Abstract
Limited health care access and missed opportunities for HIV and other sexually transmitted infection (STI) education and testing in health care settings may contribute to risk of HIV infection. In 2008, we conducted a case-control study of African American men who have sex with men (MSM) in a southeastern city (Jackson, Mississippi) with an increase in numbers of newly reported HIV cases. Our aims were to evaluate associations between health care and HIV infection and to identify missed opportunities for HIV/STI testing. We queried 40 potential HIV-infected cases and 936 potential HIV-uninfected controls for participation in this study. Study enrollees included HIV-infected cases (n=30) and HIV-uninfected controls (n=95) who consented to participate and responded to a self-administered computerized survey about sexual risk behaviors and health care utilization. We used bivariate analysis and logistic regression to test for associations between potential risk factors and HIV infection. Cases were more likely than controls to lack health insurance (odds ratio [OR]=2.5; 95% confidence interval [CI]=1.1–5.7), lack a primary care provider (OR=6.3; CI=2.3–16.8), and to not have received advice about HIV or STI testing or prevention (OR=5.4; CI=1.3–21.5) or disclose their sexual identity (OR=7.0; CI=1.6–29.2) to a health care provider. In multivariate analysis, lacking a primary health care provider (adjusted odds ratio [AOR]=4.5; CI=1.4–14.7) and not disclosing sexual identity to a health care provider (AOR=8.6; CI=1.8–40.0) were independent risk factors for HIV infection among African American MSM. HIV prevention interventions for African American MSM should address access to primary health care providers for HIV/STI prevention and testing services and the need for increased discussions about sexual health, sexual identity, and sexual behaviors between providers and patients in an effort to reduce HIV incidence and HIV-related health disparities.
Introduction
Y
Sexual transmission of HIV accounts for the majority of HIV transmission, and HIV-infected persons who are unaware of their infection may account for more than half of the sexually transmitted HIV infections in the United States. 7 Health care visits are important opportunities for HIV testing. The Centers for Disease Control and Prevention (CDC) recommends that health care facilities perform routine HIV testing for all patients aged 13–64 years and that testing be repeated annually for persons at high risk of acquiring HIV. 8 However, limited health care access may be a barrier to routine HIV counseling and testing, and among those with access to health care, opportunities to offer testing may be missed by providers. 9 –11 Earlier detection of HIV disease can lead to decreased morbidity and mortality through earlier initiation of treatment and decreased ongoing sexual transmission of HIV infection. 9,12,13
During 2005–2007, 35% of non-Hispanic African American men were uninsured compared to 25% of non-Hispanic white men. 14 Uninsured adults aged 19–24 years are significantly more likely than their privately insured peers to report barriers to obtaining health care. 15,16 Because the receipt of preventive services has been associated with having insurance and having a usual source of care, 17 –19 lacking these can lead to decreased access to care and services as well as decreased HIV testing opportunities and delayed HIV diagnoses. 10 Even for insured patients, HIV and sexually transmitted disease (STD) counseling and testing services in primary care settings can be limited by barriers such as the discomfort of health care providers and patients in discussing sexual health, the lack of recognition that sexual health should be a part of a routine medical examination, and the decreased ability of physicians to make appropriate preventive health recommendations for MSM patients based on physician lack of awareness of sexual identity and/or sexual behaviors. 20 –23 These health care factors contribute to the racial disparities that are seen in rates of HIV infections, as well as HIV-related morbidity and mortality.
From 2004–2005 to 2006–2007, in a three-county area of Jackson, Mississippi, the number of newly diagnosed cases of HIV infection among young African American MSM aged 17–25 years increased 45%. 24 While HIV surveillance data in Mississippi show African Americans to be disproportionately affected by HIV (38% of Mississippi's population and 76% of newly diagnosed HIV cases), this sharp increase among young African American MSM warranted heightened efforts to understand the context of the epidemic and improve HIV prevention activities with young African American MSM. 25 As part of these heightened HIV prevention efforts, we conducted an investigation that included a case-control study of health care visit factors associated with HIV infection in this population. Our objectives were to: (1) evaluate the association between health care access, receipt of advice about HIV/sexually transmitted infection (STI) prevention or testing, and HIV infection and (2) to identify missed opportunities in health care settings to deliver HIV and/or STI prevention and testing to young African American MSM in this southeastern metropolitan area of Jackson, Mississippi in an effort to identify HIV cases earlier and reduce ongoing sexual transmission of HIV.
Methods
Participant recruitment
During February–April 2008, we conducted an unmatched case-control study as part of an investigation of an increase in HIV diagnoses for young African American MSM in a three-county area of Jackson, Mississippi (Hinds, Madison, and Rankin Counties). Cases were identified through the HIV/AIDS Reporting System (HARS) and were defined as African American males who had received a diagnosis of HIV infection between January 2006 and April 2008. Those who were recruited for participation were aged 16–25 years at the time of diagnosis and lived in, or received their diagnosis in, the three-county area. An eligibility screener was used to identify cases with a history of anal sex with a man during the year before diagnosis. We only report on “self-reported” MSM cases and “self-reported” MSM controls. Selected controls were African American males residing in the three-county area, which reported having received a negative HIV test result in the 6 months before interview and having had anal sex with a man during the year before interview. Controls were recruited from multiple Jackson venues, including college campuses, bars and clubs, shopping malls, and an STD clinic. Controls were screened for eligibility by self-administered computer-assisted questionnaire.
For recruitment in the STD clinic, we reviewed the medical charts of all incoming patients to determine age, gender, and history of HIV infection. African American males aged 16–25 years who were not known to be HIV-infected were approached in the clinic, informed that a health survey was being conducted, and invited to complete the self-administered screening questionnaire. At other venues, interviewers approached males who appeared to be African Americans aged 16–25 years, informed them about the survey, and invited them to complete the screening questionnaire. All participants who met eligibility criteria and provided written consent completed the computer-assisted survey, for which they received a small nonmonetary incentive. Participation in this survey was voluntary, and cases and controls who were eligible, provided informed consent and completed the survey received a $25 gift card. Strict security and confidentiality measures consistent with those used for HIV surveillance data were used in maintaining all survey data files.
Data collection and analysis
We collected demographic, socioeconomic, behavioral, and health care-related data for the recall period, which was defined as the 12-month period either before HIV diagnosis (cases) or the date of interview (controls). Questions were obtained from a number of sources, including the National HIV Behavioral Surveillance System instrument and survey instruments from prior outbreak investigations. Questions regarding a health care provider's advice on HIV or STD prevention or testing were asked only of participants who reported seeing a health care provider during the recall period.
Bivariate analysis for reporting sexual identity to a health care provider was limited to those who reported seeing a health care provider. Participants who responded to the question, “How did you usually identify yourself (sexual identity) to your health care providers,” with “I do not discuss this with them” were considered as having not disclosed their sexual identity to providers. All other responses were considered as having disclosed their sexual identity to providers.
Bivariate analyses were performed with categorical variables by using the χ2 and Fisher's exact tests. Continuous variables (respondents' age) were compared among cases and controls by using the Wilcoxon-Mann-Whitney test. We performed forward stepwise logistic regression to build a multivariate model. Variables eligible for selection included those significant at the p≤0.05 level in the bivariate analysis and those that have been associated with HIV infection in published literature. Adjusted odds ratios at the p≤0.05 level were considered statistically significant. Data were collected during 2008 and analyzed during 2009 by using SAS, version 9.2 (SAS Institute, Cary, NC).
Results
From January 2006 through April 2008, 86 new HIV infections were reported among African American men aged 16–25 years who received their diagnosis in or resided in the three-county Jackson area. Of the 86 potential cases identified, 40 (47%) were interviewed. Of the 46 (53%) not interviewed, 31 could not be located, 1 was deceased, 3 had moved out of the area, 1 declined to participate, 1 did not attend the scheduled interview, and 9 had no recorded reason. There were no statistically significant differences between potential cases who were interviewed and potential cases who were not interviewed in terms of age at diagnosis, HARS reported transmission category, year of diagnosis, or residence or diagnosis in the tricounty area (data not shown). Of the 40 potential cases that were interviewed, 30 (75%) met analysis eligibility criteria as cases. Of the 10 who were excluded, 9 did not report sex with a man during the recall period and 1 was transgender.
For controls, 95 (10%) of the 936 persons who were screened as potential controls met eligibility criteria and were enrolled. Of the 841 screened controls who did not meet eligibility criteria, 88% did not report anal sex with a man, 70% did not report a negative HIV test result in the past 6 months, 17% did not live in the three-county Jackson area, 17% were not aged 16–25 years, 7% had previously taken the screener questionnaire, 2% were not African American, and 1% was not male. Controls were recruited from bars and clubs (35%), an STD clinic (24%), college campuses (24%), shopping malls (13%), a college testing facility (2%), and a community social event (2%).
Sociodemographic characteristics and sexual behaviors
Compared with controls, cases were less likely to be college students (odds ratio [OR]=0.3, confidence interval [CI]=0.1–0.7) and were older (p=0.01). Cases had 4.2 (CI=1.5–11.1) times the odds of controls of reporting unprotected anal intercourse (UAI) with a man and 6.3 (CI=2.1–20) times the odds of reporting male partners aged 26 years or older. Cases and controls did not differ significantly with respect to monthly income, employment status, or sexual identity (Table 1). There were no statistically significant differences in their reported history of STDs, concurrent sexual partnerships, exchange of sex for money or drugs, drug or alcohol use, or history of incarceration (data not shown).
χ2 and Fisher's exact tests used for bivariate analysis of categorical variables (all variables exept respondent's age). Wilcoxon-Mann-Whitney test used for respondent's age.
At time of first positive HIV test (cases) or interview (controls).
During the 12 months before positive HIV test (cases) or the past 12 months (controls).
Health care access, utilization, and HIV/STI prevention and testing
Although cases were more likely than controls to report not having health insurance (OR=2.5; CI=1.1–5.8) and to report not having a primary health care provider (PCP; OR=6.4; CI=2.4–17.1), similar proportions of both groups reported a health care visit within the recall period (OR=1.6; CI=0.7–4.0). There were no significant differences between the types of health insurance reported by cases and controls (Table 2).
Limited to those who reported having health insurance (12 cases and 59 controls).
Undefined odds ratio and confidence interval due to cells containing zero.
Limited to those who reported seeing a provider in the past year (19 cases and 71 controls); missing responses included in percentage calculation but not listed in this table; pairwise comparison for “yes” and “no” responses only with “no” response as reference group.
The number of HIV tests refers to 2 years before first positive HIV test (cases) or past 2 years (controls).
The recall period for HIV testing was 2 years before diagnosis (cases) or 2 years before interview (controls). Cases were tested for and received their diagnoses of HIV infection at multiple locations: sexually transmitted disease clinic (57%), hospital (10%), jail or prison (10%), blood donation center (10%), general clinic (7%), other non-medical setting (7%). Locations of HIV testing for controls were not collected.
Because a negative HIV test result within 6 months before interview was an eligibility requirement for controls, none of the controls reported not having an HIV test during the recall period. However, 23% of cases reported not having a prior HIV test during the 2-year recall period before the positive test result received when diagnosed with HIV. Less than 20% of cases and controls reported getting their most recent HIV test as part of a routine physical examination. There were no significant differences between where cases and controls would go for HIV testing during the recall period; however, the most frequently mentioned locations were public health (67% for both cases and controls) and STI clinics (40% cases vs. 27% controls), student health centers (17% cases versus 14% controls), and doctor's offices (10% cases vs. 27% controls). Eight percent of study respondents reported the local emergency department as a location they would visit for HIV testing (data not shown).
Of those who reported a health care visit during the recall period, cases were more likely than controls to report not receiving advice from a health care provider on HIV or STI prevention or testing during that time. Of cases and controls that reported seeing a health care provider, cases had 7 times the odds of not disclosing their sexual identity to their health care providers. Because one's sexual identity may not describe one's sexual behavior, we asked participants a separate question about reasons for not discussing their sexual behaviors with their providers. There were no statistically significant differences between cases and controls regarding the reasons for not discussing their male–male sexual behavior with their health care providers, and the most common reasons given were that their health care providers did not ask about it (37% cases versus 33% controls), they did not feel comfortable discussing this topic with health care providers (32% cases versus 23% controls), or they believed that it had nothing to do with the reason they sought care (26% cases versus 15% controls).
We performed stepwise logistic regression including, as candidates, variables significant at the p≤0.05 level and controlled for participant age, history of UAI, and history of older male partners. Although there was no significant difference between the number of cases and controls who reported a health care provider visit during the recall period, we included this variable in the pool of eligible variables because those who reported seeing health care providers would have had the opportunity to receive HIV/STI prevention counseling and testing from health care providers. We tested and found no collinearity between having a primary care provider, health insurance, and reporting a health care visit during the recall period. On multivariate analysis, cases were more likely than controls to report not having a PCP (OR=4.5; CI=1.43–14.7) and more likely than controls to report not disclosing a sexual identity to their health care providers (OR=8.6; CI=1.8–40.0). Cases were more likely to report engaging in UAI (OR=4.6; CI=1.3–16.2) and having male partners 26 years of age or older (OR=6.7; CI=2.0–22.1; Table 3).
Logistic regression performed controlled for age, history of unprotected anal intercourse, and history of older male partners during the recall period.
Discussion
We found that lacking a PCP, not disclosing one's sexual identity to a health care provider, having UAI, and having older male sexual partners were independent predictors of HIV infection among young African American MSM in this unmatched case-control study in a three-county area of Jackson, Mississippi. Our findings also suggest that, for young African American MSM who were able to access health care, those who did not report HIV/STI prevention and testing discussions with their health care providers had higher odds of HIV infection.
Cases were as likely as controls to report health care visits during the recall period, but they were less likely to have a PCP (OR=6.4; CI–2.4–17.1). Receiving a recommendation to have an HIV test from one's PCP has been found to be a strong predictor for HIV testing among African American men. 26 Our study did not collect information on the type of health care visits that the respondents reported having, which could have included primary care visits, as well as emergency or urgent care visits, and hospitalizations. Some qualitative analyses have found that some young African American men access health care more so for urgent health concerns and less so for routine preventive care. 27,28 A qualitative analysis of African American and Latino males ages 15–23 years found that health care providers could play an important role in the young men's decisions to test for HIV. 29 Also, patients often prefer to receive sexual health information from clinicians who are knowledgeable of and comfortable with discussing sexual health care, which may be hindered by inadequate provider training in HIV/STI counseling and testing techniques. 30 Training health care providers to more routinely engage in discussions with their patients about HIV/STI counseling and regular HIV testing is warranted and should be improved. 30 –32
Our study found that cases were more likely than controls not to disclose their sexual identity and/or behaviors to a health care provider. Patient–provider discussions of sexual identity and/or male–male sexual behavior have been associated with being offered an HIV test among MSM. 33,34 Yet, more than one-third of cases in our study reported that they had not received advice regarding HIV/STI testing or prevention from a health care provider during the year before they were diagnosed with HIV, which represent missed opportunities for HIV/STI prevention and testing. Previous studies have shown that provider and patient discomfort with discussing sexual identity and providers' misperceptions about risk are important barriers to HIV prevention and earlier detection of HIV infections in health care settings; discussions that focus on sexual behaviors more than identity may be warranted. 23,35 –39 In addition, for young African American MSM, personal HIV stigma and shame, perceived health care provider HIV stigma, and sexual minority stigma may all present barriers to full engagement in health care and disclosure discussions during health care visits. 40,41 While we did not collect survey data regarding the social and cultural context of living as a young, African American MSM in Jackson, Mississippi, several reports have described the additional challenges of poverty, lack of access to employment, racism, homophobia, and provider-patient discordance in the Southeastern United States, which may all have implications for barriers to sexual health/sexual behavior discussions and HIV treatment and care. 42 –44 Additional qualitative studies to explore these factors are warranted.
Although the role of a PCP in HIV testing among young African American men can be significant, ways to increase access to prevention and testing must be ensured for persons who do not have insurance, or who have other barriers to accessing primary health care. The Affordable Health Care Act, 45 by making health care more accessible for uninsured and underinsured persons, and the CDC's revised recommendations for HIV testing in health care settings, 8 will likely lead to an increase in health care access and in HIV testing opportunities for all Americans, including many young African American men, by providing free or low-cost services. In addition, HIV testing in clinical, nonclinical and outreach venues should all be considered to reach young African American MSM who may not have access to private health care settings. 26,47 –49 When primary care access is available, promoting the importance of preventive care over urgent health care seeking is also needed for all men, but particularly young African American men. 49
UAI and having male partners aged 26 years of age or older were predictors for HIV infection in our study sample. 50 These factors are known risks for HIV infection, 50 –52 and they are topics that warrant risk-reduction discussions at each health care visit by PCPs and their male patients. Strengthening the health care message regarding the importance of consistent and correct condom use is also warranted with sexually active persons at risk for HIV infection, including MSM. 39 With adequate training, HIV/STI counseling interventions led by PCPs have resulted in improved provider ability to conduct HIV/STI counseling with their patients and they have also improved patient recall of the HIV prevention discussions that they have had with their providers. 31,32
Another missed opportunity for HIV testing and prevention among young African American MSM in health care settings is the failure of both health care providers and patients to recognize sexual health as an important component of comprehensive medical care. 35 –37 In our study, less than 20% of both cases and controls reported getting their last HIV test as part of a routine medical examination. Continued efforts to normalize discussions about sexual health between patients and providers and to remove barriers, such as lack of insurance coverage of routine HIV screening, could increase routine, voluntary HIV screening of all patients aged 13–64 years in health care settings.
In our sample, HIV-infected cases were less likely to be enrolled as college students and were more likely to be older when compared with HIV-infected controls. These findings may have been affected by our recruitment strategies for our controls. Although our sample size was small, these statistically significant findings helped to support local efforts in Jackson to expand HIV education and prevention activities beyond local college campuses to include the surrounding communities and older age groups of young African American men.
This study has several limitations. Recall bias may have decreased the accuracy of responses since cases and controls were asked to recall the twelve months prior to diagnosis and the past twelve months, respectively. Selection bias may be a factor since only half of potential cases were evaluated for inclusion in the study. Selection bias may also have occurred because of unsystematic control recruitment and the collection of information on activities that are stigmatized, such as male–male sexual behavior. Recruiting controls at bars and clubs likely limited the representation of potential participants who do not frequent those places. Misclassification is possible since we did not confirm self-reports of negative HIV tests in controls, whereas cases had documented positive tests. If such misclassification occurred it would tend to minimize differences between cases and controls.
Conclusion
The domestic HIV epidemic continues to disproportionately affect young, African American MSM and as such, strategies that focus increased HIV prevention efforts with this group are warranted. The National HIV/AIDS Strategy (NHAS) in the United States has as its goals to: (1) reduce HIV incidence; (2) increase access to HIV care and optimize health outcomes for those living with HIV infection; and (3) reduce HIV-related health disparities. 53 The lessons learned in Jackson, Mississippi, a city with racial/ethnic HIV-related health disparities and an HIV epidemic that disproportionately affects young African American MSM, may help support HIV prevention strategies in similar southeastern settings in the United States. Strategies for HIV prevention among young African American MSM should include addressing barriers to health care access, utilization, missed opportunities for HIV prevention, education, and regular HIV testing with enhanced linkage to care when needed, in an effort to meet NHAS goals. HIV prevention programs should raise the awareness of those with limited health care access to the availability of HIV testing in a variety of traditional and nontraditional HIV testing settings, including nonclinical and outreach settings with free and low-cost options. Training providers and patients to be more aware the importance of patient–provider dialogue about sexual health may also encourage HIV/STI screening, earlier diagnosis and treatment, and the reduction of ongoing sexual transmission of HIV. By maximizing opportunities with young African American MSM when they do present for care, we can help ensure that these young men are equipped with tools that can improve their sexual health, decrease their risk of HIV acquisition and/or transmission, improve our overall HIV/STI prevention efforts, and increase our ability to reach NHAS goals.
Footnotes
Acknowledgments
We wish to thank Kendra Johnson, Craig Thompson, Haitham Baghdady, Michael Robinson, Anthony Fox, Deborah Dowell, Anne McIntyre, Lisa Rynn, Teri Larkins, and Jillian Doss for their assistance with recruiting and interviewing participants for this investigation. We would also like to thank Lisa Hightow for her assistance in preparation of the questionnaire and Greg Millett for input regarding study design and interpretation.
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.
Author Disclosure Statement
No competing financial interests exist.
