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JAIDS Journal of Acquired Immune Deficiency Syndromes:
Letters to the Editor

Beliefs About HIV Reinfection (Superinfection) and Sexual Behavior Among a Diverse Sample of HIV-Positive Men Who Have Sex With Men

Colfax, Grant Nash MD*; Guzman, Robert MPH*; Wheeler, Sarah MPH*; Mansergh, Gordon PhD†; Marks, Gary PhD†; Rader, Melissa MPH†; Buchbinder, Susan P. MD*

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*HIV Research Section, Department of Public Health, San Francisco, California

†Division of HIV/AIDS Prevention, US Centers for Disease Control and Prevention, Atlanta, Georgia

The content of this publication does not necessarily reflect the views or policies of the Department of Health and Human Services; nor does mention of trade names, commercial products, or organizations imply endorsement by the US government.

To the Editor:

Reinfection with a second strain of HIV after primary infection—also known as superinfection—has been confirmed in several case reports. 1–3 Reinfection could have serious health implications, due to reinfection with drug-resistant strains of virus, leading to viral escape and higher viral loads. Several studies are currently underway to characterize the clinical implications of reinfection. Until they are completed, it has been suggested that HIV-positive persons protect themselves from possible reinfection. 4

Despite these recommendations, no data have been published on the beliefs of men who have sex with men (MSMs) about reinfection, or whether beliefs about reinfection are associated with sexual behavior with HIV-positive partners. Such information is important for understanding how HIV-positive persons may react to information about reinfection, and for developing public health messages regarding the potential risks of reinfection.

We examined HIV-positive MSM attitudes regarding reinfection and whether concerns about reinfection’s potential effects on health were associated with decreased unprotected anal (UA) sex with HIV-positive and unknown status partners.

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METHODS

Study recruitment and sampling methods have been previously described in detail. 5 Briefly, from July 2000 to February 2001, men were recruited at bars, dance clubs, community service agencies, and at street locations in the San Francisco Bay Area, and through snowball sampling. Because they have traditionally been underrepresented in HIV prevention research and are at high risk for HIV infection, African American and Latino MSMs were targeted for enrollment. 6

Eligible men were at least 18 years old and either identified as gay/bisexual or reported having anal or oral sex with a man in the prior year. A total of 2278 men were approached, of whom 62% were screened. Of the 1413 men screened, 1061 (75%) were eligible; 842 (79%) agreed to do the survey; of these, 554 (66%) completed the survey. Participants provided informed consent, completed a 1-hour interviewer-administered questionnaire, and were reimbursed $25. Sexual history, HIV serostatus, viral load (VL), CD4 count, and retroviral therapy were determined by self-report. Study procedures and instruments were approved by the Centers for Disease Control and Prevention and local site institutional review boards.

Bivariate comparisons used χ2 tests to assess differences (P <0.05) between groups. Backwards, stepwise logistic regression analysis determined independent correlates of UA with other HIV-positive and unknown status partners; these analyses were limited to participants who had heard of reinfection. Response variables to reinfection questions were dichotomized to agree (agree or strongly agree) and do not agree (neutral, disagree, or strongly disagree). Sociodemographic variables for racial/ethnic group, income, education, and age were forced into models with additional potential variables of P value associations of <0.15 included.

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RESULTS

Of the total sample of 554, 196 (35%) were HIV positive and were included in this analysis. Of these participants, 33% were Latino, 29% were African American, 26% were white, and 11% were of other race/ethnicity. Median age was 38 years (range, 20–65 years). Annual income ranged from <$10,000 (48% of sample) to $10,000–$19,999 (25%) to ≥$20,000 (27%). Median time since first HIV-positive test was 7.2 years. Median self-reported CD4 count was 425 cell/uL; median viral load was 70 copies/mL; 64% of participants reported currently taking antiretroviral therapy. Fifty-seven participants (29%) reported UA with another positive partner (sero-concordant unprotected anal sex, SCUA). Thirty-three participants (17%) reported UA with an unknown partner (sero-unknown unprotected anal sex, SUUA).

Most participants had heard of reinfection (165/193, 85%). Compared with those who had not heard of reinfection, those who had heard of reinfection were more likely to have attended college (odds ratio [OR] 5.3, 95% CI 1.7–16.5, P = 0.003) and had known of their HIV-positive status longer (OR 1.2 per year known positive, 95% CI 1.0–1.3, P = 0.01). Of those who had heard of reinfection, nearly two-thirds strongly agreed that reinfection occurs (Table 1); a similar proportion agreed or strongly agreed that they were concerned about reinfection. Over three-quarters agreed or strongly agreed that reinfection was damaging to health, and over half of participants strongly agreed that they were safer sexually because of concerns about reinfection.

Table 1
Table 1
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Compared with those who did not believe reinfection was damaging to health, participants who agreed or strongly agreed with this belief were less likely to report SCUA (50 vs. 25%, P = 0.007). In a multivariate model including age, race/ethnicity, income, and education, as well as testing for potential associations of CD4 count, use of antiretroviral therapy, and VL with SCUA, the only significant factors associated with SCUA were an inverse relationship with believing that reinfection has a damaging effect on health (OR 0.34, 95% CI 0.13–0.89, P = 0.03) and a positive association with younger age (OR 5.5, 95% CI 1.2–24.2, P = 0.02 for those aged <30 years compared with ≥30 years).

We found similar associations between believing reinfection has a damaging effect on health and reporting SUUA. Compared with those who did not believe reinfection was damaging to health, participants who agreed or strongly agreed with this belief were less likely to report SUUA (30 vs.15%, P = 0.05). In the multivariate analysis including the above sociodemographic variables, as well as examining for potential associations of CD4 count, use of antiretroviral therapy, and VL with SUUA, participants who agreed or strongly agreed that reinfection has a damaging effect on health were less likely to report SUUA (OR 0.34, 95% CI 0.13–0.94, P = 0.04).

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DISCUSSION

Our results suggest that despite the lack of widespread clinical evidence that reinfection leads to adverse clinical outcomes, many MSMs are making their own risk reduction decisions about the potential consequences of reinfection, with many choosing to reduce unprotected behavior with known HIV-positive partners, as well as partners who could be HIV positive. These data have potential implications for counseling HIV-positive MSMs about their sexual behavior. If reinfection is shown to be more than a rare event and to influence health outcomes adversely, safer sex messages should continue to reinforce concerns among MSMs about reinfection and advise HIV-positive persons to use condoms with their HIV-positive partners to lower secondary transmission risk; with the high rates of UA overall in this sample, such messages would be needed. Our finding that younger HIV-positive MSMs were more likely to engage in SCUA compared with older men suggests that such messages may need to be tailored for young men. In addition, if many HIV-positive MSMs are reducing their unprotected sexual behavior due to concerns about their own health, positive reinforcement of practicing safer sex behaviors with HIV-negative partners may be predicated on practicing similar behavior with HIV-positive partners or unknown partners, potentially decreasing primary HIV transmission.

Conversely, if the clinical significance of reinfection is found to be minimal, unprotected sex among HIV-positive MSMs becomes of less concern from an HIV transmission perspective. HIV prevention messages would therefore need to reinforce the need to continue to protect unknown and HIV-negative partners: otherwise, decreased concern about protecting themselves from reinfection could lead HIV-positive persons to take more risks with all their partners. Health providers would also need to continue to counsel HIV-positive persons about the risk of transmission of other sexually transmitted infections.

This study has limitations. It was a cross-sectional study of MSMs, who may not be representative all MSM populations; our participants were more diverse and had lower income and educational levels than population-based samples of MSMs. 7 Participants may have underreported behaviors in the interviewer-administered questionnaire. We were not able to collect data on all possible confounding variables that may influence sexual behavior. Finally, data were collected prior to scientific confirmation of reinfection; it is possible that concern about reinfection increased following these reports.

As more data about reinfection and its clinical implications are published, careful consideration should be given to the effects such information may have on the sexual behavior of HIV-positive individuals.

Grant Nash Colfax, MD*

Robert Guzman, MPH*

Sarah Wheeler, MPH*

Gordon Mansergh, PhD†

Gary Marks, PhD†

Melissa Rader, MPH†

Susan P. Buchbinder, MD*

*HIV Research Section, Department of Public Health, San Francisco, California

†Division of HIV/AIDS Prevention, US Centers for Disease Control and Prevention, Atlanta, Georgia

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REFERENCES

1. Jost S, Bernard M-C, Kaiser L, et al. A patient with HIV-1 superinfection. N Engl J Med. 2002;347:731–736.

2. Ramos A, Hu DJ, Nguyen L, et al. Intersubtype human immunodeficiency virus type 1 super-infection following seroconversion to primary infection in two injection drug users. J Virol. 2002;76:7444–7452.

3. Altfeld M, Allen TM, Yu XG, et al. HIV-1 superinfection despite broad CD8+ T-cell responses containing replication of the primary virus. Nature. 2002;420:434–439.

4. Goulder PJ, Walker BD. HIV-1 superinfection: a word of caution. N Engl J Med. 2002;347:756–758.

5. Mansergh G, Marks G, Colfax GN, et al. “Barebacking” in a diverse sample of men who have sex with men. AIDS. 2002;16:653–659.

6. Valleroy LA, MacKellar DA, Karon JM, et al. HIV prevalence and associated risks in young men who have sex with men. Young Men’s Survey Study Group. JAMA. 2000;284:198–204.

7. Catania JA, Osmond D, Stall RD, et al. The continuing HIV epidemic among men who have sex with men. Am J Public Health. 2001; 91:907–914.

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© 2004 Lippincott Williams & Wilkins, Inc.

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