statistically significant association with coinfection between patients aged ≥30 years (OR = 2.3; 95% CI 1.3–3.9), men (OR = 3.5; 95% CI 1.9–6.3), men who have sex with men (MSM) (OR = 17.9; 95% CI 11.0–29.1), MSM who are IDUs (OR = 41.4; 95% CI 10.2–168.7), bisexual men (OR = 10.1; 95% CI 4.3–23.9), men with unknown sexual orientation (OR = 2.5; 95% CI 1.3–5.1) (data not shown), attending a CDPH-based clinic (OR = 2.2; 95% CI 1.3–3.7), and those whose response to having sex while drinking or using drugs was unknown (OR = 2.4; 95% CI 1.1–5.6) (data not shown). Patients aged 15 to 19 years (OR = 0.31; 95% CI 0.12–0.81) and heterosexual (OR = 0.08; 95% CI 0.05–0.13) were statistically significantly associated with a lower risk of HIV and STD coinfection (Tables 1 and 2). Among distinct STDs reported, syphilis was the most infrequent (7.5%), but showed the highest frequency (43.7%) and greatest risk (OR = 11.0, 95% CI, 7.7–15.8) for newly diagnosed HIV in concomitant infections (Table 3).
In the logistic regression model, 48 patients with concomitant STD and newly diagnosed HIV were analyzed. After controlling for potential confounders such as non-Hispanic black ethnicity, age ≥30 years (OR = 1.9; 95% CI 1.0–4.4), MSM (OR = 22.2; 95% CI 11.3–43.7), and bisexual male (OR = 22.4; 95% CI 7.8–64.8) were independently associated with newly diagnosed HIV and STD coinfection (Table 4).
Surveillance tracking visits to statewide public health clinics in which tests for HIV and at least one STD were performed showed a high proportion, nearly one-quarter, of newly diagnosed HIV patients were concomitantly infected with a laboratory-confirmed bacterial STD. The greatest risk factors for STD and newly diagnosed HIV coinfection were MSM and older age (≥30 years). In 2002, an estimated 51% of all recently acquired HIV infections in the United States were among MSM, consistent with previous years within the past decade.7 In our study, examining a subset of patients screened concomitantly for STDs and HIV among a large general population, 50% of cases with known sexual behavior history with newly diagnosed HIV and a concurrent STD were among men reporting sex with men, paralleling national data for newly acquired HIV infection.
In HIV epidemics concentrated in core groups, such as MSM in the United States, the principal STDs that amplify HIV transmission are typically bacterial ulcerative and inflammatory infections, as opposed to generalized epidemics, notable in sub-Saharan populations, in which genital herpes replaces bacterial STDs as an infectious cofactor.8–11 Gonorrhea, syphilis, and, to a lesser extent, Chlamydia are associated with higher amounts of HIV in genital secretions.4,12–15 To maximize the likelihood that we evaluated active STDs, rather than potentially nonspecific genital conditions or ill-defined urethritis, we limited our criteria for concomitant STDs to only laboratory-confirmed gonorrhea or Chlamydia cases or early syphilis cases established through public health investigation in addition to laboratory confirmation. Our results highlight the role in particular of syphilis among populations at high risk for HIV transmission. With 44% of concurrent STD and newly diagnosed HIV cases identified with early syphilis, syphilis showed the highest frequency and greatest risk associated with newly diagnosed HIV in concomitant infections. It is possible that early syphilis cases may also have been underestimated because the surveillance definition for early syphilis may not capture very early primary cases that have negative or low titer nontreponemal test results with positive darkfield microscopy or compatible chancre. In Chicago, syphilis cases among MSM peaked in 2002. By 2004, syphilis cases declined by 23%. However, in 2005 a high incidence rate of syphilis among MSM reemerged with a 25% increase despite a targeted social marketing campaign.16
In major US cities, an increasing number of concurrent syphilis and HIV infections are being reported, with an estimated prevalence of 20% to 50% among MSM.17–19 Since 2001, there has been a dramatic resurgence in primary and secondary syphilis reported nationally, with a 46% increase in reported cases by 2005, of which 65% occurred in MSM. Men overall accounted for 86% of all persons with acute syphilis in 2005.17 An increase in syphilis has also been observed in heterosexual populations during this 5-year period.6 Among men reporting sex with men in our study with newly diagnosed HIV and a concurrent STD, 17% identified themselves as bisexual. This proportion is similar to national survey data showing 14% of 10,030 MSM reported engaging in anal, vaginal, or oral sex with a female partner during the preceding 12 months, of which the highest prevalence of unprotected intercourse was with their female partners.20 Our data support the potential among persons with high-risk sexual behavior to further the HIV epidemic beyond core groups into the general population.
Age ≥30 years represented the age group with the highest proportion (44%) of newly diagnosed HIV cases with a concomitant STD, and was an independent risk factor for this outcome in our study. This age group is older than US populations that generally constitute the greatest proportion of STD cases. The risk for coinfection in this age group was analyzed regardless of sexual orientation, though may have been influenced by older MSM included within this factor; MSM showed an approximately 10-fold higher magnitude of adjusted risk than older age itself. In the first report of the National HIV Behavioral Surveillance System during the first cycle of interviews among 13,670 MSM from November 2003 to April 2005, 77% reported being tested for HIV during the preceding 12 months, but only 43% reported having been tested for syphilis, gonorrhea, or another STD during that same time period. Rates of STD testing were less common among MSM aged >35 years than in younger MSM populations.20 Among STD clinics in Baltimore from 1993 to 2002, 66% of all new HIV seroconversion cases were aged ≥30 years. Genital ulcer disease and syphilis were associated with a much higher HIV seroconversion risk.21 In MSM populations, concomitant gonoccocal or chlamydial infections were present in 25% and 18%, respectively, among newly recognized HIV-positive patients screened at urban STD clinics in San Francisco from 2004 to 2006. The median age of these cases was 34 years.22 Several factors may explain these findings. MSM with large numbers of anonymous partners, likely thus of unknown HIV serostatus, have been targeted by syphilis screening programs in nonmedical settings, such as bars, bathhouses, and sex venues, during syphilis outbreaks in many metropolitan US cities since 2000.23 Persons may not seek medical attention until several years after HIV acquisition because of the relative asymptomatic natural history of disease within the first decade of infection. Upon HIV screening in persons with a suspected STD, individuals with previously undiagnosed HIV are identified as newly recognized HIV cases. Together, these recent data underscore the need for greater emphasis and expanded testing for bacterial STDs at public health and STD clinics among high-risk populations for HIV acquisition, especially MSM and persons aged ≥30 years, for which prompt treatment of these curable bacterial STDs may impact transmission patterns of HIV.
Our study had several limitations. There was a small degree of recidivism, 7.4% of all encounters with available risk behavior data; therefore, risk factors cannot be completely attributable to distinct individual patient reporting patterns. However, no duplicate encounters were analyzed as we were able to determine each encounter as a singular visit by cross-matching PCN, name, and birth date data from two separate sources (clinic records and laboratory submission and reporting records). We did confirm that each newly diagnosed HIV infection, the endpoint for our comparative analysis, represented a unique patient. Our analysis was limited by the high proportion of missing data from the risk behavior surveys. Approximately one-third of all questions were not filled in by patients, which often rendered modifiable behaviors that were “unknown” as the most extreme risk in the analysis. The missing data may be ascribed to the unavailability of surveys or trained facilitators at numerous clinics that provided testing, chiefly the non-STD clinical settings. Potential barriers that preclude the administration of these surveys in various settings should be explored and resources should be allocated where possible to promote survey completion, particularly as expanded policies for “opt-out” HIV testing are introduced into general clinical practices. In addition, risk behaviors that are self-reported may be inherently unreliable if collected in settings lacking trained personnel and interpreters where needed. By not incorporating gonococcal and Chlamydia detection to sites other than genital areas, and excluding other genital ulcerative diseases associated with HIV acquisition, in particular active herpes infections, for which sensitive and specific diagnostic tools for active infections are not readily available in the clinical setting, we may have underestimated the full spectrum of concomitant STDs that can contribute to newly recognized HIV infections.
Our study featured a few advantages over many relevant longitudinal studies. Most published studies that have investigated the interaction between STDs and HIV susceptibility have been prospective cohort or nested case control studies with a median subject size of approximately 850.24 Numerous population-based studies in the United States have also examined risks for subsequent STDs in persons with known HIV infection in STD clinic settings.25–29 Our study assessed a large database that used integrated laboratory, clinic surveillance, and self-reported behavioral risks that is likely more representative of a broad demographically diverse population attending public health STD clinics than cohort studies and evaluated risk factors in a multivariate model that are perhaps unique to concomitant STD and newly recognized HIV infection.
Of the estimated 40,000 new HIV infections acquired annually in the United States, the proportion transmitted by those unaware of their seropositive status or coinfected with STDs is unknown.30 Recently, intensive testing and social marketing campaigns have targeted core groups at increased risk for STD and HIV transmission, most cogent are syphilis control programs among MSM populations in major US cities. Despite these efforts, consistent declines in early syphilis and HIV incidence have not occurred, and might have increased within these networks.16,31–40 As universal HIV screening recommendations without extensive pretest counseling are introduced in healthcare settings serving adolescents and adults, STD screening programs and prompt treatment should be concurrently implemented. Innovative public health strategies that support complete and accurate information regarding risk behaviors should be created to advance our understanding of modifiable factors for STDs and HIV seroconversion within the general population.
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