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Original Article

A Population-Based Study of Sexually Transmitted Disease Incidence and Risk Factors in Human Immunodeficiency Virus-Infected People

BELONGIA, EDWARD A. MD*; DANILA, RICHARD N. PhD, MPH; ANGAMUTHU, VELMURUGAN BS; HICKMAN, CYNTHIA D. MPH; DeBOER, JILL M. MPH; MacDONALD, KRISTINE L. MD, MPH; OSTERHOLM, MICHAEL T. PhD, MPH

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Sexually Transmitted Diseases: May 1997 - Volume 24 - Issue 5 - p 251-256
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Abstract

SEVERAL STUDIES have examined the risk of human immunodeficiency virus (HIV) seroconversion among people with sexually transmitted diseases (STDs), and there is evidence that both genital ulcer disease and nonulcerative STDs may increase the risk of HIV transmission.1–6 However, little is known about the incidence of STDs among people with known HIV infection. Previous studies of STD clinic clients have shown high STD rates among clients who were HIV infected. At the Baltimore STD clinics, 9.7% of HIV-infected clients were diagnosed with an STD during the 6- to 23-month follow-up period.7 In the Miami STD clinics, large cohorts of HIV-positive and HIV-negative clients were compared for the period 1988 to 1992.8 The percentage of clients who were diagnosed with a new STD was similar in the two groups, but return visits with an STD within 1 year decreased in each group from about 16% in 1988 to about 3% in 1992. However, these studies were restricted to a selected subset of HIV-infected people (those visiting an urban STD clinic), and they were unable to assess the number of people who were lost to follow-up. To assess the occurrence of STDs in an unselected population of HIV-infected people, we studied a population-based cohort of HIV-infected people in Minnesota over a 2-year period.

Methods

Statewide surveillance for cases of HIV infection, gonorrhea, Chlamydia trachomatis infection, and syphilis has been carried out in Minnesota since 1985 or earlier. Since 1992, STD records have been stored in a computerized database that facilitates cross-matching with HIV records. For this investigation, we examined the incidence of reportable STDs in 1993 to 1994 among people who had been diagnosed with HIV infection or acquired immunodeficiency syndrome (AIDS) before 1993. We also used data routinely collected through HIV/AIDS surveillance to assess risk factors for STD acquisition in this population.

All licensed health care providers and laboratories are required to report cases of HIV infection (including AIDS), gonorrhea, chlamydial infection, and syphilis to the Minnesota Department of Health. HIV/AIDS cases are ascertained through both active and passive surveillance. Active surveillance includes monthly contact with all 14 HIV/AIDS clinics and 25 major acute-care hospitals in the state to identify new cases and update the status of previously reported cases. In addition, all positive HIV serologic tests are reported by six Minnesota laboratories and two out-of-state laboratories that perform confirmatory Western blot testing for Minnesota residents. Laboratory reports are followed up to ascertain cases. Passive surveillance is based on case reports submitted by physicians, hospitals, clinics, drug abuse treatment centers, blood/plasma collection centers, correctional facilities, military facilities, U.S. Job Corps facilities, and other sites.

Surveillance for STDs other than HIV/AIDS (i.e., gonorrhea, chlamydial infection, and syphilis) is based on reporting by physicians and clinics with supplementation by laboratory reports. Laboratory reports are used to identify cases from nonreporting physicians. For reporting purposes, a case of gonorrhea or chlamydial infection is defined as a written report submitted by a physician and confirmed by a positive laboratory test (culture or other test). A syphilis case is defined as a written report submitted by a physician and confirmed by a reactive serologic test for syphilis (reactive nontreponemal test with fluorescent treponemal antibody confirmation) or direct detection of Treponema pallidum. The following information is collected for each case: patient name, street address, city, zip code, date of birth, date of diagnostic test, gender, race, ethnicity, diagnosis, site of infection, treatment, and reporting source. STD case reports have been maintained in a computerized database since 1989 for gonorrhea and 1986 for chlamydial infection. However, individual identifying data (name and date of birth) were not entered before 1993.

For this analysis, we identified surveillance records for people who were reported to have adolescent/adult HIV infection or AIDS (age greater than 12 years) with an initial positive HIV test before January 1, 1993. People who had died before January 1, 1995, were excluded, as were people with a missing or incomplete date of birth. The HIV records were matched against the database of people who were diagnosed with gonorrhea, chlamydial infection, or primary/secondary syphilis from January 1, 1993 through December 31, 1994. The following fields were used for matching: last name, first name, date of birth, and gender. Matching records were defined as those with identical entries in all four fields. First names that are considered synonymous (e.g., William and Bill) were accepted as identical entries. For each matching record, STD case information was abstracted and entered into the HIV database.

Gonorrhea rates were calculated for the cohort and standardized to the age distribution of the Minnesota population in 1993 for comparison. Statewide rates for gonorrhea were calculated from 1993 population estimates and compared with the HIV-infected population. Confidence intervals for rate ratios were estimated by logarithmic transformation.9 Risk factors for diagnosis of one or more STDs were examined by univariate analysis. Odds ratios (OR) and exact 95% confidence intervals (CI) were calculated with standard microcomputer software (Epi-Info 6.0; Centers for Disease Control and Prevention, Atlanta, GA). The chi-square or two-tailed Fisher's exact test were used to test differences in categorical variables. The Wilcoxon rank sum test was used to test differences in continuous variables. Variables significantly associated (P < 0.10) with STD acquisition were entered into a stepwise multiple logistic regression model (SPSS 6.0; SPSS, Inc., Chicago, IL).

Results

There were 2,328 people diagnosed with HIV infection or AIDS from 1983 through 1992 who were still alive as of December 31, 1994. Of these, 13 (0.6%) were excluded from further analysis because the date of birth was missing or incomplete. The remaining 2,315 constituted the cohort for analysis (Table 1). Ninety percent were white (not Hispanic) men, and 83% were 25 to 44 years of age. The median age was 34 years (range, 16–74 years) and the median year of initial HIV diagnosis was 1989. Over three fourths lived in Hennepin County or Ramsey County, the two most densely populated urban counties in Minnesota. The most common HIV transmission categories among men and women were male-to-male sex and heterosexual contact, respectively. AIDS developed in approximately one third from 1985 through 1994.

TABLE 1
TABLE 1:
Characteristics of Adolescents/Adults With HIV Infection/AIDS in Minnesota Before 1993 and Still Alive as of December 31, 1994

Thirty (1.3%) of 2,315 HIV-infected people were diagnosed with one or more episodes of gonorrhea, chlamydial infection, or primary/secondary syphilis in 1993 or 1994. Twenty-one (70%) were male and 19 (63%) were white (not Hispanic). The median interval from initial HIV diagnosis to STD diagnosis was 3 years (range, 6 months to 8 years). Among men, the HIV transmission category was male-to-male sex for 17 (81%), male-to-male sex and injecting drug use for 3 (14%), and not specified for 1 (5%). Among women, the HIV transmission category was injecting drug use for three (33%), heterosexual contact for two (22%), and not specified for four (45%). All 30 received HIV risk reduction counseling when initially notified of their positive HIV test result, and 19 (63%) received at least two counseling sessions. All risk reduction counseling sessions were provided by specially trained staff members employed by the Minnesota Department of Health.

There were 24 people (18 men and 6 women) with 31 episodes of gonorrhea; 4 (17%) had 2 or more episodes. All people with multiple episodes were male. Of the 25 episodes in men, 21 (84%) were urethral and 4 (16%) were rectal. Among women, the site of infection was the cervix in five and unknown in one. There were seven people (four men and three women) diagnosed with chlamydial infection. All three women had cervical infections; two of the men had urethral infections and for two the site was not specified. There were no people with multiple episodes of chlamydial infection, but two men were diagnosed with both chlamydial infection and gonorrhea. There was one diagnosis of secondary syphilis.

The age-adjusted gonorrhea incidence rate was 10-fold higher in the cohort of HIV-infected people compared to the general population in Minnesota (Table 2). The rate ratios comparing HIV-infected to non-HIV-infected were similar for men and women, but they were higher in older age groups compared to people 15 to 24 years old. The rate ratio was significantly elevated for whites (not Hispanic), and for residents of both urban (Hennepin, Ramsey) and rural counties.

TABLE 2
TABLE 2:
Rates of Reported Gonorrhea in 1993–1994 Among Adolescents and Adults With HIV Infection/AIDS Before 1993 Compared With All Other Minnesota Residents

Several factors were associated (P < 0.10) with a diagnosis of one or more STDs by univariate analysis (Table 3). These included female gender, residence in Hennepin County, younger age, more recent year of initial HIV diagnosis, and lack of AIDS diagnosis (before January 1993). Of the nine women with a reported STD, seven were residents of Hennepin County and five were black (not Hispanic). Twenty (1.2%) of 1,623 men with a history of male-to-male sex were diagnosed with an STD, compared to none of 308 men with another risk factor for HIV transmission (excluding those with risk undetermined or not specified; OR undefined; P = 0.06).

TABLE 3
TABLE 3:
Univariate Analysis of Risk Factors for STD Diagnosis in 1993–1994 Among Persons With Known HIV Infection/AIDS Before 1993

In a stepwise logistic regression model, the only independent risk factors for HIV diagnosis were female gender (OR 3.8; 95% CI, 1.7–8.4; P = 0.001) and Hennepin County residence (OR 2.6; 95% CI, 1.1–6.5; P = 0.035). Risk factors for STD diagnosis among HIV-infected men were analyzed in a separate logistic regression model that included HIV transmission mode (male-to-male sex vs. all others) as an independent variable. STD diagnosis was not significantly associated with any of the variables examined.

Discussion

To our knowledge, this is the first study to use surveillance data to assess STD incidence in a population-based cohort of HIV-infected people. Other studies of STD incidence in HIV-infected people have been based on people attending STD clinics,7,8 and these clinic populations are not representative of all HIV-infected people in a city or state. The availability of computer technology has increased the capacity for public health agencies to link HIV and STD surveillance data, and this can be helpful for the evaluation of HIV/STD prevention programs. Information on the effectiveness of these programs is often hard to obtain, but the incidence of STDs among HIV-infected people provides a surrogate measure of high-risk sexual behavior in that population. A declining STD incidence in the HIV-infected population would support the effectiveness of HIV prevention efforts, whereas an increasing STD incidence would suggest a need for additional interventions.

People infected with HIV in Minnesota had a significantly increased incidence of reported gonorrhea relative to the general population. However, less than 2% of HIV-infected people acquired an STD, and the gonorrhea incidence in this group was low compared with cohorts of HIV-infected people attending urban STD clinics.7,10 HIV-infected people represent a subset of the population that is at higher risk for STD acquisition, and within this group there is another subset of people who continue high-risk behaviors after HIV diagnosis. This subset should be characterized further because they are an important source of HIV transmission.

In this study, there were potential sources of bias that may have also contributed to the high STD rate among HIV-infected people. Ascertainment bias may have occurred if people with HIV infection were more likely to seek medical care for STD symptoms or more likely to be screened compared to the general population. This is particularly likely for women, who are more often screened for STDs. Although we could not assess STD symptom status in this study, the markedly elevated gonorrhea rates across age, gender, and geographic groupings suggest that ascertainment bias was not a major factor. Increased susceptibility to STD infection could also contribute to the high incidence among HIV-infected people, although we found that people with more severe immunodeficiency (i.e., AIDS) were not more likely to be diagnosed with an STD.

We were unable to compare gonorrhea incidence before and after HIV diagnosis, and it is possible that knowledge of HIV infection status led to changes in sexual behavior and decreased gonorrhea incidence. This hypothesis can be assessed in geographic areas where STD and HIV surveillance data can be linked over a longer time to measure gonorrhea rates before and after HIV diagnosis. An additional limitation of this study is that we were unable to document that all STDs were acquired after HIV diagnosis. We did not have access to medical records, and we do not know how many people were screened for STDs when initially diagnosed with HIV infection. However, the long interval between HIV diagnosis and STD diagnosis (median, 3 years) suggests that most of these STDs were acquired after HIV diagnosis.

In the multivariate analysis, HIV-infected people with incident STDs were more likely to be female and residents of Hennepin County, which includes the city of Minneapolis and surrounding suburbs. The higher risk in Hennepin County is consistent with STD surveillance data that show the highest incidence of reported gonorrhea and chlamydial infection in this county. The increased STD risk among HIV-infected women was based on a small sample, and there was a potential for ascertainment bias due to more frequent screening. This association should be examined further in a larger cohort study. Five of the nine women with a reported STD were black, a subpopulation that has a high incidence of gonorrhea.

The age-adjusted gonorrhea rates in HIV-infected men and women were similar, which seems counterintuitive since female gender was an independent risk factor for STD acquisition. The gonorrhea rate in men was affected by the number of recurrent episodes (n = 11) among four men, whereas all women had a single episode. Recurrent episodes did not affect the multivariate STD risk factor analysis because the outcome variable was dichotomous (any STD diagnosis vs. no STD diagnosis). When we recalculated the gonorrhea rates without the contribution of recurrent episodes, we found that the rate ratio was lower in men (5.5) than in women (9.5). This was consistent with the results of the STD risk factor analysis.

Prevention activities directed toward HIV-infected people are an important part of a comprehensive HIV prevention strategy. The occurrence of an STD is a sentinel marker for high-risk behavior, and linkage of STD and HIV surveillance data can be used to identify the subset of individuals who require more intensive counseling and partner notification efforts. Because the number of these individuals is small relative to all people with HIV infection, it may be feasible to provide these additional interventions despite limited resources. “Noncompliant carrier” interventions are controversial but may also play a role in limited and well-defined circumstances. Some states, including Minnesota, have passed legislation that allows state health officials to intervene when HIV-infected people repeatedly engage in behaviors that put others at risk. These interventions are labor intensive and legally complex, and few data exist on their effectiveness.11,12 If used, they must be part of a multifaceted approach that includes surveillance, widespread access to testing, partner notification, community-based education, mass media outreach, and HIV service programs.

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