OVER THE LAST 20 YEARS, numerous studies have documented high rates of sexually transmitted infections (STIs) among persons previously diagnosed with human immunodeficiency virus (HIV).1–10 Additional reports have shown an increase in STIs over the past decade, particularly among men who have sex with men (MSM).11,12 STIs among people living with HIV are an important cause of morbidity and enhanced HIV transmission and may be indicative of ongoing behaviors related to risk of further HIV transmission.13–17 Screening, diagnosis, and treatment for STIs in people with HIV are important as both clinical and public health measures.
STIs are a continuing problem among all people with and at higher risk for HIV infection, including high-risk heterosexuals, injection drug users (IDU), and MSM.18–21 For example, epidemics of syphilis and gonorrhea among MSM have been ongoing in King County, Washington, and other geographic regions worldwide since the late 1990s.11,12,22–24 In response to endemic and recent epidemics of STIs, and because of enhanced transmission of HIV from untreated curable STIs, the Centers for Disease Control and Prevention (CDC) released the 1998 guidelines for HIV prevention through early detection of STIs.25 Additionally, in April 2001, Public Health, Seattle and King County (PHSKC) released local STI screening guidelines for MSM, the same year similar guidelines were released by the California State Department of Health.26,27 As MSM make up more than three-fourths of local residents living with HIV/AIDS, the PHSKC guidelines promote annual STI screening specifically for sexually active HIV-infected MSM but are applicable to other HIV-infected people at risk for STIs. Our analysis looks at trends in and factors associated with STI risk evaluations and screening in King County among a large cohort of HIV-infected patients.
To evaluate STI screening and risk assessments, we used data from the Adult/Adolescent Spectrum of HIV-Related Diseases (ASD) project. ASD was a CDC-sponsored medical record review surveillance project conducted in selected medical facilities in Seattle, Atlanta, Dallas, Denver, Detroit, Houston, Los Angeles, New Orleans, New York, Bayamon (Puerto Rico), and San Antonio. Seattle ASD data were collected from January 1990 through June 2004. HIV-infected persons aged ≥13 years who attended participating clinics were eligible for enrollment in ASD. Detailed methods used in ASD have been previously described.28 Briefly, medical record data were collected for a baseline period of up to 1 year, followed by 6-month intervals until death, relocation, loss to follow-up (defined as 18 months with no contact), or the end of the study. Data collected included demographic information, mode of exposure to HIV, antiretroviral and other medications prescribed, laboratory data, AIDS-defining opportunistic infections, other infections and conditions, STIs, and screening data for STIs. In Seattle, medical records were reviewed at 8 facilities, including private and publicly funded clinics and hospitals. Facilities included 3 clinics specializing in HIV care, 1 emergency care facility, and 4 privately and publicly funded general practice clinics/offices. Beginning in 2000, a supplementary data collection form was used to collect STI evaluation information. Therefore, this analysis is restricted to individuals seen during 2000–2004.
We examined data for patients with at least one outpatient visit to an ASD facility subsequent to the baseline interval, because having no outpatient visits or having only emergency room or inpatient visits would not necessarily have provided suitable opportunities for STI screening. We further selected all patients with outpatient visits between April 2000 and March 2003 that corresponded to the data collection periods. To assess trends in STI screening and evaluation, we considered 6-month time periods between April 2000 and March 2003. To ensure completeness of STI diagnoses, patients in this study were matched to the PHSKC Sexually Transmitted Disease (STD) Program database where all reported STI diagnoses are maintained. This database also included reasons for STI testing (e.g., symptomatic infection, exposure, routine testing, and unknown reason).
The types of STI screenings evaluated in this study were based on recommendations made in the PHSKC guidelines for STI screening of MSM. These guidelines recommended that MSM receive annual testing for HIV, syphilis, Neisseria gonorrheae, and Chlamydia trachomatis, with more frequent evaluation for MSM who have multiple and/or anonymous partners, who use illegal drugs, or who have partners that engage in these activities. Although PHSKC MSM STI screening guidelines do not specifically recommend screening for trichomoniasis, we included trichomoniasis in our analyses because it is the most frequently diagnosed curable STI in HIV-infected women, testing is recommended in the CDC/IDSA/HRSA guidelines on prevention in persons with HIV, and the infection may enhance transmission of HIV among heterosexuals.29,30 We defined having a risk assessment or STI evaluation (hereafter referred to as risk/STI evaluations) as one or more of 3 elements documented in the medical record: 1) information about the patient's recent sexual behavior; 2) referral to the local STD clinic; or 3) testing for Treponema pallidum (syphilis), Neisseria gonorrhoeae, C. trachomatis, and/or Trichomonas vaginalis (regardless of whether the test was conducted because of symptoms or not). We included an STI diagnosis even if test documentation was lacking in the medical record. Documentation of sexual history included references in the medical record to discussion of use of condoms or other barrier/contraceptive methods, number or serostatus of partners, disclosure of HIV serostatus, and types of sexual activities. STI testing methods included in this analysis were limited to 1) syphilis screening by rapid plasma regain and Venereal Disease Research Laboratory test with confirmatory testing using microhemagglutination test, fluorescent treponemal antibody absorption test or T. pallidum particle agglutination assay; 2) gonorrhea testing using a culture, Gram stain, or a nucleic acid amplification test; 3) chlamydia testing using culture, a nucleic acid amplification test, or enzyme immunoassays; and 4) trichomoniasis testing for female patients only by wet mount or culture.
We examined a number of demographic and medical characteristics, including HIV transmission risk, race/ethnicity, age at time of outpatient visit, type of facility (HIV or other), residence, any history of treatment with highly active antiretroviral therapy (HAART), and lowest CD4 cell count at time of outpatient visit. HIV transmission risk categories were defined as MSM, MSM who also inject nonprescription drugs (MSM/IDU), non-MSM IDU, other risk categories (heterosexual, perinatal, hemophilia, and blood transfusions), and unknown risk. STI incidence was calculated as new STI diagnoses over all person-years of observation.
Statistical analyses were conducted using SAS v.8.2 (SAS Institute, Cary, NC) and Epi Info 6 v.6.04 (CDC, Atlanta, GA). We analyzed risk/STI evaluation and the diagnoses of STIs over time using the χ2 test for trend. We also analyzed the subset of patients reported to Public Health with an STI to compare reasons for testing. To estimate odds ratios and 95% confidence limits for independent factors significantly associated with STI evaluation, we used PROC GENMOD for generalized estimating equations with exchangeable correlation structure to control for repeated observations of patients over time. Factors included in the regression model were demographic and clinical characteristics found to be significant in the trend analysis and factors reported as significantly associated with STI diagnosis or evaluation in the medical literature.
Of the 4711 patients in the ASD cohort, 1720 were seen at an ASD facility between April 2000 and March 2003. Of these, most patients were male, over half were white, and the majority were between 30 and 50 years of age (Table 1). Of the known transmission risks, over half were MSM, including MSM/IDU. Most of the patients lived in Seattle, were seen at an HIV specialty clinic and had a history of HAART use. Trend analysis for 6-month intervals showed statistically significant increases in the proportions of women, blacks, people of Hispanic ethnicity, older patients (50 years and more), patients being seen at HIV specialty clinics, and patients with CD4 counts ≥350 cells/μL at the time of each interval. Significant decreases were seen among the proportions of men, patients aged 30 to 39 years, patients with IDU or MSM/IDU transmission risk, and patients with a CD4 count <350 cells/μL.
In bivariate analyses, patients significantly more likely to be evaluated for risk/STIs included patients <40 years of age, patients receiving primary care at an HIV specialty clinic, and patients seen more recently. Patients significantly less likely to receive a risk/STI evaluation were patients with any history of HAART, patients with a CD4 count <350 cells/μL, and patients with an average of 3 or fewer outpatient visits in an interval. Although not significant, women had a higher proportion of risk/STI evaluation than men, MSM had a higher proportion of risk/STI evaluations compared with IDU. Adjusting for all other factors in the regression model, risk/STI evaluations were significantly more likely to be performed if the patient was MSM, younger, seen at an HIV specialty clinic, or had an outpatient visit in later intervals. A history of HAART use, CD4 count <350 cells/μL, an average of 3 or fewer outpatient visits per interval and nonwhite race/ethnicity was inversely associated with risk/STI evaluations.
In the year before the release of the STI screening guidelines, an average of 23% of patients were evaluated for risks/STIs in two 6-month periods. In the 2 years after the release of the guidelines, an average of 46% patients were evaluated for risks/STI in two 6-month periods (Fig. 1). χ2 for trend shows a significant increase in risk/STI evaluation from April 2000 through March 2003 (P <0.05). This increase was present for all HIV-infected patients followed, regardless of demographic and clinical characteristics. Documentation of HIV medical providers taking a sexual history rose from 8% in the first 6-month period to 35% in sixth 6-month period, and testing for any STI increased from 12% in 2000 to 30% in 2003. Referrals to the local STD clinic did not significantly increase. Overall, all 3 types of risk/STI evaluations combined (testing, history taking, and referral) increased significantly from 16% to 47% (P <0.05). Syphilis was the most common STI for which testing was noted, followed by gonorrhea, chlamydia, and trichomoniasis (women only) (Fig. 2). From early 2000 to 2001, testing increased for all STIs; syphilis 13% to 25%, gonorrhea 6% to 9%, chlamydia 6% to 10% (P <0.05 for all).
The number of new diagnoses of specified STIs fluctuated over time (Fig. 3). The average percent testing positive in a year was 1% for syphilis, 4% for gonorrhea, and 2% for chlamydia among the patients evaluated for STIs. The incidence of gonorrhea and all STIs increased over the period of observation (P <0.05). Patients under 30 years of age, seen in an HIV specialty clinic, and with no history of HAART had a significantly higher incidence of STIs; patients with a CD4 count ≥350 cells/μL had a lower incidence of STIs. Young MSM under 30 years of age were found to have a higher incidence of STIs diagnosed than other MSM or any other HIV risk group (P <0.05).
From the STD Program database, 155 patients with STI diagnoses, based on tests, were matched to patients in this study to review reasons for testing. Of these, 114 (74%) patients diagnosed with at least one STI reported symptoms as the reason for testing for STIs. Other reasons given for testing included routine screening (16%), exposure to an STI (6%), and no reason given/unknown (5%) The proportion of patients reporting symptoms increase significantly (P <0.05) during the study period for all STIs (47%–87%) and specifically for chlamydia (25%–89%).
Between April 2000 and March 2003, risk/STI evaluation rates increased significantly for MSM and leveled out in the subsequent intervals. Several factors could have contributed to this trend. First, the increase could have resulted from the release of PHSKC guidelines and associated public health efforts to promote STI testing, particularly as they are related to the health department's syphilis elimination program based on the national Syphilis Elimination Effort.31 The increase in testing was most dramatic in the 6 months periods before and after release of the local STI screening guidelines. The fact that so much of the observed increase occurred before the guidelines actual release, as well as previous research suggesting that development of guidelines alone is not effective in changing physician behavior32–34 suggest that the guidelines may not have been the primary cause of the observed change. Second, the growing STI epidemic in King County, particularly the syphilis epidemic, may have prompted clinicians to increase their evaluations related to sexual risk and STI. In this study, testing for syphilis was by far greater than any other STI. However, testing for other STIs also increased significantly. Third, increases in testing may have been because of the increases in patients reporting symptoms associated with STIs. The analysis of a subset of the study cohort showed an increase in the proportion of STI-positive patients reporting symptoms as the reason for testing. However, this analysis was limited to only patients with a diagnosis of an STI, and because only a small proportion of tests was positive, an increase in symptomatic infections alone cannot explain the observed increase in testing. ASD data were limited by not having a mechanism for reporting reason for STI evaluation for the entire cohort and information about symptomatic infection could not be ascertained. Last, increases in documenting sexual history were possibly a result of increased awareness of risky sexual behaviors among HIV-infected people and its impact on HIV transmission. In the last several years, widely disseminated research has shown the need for greater emphasis on the sexual behaviors of HIV-infected patients in an effort to prevent further transmission and has encouraged providers to discuss and document sexual behaviors of patients.35–38
MSM were more likely to be evaluated for risk/STIs than other HIV risk groups and were more likely to be evaluated after the guidelines were released. This is no surprise because MSM make up the highest proportion of HIV infections in King County, local guidelines were developed to increase STI testing among MSM, and the increases in STIs in King County have specifically impacted MSM. Younger MSM seen at HIV clinics seem to be the group most associated with risk/STI evaluation as well as having a higher likelihood of being diagnosed with an STI. Other studies have also shown that young MSM are more likely to participate in high-risk sexual activities and be diagnosed with an STI. Therefore, young MSM may be targeted by providers for risk/STI evaluation.39–41
This study was limited by several factors. ASD data were drawn from a convenience sample and may not be representative of the HIV epidemic locally or nationally. However, the demographic composition of people followed by ASD is very similar to the HIV-infected population of King County.42 Also, STI evaluation rates analyzed in this study were limited to HIV-infected people in care at specific clinics and may not reflect broader trends in the community. Because the ASD project relied solely on medical record abstractions, STI diagnoses, tests, and sexual histories could have been missed or not well documented. Finally, although data on STI diagnoses have been collected for ASD patients since 1990, documentation of risk/STI evaluations was not regularly collected until 2000. However, the accuracy of these data have been verified through repeat record abstraction audits, double data entry protocols, and comprehensive error seeking procedures. Additionally, patients in the ASD cohort were matched to PHSKC STD data to increase completeness of reporting diagnoses of STIs.
In summary, we found that the proportion of persons with HIV in King County who underwent some documented evaluation for sexual risk or STI increased between 2000 and 2001 but is now stable. The likelihood of being evaluated was lower in identifiable groups of patients, including persons receiving care outside of HIV specialty clinics. Although our findings are encouraging insofar as they suggest that clinicians increased the number of persons they evaluated for ongoing sexual risks and STI concurrent with widespread recognition of a burgeoning STI epidemic in MSM, they also demonstrate the need for substantial improvements. In any given 6-month period, only approximately one-third of patients seen for HIV care has any evidence of a sexual history documented in their chart. A similar number are tested for any STI, though STI testing is limited to syphilis serological testing along in most instances. A much more concerted and organized effort to promote prevention and STI control among persons with HIV is required.
Guidelines for STI testing among all HIV-positive patients recommend routine testing for gonorrhea and chlamydial infection, although this testing has been relatively uncommon. Such testing is more time consuming for clinicians and invasive for patients than serological testing for syphilis, as routine HIV care already includes phlebotomy to monitor disease progression. Promoting nonsyphilis STI testing clearly requires additional effort. Efforts to have such testing done routinely by persons other than clinicians, possibly via self-obtained swabs, merit further evaluation.
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