Liver-related conditions, particularly viral hepatitis infection, have become a major source of morbidity and mortality among HIV-infected patients.1 Because of shared transmission routes, hepatitis C (HCV) coinfection is relatively common among people with HIV.1 Studies have found that the prevalence of HCV among both HIV-infected2 and non–HIV-infected3 men who have sex with men (MSM) is higher than the HCV prevalence in the general population in the United States. In New York City (NYC), despite an overall decrease in the number of people being diagnosed as having HCV, the proportion of this population who are HIV-infected MSM without a history of injection drug use (IDU) has more than tripled between 2000 and 2010,4 which may be a result of both an increase in new infections as well as new diagnoses of existing infections. Whether or not this is a recent phenomenon is a subject of debate, as the findings from a prospective cohort study conducted from 1984 to 2011 have suggested that HCV has been a common issue among HIV-infected MSM since the early days of the AIDS crisis.5 HIV/HCV coinfection is of particular concern because it accelerates HCV disease progression,1,6 increases rates of morbidity and mortality from HCV,6 and increases adverse effects from HIV medications.1,6
The most common HCV risk factor in the United States is IDU.7 In 2007, a study of 11 HIV-infected MSM in NYC was one of the first to suggest that HCV may be associated with high-risk sexual behavior in this population.8 Later, additional phylogenetic9,10 and behavioral studies from NYC11 and other locations10,12 added support to the possibility of sexual transmission of HCV among non-IDU HIV-infected MSM. Evidence has been equivocal for whether sexual transmitted diseases (STDs) are an independent risk factor for HCV infection in this population, with some studies failing to find such an association11,12 and others finding a significant association between STDs and risk of HCV.10,13
The basic mechanism of HCV transmission involves the disruption of a protective biological barrier (e.g., skin or mucous membranes) and exposure to HCV-infected fluid, usually blood.7 Multiple biological and behavioral risk factors put HIV-infected MSM at increased risk for sexual transmission of HCV. HIV-infected individuals, particularly those with unsuppressed HIV viral load, are more susceptible to HCV infection due to a weakened or delayed immune response to the virus.14 Secondary HCV transmission is more likely in those with HIV due to an increased HCV viral load6 and a higher probability of shedding the virus through semen.15 The use of noninjection drugs may play a role because of their association with risky sexual behavior.11,12 Also, high-risk sexual behaviors, such as unprotected anal sex, can cause mucosal trauma that facilitates HCV transmission.10–12
The Centers for Disease Control and Prevention guidelines16 indicate that HIV-infected MSM should be tested for HCV upon entry into HIV care and at least annually thereafter, with more frequent screening being recommended for individuals who are at increased risk. Identifying coinfected individuals and linking them to care is especially important and can reduce the burden of disease. Understanding the risk factors for HCV infection and describing the populations at greatest risk are critically important for designing effective interventions, educating clinicians, and providing testing and treatment guidelines to identify HIV/HCV coinfection and reduce morbidity, particularly now with more effective HCV treatments.17
In this article, we describe the diagnosis rate and demographic distribution of HCV among non-IDU MSM with diagnosed HIV in NYC between 2000 and 2010 using cross-matched surveillance data from the NYC Department of Health and Mental Hygiene (DOHMH), to better understand the epidemiology of HCV among HIV-infected MSM. We also examine the association between reported STDs and HCV infection to determine potential risk factors for HCV and to explore the possibility of sexual transmission of HCV.
In 2010, the NYC DOHMH implemented the Centers for Disease Control and Prevention's Program Collaboration and Service Integration initiative to increase data integration and describe interactions between infectious diseases in NYC.18 We conducted a deterministic cross-match of data from the HCV, HIV, hepatitis B virus, tuberculosis, and STD surveillance registries from 2000 to 2010, and vital statistics mortality data from 2000 to 2011. Individuals in each registry were matched against each of the others. The methods of the matching process have been described in detail elsewhere.19 Disease surveillance by the DOHMH is passive, with the reporting of certain diseases being required by NYC's Health Code Article 11. There is a dual-reporting requirement: all NYC providers diagnosing reportable diseases and all clinical laboratories licensed by New York State to test NYC residents are legally required to report cases to the NYC DOHMH. New York City disease surveillance data include reported persons who reside within the 5 boroughs of the city. Reports on persons diagnosed in NYC who reside in neighboring jurisdictions are referred to those health departments for inclusion in their surveillance data.
HIV-infected persons were defined as individuals diagnosed as having HIV and reported to the DOHMH. Information on HIV transmission risk factors was obtained during an HIV case investigation from patient medical records and interviews with patients. Risk categories, in order of decreasing probability of transmission per act, were IDU, MSM, heterosexual, and other/unknown. Persons with multiple transmission risk factors were assigned to the category with highest probability of transmission per act; that is, those with both IDU and MSM risk factors were classified as IDU and excluded from this analysis. Persons included in the analysis were diagnosed as having HIV before December 31, 2010 and not known to be dead as of January 1, 2000, with MSM as the HIV transmission risk factor.
Hepatitis C–infected persons were defined as individuals with a positive HCV antibody or RNA test result reported to the DOHMH. HIV/HCV coinfected persons were defined as HIV-diagnosed persons reported to DOHMH who matched to a report of HCV. Persons who had an HCV diagnosis before 2000 or who had an HCV diagnosis before or within 90 days after their HIV diagnosis were excluded from this analysis to maximize the probability of including only those HCV cases detected after HIV diagnosis, rather than before or during the initial HIV diagnostic workup. The population of HIV-infected MSM was divided into 2 groups: HIV/HCV coinfected MSM and HIV-infected MSM with no HCV diagnosis. Lacking specific data, we assumed no HIV-infected persons moved away from NYC between 2000 and 2010. To test this assumption we conducted a sensitivity analysis restricting the study population to persons with HIV diagnosis after January 1, 2000, thus providing some evidence that they lived in NYC during the study period.
Reports of gonorrhea, chlamydia, and syphilis (primary, secondary, and early latent) between January 1, 2000 and December 31, 2010, were identified through cross-registry matching. Individuals could have multiple STDs during the study period; for our analyses, we considered STD diagnoses among those with multiple reports in both mutually exclusive and nonmutually exclusive ways. To examine differences in STD history between HIV/HCV coinfected and HIV-monoinfected MSM, we counted individuals only in 1 STD category and used a mutually exclusive approach with STDs grouped hierarchically, such that persons with syphilis comprised the syphilis category regardless of whether they also had any gonorrhea and/or chlamydia diagnoses during the analytic period; persons in the gonorrhea category had been diagnosed as having gonorrhea and may or may not have had a chlamydia report, whereas the chlamydia category contained persons who had only chlamydia reported during the 11-year period.
Multivariable methods were used to identify the individual effect of each STD controlling for the other STDs, so we counted STD reports in a nonmutually exclusive manner. Additional demographic information included race/ethnicity, age, and incarceration history. Incarceration history was obtained from information collected as part of the HIV case investigation at the time of diagnosis and updated with new information when available. Person-years were calculated beginning with HIV diagnosis date or January 1, 2000, whichever was later, and ending with HCV diagnosis date, date of death, or December 31, 2010, whichever was earlier. Lacking specific data, we assumed no HIV-infected persons moved away from NYC between 2000 and 2010. To test this assumption we conducted a sensitivity analysis restricting the study population to persons with HIV diagnosis after January 1, 2000, thus providing some evidence that they lived in NYC during the study period.
Demographic characteristics and STD diagnoses of the coinfected and monoinfected groups were compared. Mann-Whitney U tests were used to assess differences in median age at HIV diagnosis. Pearson χ2 tests were used to test the association between HCV status and STD report as defined by the mutually exclusive hierarchical categories, incarceration history, and demographic characteristics. Hepatitis C diagnosis rates were calculated, adjusted using the direct method for age at HIV diagnosis and weighted by the 2000 US standard population.20 Multivariable Poisson regression models, with the number of HCV cases as the outcome of interest and the natural logarithm of the number of person-years contributed by non-IDU HIV-infected MSM, regardless of HCV status, as the offset, were used to calculate rate ratios (RRs) of HCV diagnoses by race/ethnicity and by history of nonmutually exclusive diagnoses of chlamydia, gonorrhea, and syphilis. Both crude RRs and RRs adjusted for birth year, incarceration history, age at HIV diagnosis, and, for the STD model, race/ethnicity, were estimated. We also investigated the STD-HCV association after restricting our analysis to include only STDs that were reported within 1 year before the HCV report date, to focus on risky sexual behavior that directly preceded HCV acquisition. All analyses were conducted using SAS software, version 9.2 (SAS Institute, Cary, NC).
There were 41,970 non-IDU MSM diagnosed as having HIV before 2010 alive as of 2000. Persons with an HCV diagnosis before 2000 (n = 256) and those with an HCV diagnosis before or within 90 days after their HIV diagnosis (n = 411) were excluded. The final analytic population consisted of 41,303 individuals who contributed a total of 315,392 person-years to the analysis. Just more than one-quarter (28.0%) of the population were Hispanic, 30.3% were non-Hispanic black, 39.1% were non-Hispanic white, 2.2% were Asian or Pacific Islander, and less than 1% (0.4%) were of other or unknown race. Nearly one-quarter (23.5%) had a syphilis, gonorrhea, or chlamydia diagnosis between 2000 and 2010, and 5.3% had a history of incarceration (Table 1). Among the analytic population, 2016 (4.9%) were diagnosed as having HCV for an age-adjusted diagnosis rate of 605 per 100,000 person-years.
The median age at HIV diagnosis was 34 years (interquartile range [IQR], 27–40 years) among those with no HCV diagnosis and 35 years (IQR, 29–43 years) among those with an HCV diagnosis (P < 0.01). The median age at HCV diagnosis was 44 years (IQR, 38–50 years; Table 1). A greater proportion of persons with an HCV diagnosis had a history of incarceration compared with those without an HCV diagnosis (11.5% vs. 4.9%, P < 0.01; Table 1).
Almost 90% of HIV-infected MSM with any STD diagnosis had at least 1 STD reported after their HIV diagnosis (95.0% of those with any STD and HCV and 85.1% of those with any STD but without HCV, P < 0.01). Among persons with any STD diagnosis, a greater proportion of HCV coinfected persons had multiple STD diagnoses compared with those without HCV (51.5% vs. 45.0%, P < 0.01). Compared with those with no HCV diagnosis, a smaller proportion with an HCV diagnosis were in the hierarchically defined chlamydia (2.0% vs. 2.9%, P = 0.01) and gonorrhea (5.8% vs. 7.8%, P < 0.01) categories, whereas a larger proportion were in the syphilis category (23.6% vs. 12.4%, P < 0.01; Table 1).
The age-adjusted diagnosis rate of HCV was highest among non-Hispanic blacks (765 diagnoses/100,000 person-years) and lowest among Asian and Pacific Islanders (215/100,000 person-years). After adjusting for birth year, age at HIV diagnosis, and incarceration history, the rates of HCV diagnoses were significantly greater among Hispanics (RRs, 1.4; 95% confidence interval [CI], 1.2–1.5) and non-Hispanic blacks (RR, 1.6; 95% CI, 1.4–1.8) than among non-Hispanic whites (Table 2).
Persons with a history of STD had an age-adjusted HCV diagnosis rate of 811/100,000 person-years, compared with 535/100,000 person-years for those with no history of STD (P < 0.01). In multivariable analysis, after adjusting for race/ethnicity, birth year, age at HIV diagnosis, and incarceration history, the HCV diagnosis rate for persons with any STD diagnosis (chlamydia, gonorrhea, or syphilis) was 2 times higher than among those with no STD diagnosis (P < 0.01). Syphilis (RR, 2.5; 95% CI, 2.3–2.8) and chlamydia (RR, 1.2; 95% CI, 1.0–1.4) each was associated with an increased rate of HCV diagnoses (Table 3).
For the first sensitivity analysis, we excluded persons diagnosed as having HIV before January 1, 2000. All previously mentioned associations remained similar. Non-Hispanic blacks and Hispanics had significantly higher adjusted diagnosis rates compared with non-Hispanic whites (RR, 1.4 and 1.3, respectively; P < 0.01 for both), and syphilis was associated with an adjusted diagnosis rate more than 2 times higher than the rate for people with no history of syphilis (P < 0.01). For the second sensitivity analysis, we only included STD reports occurring within 1 year before the HCV diagnosis among HIV/HCV coinfected MSM. Syphilis (adjusted RR, 1.9; 95% CI, 1.7–2.2) remained significantly associated with an increased rate of HCV diagnoses, and gonorrhea (RR, 0.8; 95% CI, 0.7–0.9) was significantly associated with a decreased rate of HCV diagnoses.
We found that 1 in 20 non-IDU HIV-infected MSM in NYC were diagnosed as having HCV between 2000 and 2011. We also identified a marked racial/ethnic disparity in HCV diagnosis rates and a strong association between HCV and syphilis among HIV-infected MSM. Our study is unique in that it uses a cross-matched population-level data set with surveillance data from multiple disease programs at a large, urban health department, allowing for the analysis of co-occurring infections.
The diagnosis rate of HCV among HIV-infected MSM in NYC between 2000 and 2010 was 605 diagnoses per 100,000 person-years, consistent with findings from a meta-analysis that estimated the incidence of HCV among HIV-infected non-IDU MSM to be 608 per 100,000 person-years.3 The prevalence of diagnosed HCV in this study population of HIV-infected MSM was 4.9%, nearly 5 times higher than the national prevalence of 1.0%21 and double the general NYC prevalence of 2.4%.22
The racial/ethnic disparity of HCV diagnosis rates among non-IDU HIV-infected MSM is striking. Non-Hispanic blacks and Hispanics had an adjusted rate of HCV diagnosis approximately 1.5 times greater than that of non-Hispanic whites; this is consistent with the disparity in HCV found among HIV-infected people in NYC overall.23 Also, more than 1 in 10 HIV/HCV-coinfected MSM had a history of incarceration. This is likely an underestimation due to limitations in ascertainment of incarceration history. The knowledge of this racial/ethnic disparity and the relationship between incarceration and HCV coinfection can guide the development of interventions and educational campaigns.
The finding that approximately one-quarter of our study population had 1 or more STD diagnoses, and that for the vast majority, at least 1 STD occurred after HIV diagnosis, supports previous findings that MSM continue to practice unprotected sex after HIV diagnosis.24 The practice of serosorting, or choosing HIV-concordant sexual partners, may result in higher rates of unprotected anal sex and other high-risk sexual behavior. A 2008 study from San Francisco revealed that more than 50% of HIV-infected MSM practiced serosorting,25 and an association between serosorting and higher incidence of STDs has also been identified.26 If HCV is sexually transmitted with at least modest frequency, one would expect that individuals who are at risk for acquiring other sexually transmitted diseases would also be prone to acquiring HCV sexually. Our data are consistent with this transmission mechanism. We found a significant association between certain STDs and HCV infections, suggesting a shared mode of transmission. Even after restricting STD diagnoses to those occurring within 1 year before HCV report, the association between syphilis and HCV report rate remained strong, although there was an opposite relationship between gonorrhea and HCV report rate. This may mean that only those at heightened risk for syphilis are at increased risk for HCV.
Low levels of knowledge about HCV among HIV-infected MSM may be contributing to the spread of HCV, as awareness of HCV risk and modes of transmission remains low among MSM.27,28 Furthermore, there is evidence that HCV infection carries stigma within the HIV-infected MSM community, which may lead to partners not disclosing their HCV status before engaging in high-risk sexual activity.29 To our knowledge, serosorting based on HCV status is not commonly practiced.
There are several limitations to this study. First, surveillance data contain only the date of the first positive test result for each of the infections in our analysis; we do not have negative HCV test results or the actual date of infection, making it impossible to determine the true relative timing of infections. It is likely that many of the HCV infections were acquired years in the past but are being discovered because of HIV providers’ increased awareness of the possibility of sexual transmission of HCV among their patients. The lack of negative test results prevents us from exploring the possibility of case ascertainment bias; a syphilis diagnosis could be a trigger for providers to screen for HCV, and likewise, providers who adhere to STD screening guidelines may be more likely to adhere to those for HCV. Second, risk factors captured in these data are those for HIV transmission and not HCV transmission; therefore, risk factors such as blood transfusion before 1992 are not known. In addition, risk factors are self-reported and are collected at the time of HIV diagnosis, meaning that data on risk factors in the period after HIV diagnosis and before HCV diagnosis, which may include IDU initiated after HIV diagnosis, are not captured. A final limitation is that surveillance data do not include any infection that is undiagnosed and unreported. Underascertainment of disease could have impacted our results, particularly in the case of gonorrhea; unlike results regarding syphilis, we found no association between HCV and gonoccocal infection. Rectal infection with gonorrhea is not uncommon among MSM and might be important with regard to HCV transmission; however, a general failure to screen for rectal STD results in these infections often being undiagnosed and underreported.30
Recent reports have found that adherence to guidelines recommending baseline HCV screening among HIV-infected MSM remains poor,31,32 despite the fact that routine HCV screening programs for the HIV-infected MSM population have been shown to be a cost-effective intervention.33 Multiple studies have shown that late diagnosis of HCV is a major risk factor for HCV-related morbidity and mortality because symptoms tend to only appear once significant liver damage has occurred,34 particularly among HIV-infected individuals, due to the rapid progression from initial HCV infection to severe morbidities and mortalities.35 Therefore, early detection of HCV is essential for optimal health outcomes.
Because of the increased risk of HCV infection among HIV-infected MSM with syphilis, a diagnosis of syphilis should prompt a test for HCV among HIV-infected MSM, regardless of whether there are known HCV risk factors or prior negative HCV test results. Based on the prevalence and diagnosis rate of HCV among HIV-infected MSM in NYC, the racial/ethnic disparity of HCV in this population, and the available literature, we also recommend that clinical practices implement quality assurance activities for regular HCV screening. These activities may include monitoring adherence to recommended HCV screening guidelines, developing electronic health record alerts to prompt HCV screening, and education for providers about risk factors and potential transmission mechanisms of HCV among HIV-infected MSM.
Greater emphasis should be placed on HCV prevention counseling and patient education for HIV-infected MSM, including the need to practice safe sex even among persons with undetectable HIV viral loads or those who practice HIV serosorting. Direct outreach to HIV-infected MSM to provide HCV education and prevention messaging using mobile applications designed for men to meet sex partners, which has been shown to be acceptable to users for HIV prevention,36 should also be considered. Addressing HCV among HIV-infected MSM is crucial for supporting the health of this population, increasing primary prevention, ensuring early identification of HCV infection, prompting linkage to care, and curing HCV.
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