Behavioral Changes Associated With Testing HIV-Positive Among Sexually Transmitted Infection Clinic Patients In Cape Town, South Africa

Abstract

Objectives. We sought to examine behavioral risks and behavior changes associated with testing HIV-positive among sexually transmitted infection (STI) patients, in order to inform HIV- and STI-prevention interventions.

Methods. We performed a cohort study of 29 STI patients who seroconverted from HIV-negative to HIV-positive during 1 year of observation and 77 STI patients who persistently tested HIV-negative. Computerized behavioral interviews were collected at baseline and at 1 year, and STI clinic charts were abstracted over the same 1-year period.

Results. The STI patients who reported genital bleeding during sexual activity at baseline were significantly more likely to test HIV-positive. Reductions in number of sexual partners and rates of unprotected intercourse occurred for all STI clinic patients regardless of whether they tested HIV-positive.

Conclusions. Although risk reductions occurred, 5% of HIV-negative STI clinic patients subsequently tested HIV-positive over 1 year. Behavioral risk-reduction interventions are urgently needed for male and female STI clinic patients.

People who are newly diagnosed with HIV infection are a critical population for prevention interventions, particularly individuals with co-occurring sexually transmitted infections (STIs). Although HIV is transmissible at any time during the course of HIV disease, infectiousness is greatest just after HIV seroconversion and during episodes of co-occurring STIs.¹ Research in the United States, Europe, and Australia shows that a significant minority of newly diagnosed HIV-positive persons continues to engage in HIV-transmission risk practices immediately after learning their HIV status.² In one study of recently seroconverted men who have sex with men, Colfax et al.³ found that HIV transmission risk behaviors persisted for a substantial number of infected men. Most concerning was the continued practice of unprotected anal intercourse with HIV-negative or unknown-HIV-status partners. Case–control and prospective cohort studies report that men who seroconvert for HIV are distinguishable from men who remain HIV-negative by their use of psychoactive drugs, sensation-seeking personality characteristics, and intentional risk taking.^4–6

Although the majority of HIV infections occur in southern Africa, there is little research available on the behavioral characteristics of people who seroconvert for HIV in this region. One study of Kenyan commercial sex workers showed that women who seroconverted for HIV demonstrated significant reductions in risk practices, with further risk behaviors diminishing over advancing HIV disease.⁷ The HIV epidemic in southern Africa is amplified by co-occurring STIs for several reasons. HIV transmission is facilitated by other STIs degrading naturally protective mucosal and epithelial barriers, creating a portal of entry to the bloodstream and increased access to HIV-susceptible cells. Studies of STI clinic patients show that the median time to HIV seroconversion is 1.5 years from initial STI clinic visit, and that substance use and sexual partners with STIs are major contributing factors to HIV seroconversion.⁸ Sexually transmitted infection clinic patients who seroconvert are at considerable risk for transmitting the virus to others because they are likely to be highly infectious.⁹ A meta-analysis of factors that influence per-act HIV-transmission risks showed that a history of ulcerative STI in either couple member increases the risk for HIV transmission more than 5-fold.¹⁰ Importantly, it is estimated that infectivity in the early stages of HIV infection is 9 times greater than during asymptomatic stages.¹⁰ Therefore, people diagnosed with an STI who also contract HIV represent a critical population for prevention interventions.

The purpose of our study was to examine the behavioral characteristics of STI clinic patients who seroconvert for HIV. We were particularly interested in identifying behavioral risk factors as well as subsequent behavior changes among STI clinic patients who test HIV-positive following an STI infection. To achieve these goals we conducted risk behavior assessments in a cohort of STI clinic patients who had tested HIV-negative and then subsequently tested HIV-positive compared with their persistently HIV-negative counterparts.

METHODS

Participants were 413 men and 203 women who were receiving services from a large public primary health care and STI specialty clinic between February 2006 and June 2008. Potential participants were referred by a clinic nurse to participate in the study, which involved completing computerized interviews, receiving a single counseling session, and participation in follow-up interviews over a 1-year period. The criterion for referral to the study was that the patient was being seen at the clinic for STI treatment services. The STI clinic that participated in this research is one of the largest in Cape Town, South Africa, a city with a population of more than 3 million people. Patients come to this clinic for services from throughout Cape Town as they are assured greater confidentiality than is offered at neighborhood primary health care centers. The clinic sees approximately 600 STI patients in a typical month. Approximately half of all patients have previously received STI services. The estimated clinic HIV prevalence is 25% based on reactive tests among the approximately 50% of patients who accept HIV testing.

Study Design and Procedures

We examined 29 STI clinic patients who were initially HIV-negative but later tested HIV-positive (seroconverters) and 77 who were confirmed persistently HIV-negative. All participants indicated that they were HIV-negative at the baseline and received another HIV test during the subsequent year. Participants completed informed consent prior to the baseline audio-computer–assisted structured interview (ACASI), followed by a single risk-reduction counseling session and treatment of their presenting STI. Participants completed follow-up ACASI interviews 1 year later and provided a separate consent to access and extract data from their clinic records. A trained and experienced STI nurse specialist familiar with the clinic charts and the national STI reporting system collected each participant's clinical record for all STI visits over the year. The nurse abstracted exact diagnostic entries and reviewed all charts twice to ensure complete abstraction. Clinic visits that occurred between the date of the baseline assessment and the 12-month follow-up were extracted. Participants were assured that their identities would be protected.

The flow of participants through the study is shown in Figure 1. Using chart abstracted STI codes, we identified 29 participants who were initially HIV-negative at baseline and either returned to the clinic for HIV voluntary testing and counseling and tested HIV-positive (n = 15) or indicated that they subsequently tested positive elsewhere during the observation period (n = 14). Of the original 625 participants, 187 were excluded from the study either because they had never been tested for HIV or because they were HIV-positive prior to the baseline assessment. In addition, 250 participants did not return to the clinic for HIV testing and did not report that they had tested HIV-positive elsewhere over the 1-year observation period. Participants who self-reported HIV-negative status at the follow-up but could not be confirmed to have retested HIV-negative were excluded to increase the internal validity of the study. A total of 82 participants were lost to follow-up. Therefore, we compared the 29 cases that were diagnosed with HIV infection with a control sample of 77 STI patients who were initially HIV-negative and subsequently confirmed to be HIV-negative prior to their 12-month follow-up.

FIGURE 1.

Flow of STI clinic patients who were initially HIV-negative and retested either HIV-positive or HIV-negative at 12-month follow-up: Cape Town, South Africa, 2006–2008.

Measures

We adapted measures from previous research conducted in South Africa. All measures were administered at the baseline and 12-month follow-up assessments in English and Xhosa, the 2 languages spoken by nearly all clinic patients. Participants viewed assessment items on a 15-inch color monitor, heard items read by machine (English) or human (Xhosa) voice through headphones, and responded by clicking a mouse. Research has shown that ACASI procedures yield reliable responses in sexual behavior interviews.¹¹ Participants were instructed on how to use the mouse and how to respond to measures prior to the baseline assessment and were provided with additional instruction in how to use the mouse when needed.

Demographic and HIV-risk history characteristics.

Participants reported demographic information, history of alcohol and other drug use, and history of exchanging sexual intercourse for money, a place to stay, or to meet other survival needs. Participants also reported whether they had engaged in intercourse that involved either their genitals or their partner's genitals bleeding, with those who had experienced bleeding during intercourse asked whether it had occurred in the past month and, if so, how many times.

Alcohol and other drug use.

We administered the Alcohol Use Disorder Identification Test (AUDIT),¹² a 10-item self-report instrument that includes quantity and frequency of alcohol use and was designed to identify individuals for whom the use of alcohol places them at risk for developing alcohol-related problems or who are currently experiencing alcohol-related problems. AUDIT scores range from 0 to 40, and scores of 8 or greater are used to identify individuals who may be experiencing problems with alcohol.¹³ AUDIT has been used in South Africa and is reliable and valid.¹⁴ To determine lifetime substance use, participants were also asked whether they had ever used dagga (cannabis), cocaine, Mandrax (methaqualone), or other drugs.

Sexual risk and protective behaviors.

Participants responded to items assessing number of male and female sexual partners and frequency of sexual behaviors in the previous month—specifically vaginal and anal intercourse with and without condoms. We selected a 30-day retrospective period because previous research has shown reliable reports of numbers of partners and sexual events within this time period.^15,16 Participants were instructed to think back over the past month and estimate the number of sexual partners and number of occasions in which they practiced each sexual behavior. In addition, we calculated the percentage of intercourse occasions protected by condoms by using the ratio: condom-protected vaginal intercourse plus condom-protected anal intercourse divided by total vaginal intercourse plus total anal intercourse. So we could assess condom use at the event level, participants were asked whether they or their sexual partner used a condom the most recent time they had sexual intercourse. Responses to the event-level measure were dichotomous (yes or no).

Data Analyses

We conducted 3 steps of data analysis to examine behaviors associated with HIV seroconversion. First, we performed descriptive analyses comparing the 29 participants who seroconverted to the 77 participants who were persistently HIV-negative on baseline characteristics by using t tests for continuous variables and contingency table χ² tests for categorical variables, and the Fisher exact test for tables with cells that contained values less than 5. Next, we examined differences between persons who had seroconverted and those who had not in terms of their substance use and sexual behaviors at the 12-month follow-up while we controlled for baseline rates. These analyses used logistic regression with odds ratios (ORs) and 95% confidence intervals (CIs). Finally, we examined within-participant changes in behaviors for seroconverters and nonseroconverters. In these analyses we used repeated measures analyses of variance to test for behavior changes as well as the interaction between assessment time (baseline and 12-month follow-up) and seroconversion group (seroconverted and remained HIV-negative). Sexual-behavior frequency data were transformed by using the formula log₁₀(x + 1) for parametric tests with nontransformed observed values reported in the tables. For all analyses we defined statistical significance as P < .05.

RESULTS

A total of 14 men and 15 women who were initially HIV-negative at the baseline assessment tested HIV-positive within the subsequent year, representing 5% (29 of 578) of persons who were not HIV-positive at the baseline assessment. Seven (24%) of the 29 persons who tested HIV-positive had entered care services by the 12-month follow-up and were taking antiretroviral medications. We also identified 77 participants who repeatedly tested HIV-negative in the year following baseline, representing 17% (77 of 438) of the initially HIV-negative sample. Table 1 shows that women were significantly more likely to test HIV-positive over the follow-up than were men. However, there were no other demographic differences between participants who seroconverted and those who remained HIV-negative.

TABLE 1.

Demographic and HIV-Risk History Characteristics of STI Clinic Patients Who HIV Seroconverted and Patients Who Remained HIV-Negative At Follow-Up: Cape Town, South Africa, 2006–2008

	Seroconverters (n = 29), No. (%)	Remained HIV-Negative (n = 77), No. (%)	χ2
	Demographics
Men	14 (48)	58 (75)
Women	15 (52)	19 (25)	7.1**
Black	25 (86)	70 (91)
Other race	4 (14)	7 (9)	3.2
Unemployed	13 (45)	27 (35)	1.5
Married	4 (14)	25 (33)	5.1
Has children	17 (59)	48 (62)	0.1
	HIV-risk history
History of needle sharing	4 (14)	3 (4)	NSa
Received money for sexual intercourse	1 (3)	3 (4)	NSa
Given money for sexual intercourse	2 (7)	5 (6)	NSa
Genital bleeding during intercourse	9 (31)	9 (12)	5.6**
Genital bleeding during intercourse in previous month	7 (24)	6 (8)	5.2*
Circumcised (men only)	10 (71)	48 (84)	1.2

Note. NS = not significant; STI = sexually transmitted infection.

^aBy Fisher exact test.

*P < .05; **P < .01.

Comparisons between participants who were confirmed to have repeat tested HIV-negative (n = 77) and the remainder of those who were not HIV-positive at baseline (n = 501) showed that the groups did not differ on any demographic or risk-behavior characteristics except HIV-negative repeat testers were older (mean = 30.5 years; standard deviation [SD] = 8.2) than was the rest of the sample (mean = 28.9 years; SD = 6.7; t₅₇₇ = 2.2; P < .05). The repeat-test HIV-negative group also was more likely to have given someone money or materials in exchange for sexual intercourse (χ²_1,578 = 5.3; P < .05): 13 (12%) patients who repeat tested HIV-negative compared with 31 (5%) who were not confirmed to have repeat tested HIV-negative.

HIV Risk History Characteristics

There were no differences between seroconverters and those who remained uninfected in their history of needle sharing, sexual exchange, and male circumcision status. Results did indicate a significant association between seroconversion and baseline experience of coital bleeding. Participants who had ever engaged in sexual intercourse with blood present as well as participants who reported coital bleeding in the previous month were significantly more likely to seroconvert over the subsequent year (Table 1).

Substance Use and HIV Seroconversion

Table 2 shows alcohol and other drug use of participants who seroconverted and those who remained HIV-negative. Overall, alcohol use was relatively high in the sample at baseline including problem drinking and alcohol use before sexual activity. However, baseline alcohol use did not distinguish seroconverters from nonseroconverters. Reductions in drinking were observed across groups, with alcohol use in the previous month declining significantly more among seroconverters compared with those who remained HIV-negative. Other substance use was far less frequent than was alcohol use, but the same pattern was observed across groups. There were no differences in drug use between groups at baseline and both HIV seroconverters and persistently seronegative groups evidenced reductions in drug use over the subsequent year.

TABLE 2.

Alcohol and Drug Use Among STI Clinic Patients Who HIV Seroconverted and Patients Who Remained HIV-Negative At Follow-Up: Cape Town, South Africa, 2006–2008

	Seroconverters (n = 29), No. (%)	Remained HIV-Negative (n = 77), No. (%)	OR (95% CI)
Previous month alcohol use
Baseline	10 (35)	36 (47)
12-month follow-up	4 (14)	33 (43)	4.9* (1.4, 17.5)
Problem drinkinga
Baseline	11 (38)	30 (39)
12-month follow-up	3 (11)	12 (16)	2.6 (0.5, 13.6)
Alcohol use before sexual intercourse
Baseline	10 (35)	29 (38)
12-month follow-up	3 (10)	19 (25)	2.9 (0.7, 11.2)
Previous month other drug use
Baseline	4 (14)	13 (7)
12-month follow-up	1 (4)	11 (15)	4.8 (0.69, 41.4)
Drug use before sexual intercourse
Baseline	4 (14)	5 (6)
12-month follow-up	1 (3)	4 (5)	2.2 (0.2, 24.2)

Notes. CI = confidence interval; OR = odds ratio; STI = sexually transmitted infection.

^aAssessed by lcohol Use Disorder Identification Test. a 10-item self-report instrument that includes quantity and frequency of alcohol use and was designed to identify individuals for whom the use of alcohol places them at risk for developing alcohol-related problems or who are currently experiencing alcohol-related problems.¹²

^*P < .01.

Sexual Behavior and HIV Seroconversion

Table 3 shows the sexual behaviors at baseline and follow-up for seroconverters and persistently HIV-negative participants. Results demonstrated that the observed reduction in numbers of sexual partners was significant as well as were reductions in unprotected sexual behaviors. Sexual partners were reduced over the follow-up period among both seroconverters and participants who remained HIV-negative. At baseline, 14 (48%) participants who later seroconverted reported 2 or more sexual partners in the previous month as did 36 (47%) of nonseroconverters. At follow-up, only 3 (10%) seroconverters and 19 (25%) nonseroconverters reported multiple recent sexual partners. With only the exception of unprotected anal intercourse, which showed greater reduction among seroconverters, there were no significant differences in unprotected intercourse acts between seroconverters and participants who remained HIV-negative.

TABLE 3.

Sexual Behaviors Among STI Clinic Patients Who HIV Seroconverted and Patients Who Remained HIV Negative at Follow-Up: Cape Town, South Africa, 2006–2008

	Seroconverters (n = 29)		Remained HIV-Negative (n = 77)
	∑	Mean (SD)	∑	Mean (SD)	FWSF	Finteraction
Sexual partners
Baseline	65	2.2 (2.7)	129	1.7 (1.2)
12-month follow-up	26	0.9 (0.7)	99	1.3 (1.3)	19.1**	3.5
Unprotected vaginal intercourse
Baseline	98	3.4 (6.0)	141	1.8 (2.1)
12-month follow-up	17	0.6 (1.8)	55	0.7 (1.7)	31.6**	0.9
Unprotected anal intercourse
Baseline	39	1.3 (2.9)	37	0.5 (1.7)
12-month follow-up	0	0	10	0.1 (1.0)	17.1*	4.8*
Total unprotected intercourse
Baseline	137	4.7 (7.8)	178	2.3 (3.1)
12-month follow-up	17	0.6 (1.8)	65	0.8 (1.9)	56.5**	3.1
Vaginal intercourse with condoms
Baseline	118	4.1 (3.1)	473	6.1 (9.3)
12-month follow-up	218	7.5 (10.7)	475	6.1 (6.2)	1.5	0.7
Anal intercourse with condoms
Baseline	33	1.1 (2.5)	127	1.6 (6.2)
12-month follow-up	11	0.4 (1.7)	99	1.3 (3.9)	5.1*	1.1
Total protected intercourse
Baseline	151	5.2 (4.1)	300	7.8 (11.7)
12-month follow-up	229	7.8 (10.9)	574	7.5 (8.7)	0.2	0.1
Total sexual acts
Baseline	288	9.9 (8.7)	778	10.1 (11.8)
12-month follow-up	246	8.5 (10.8)	639	8.3 (9.0)	15.5*	0.7
% condom use
Baseline		66.9 (32.8)		66.7 (35.5)
12-month follow-up		90.9 (20.5)		89.3 (23.3)	23.1**	0.1
Times obtained condoms
Baseline		6.1 (5.1)		6.6 (6.7)
12-month follow-up		6.1 (9.9)		4.4 (3.9)	1.6	1.6

Notes. F_interaction = F test for the within-participant change × HIV status group interaction; F_WSF = F test for within-participants change; STI = sexually transmitted infection.

*P < .05; **P < .01.

Consistent with the reductions in unprotected sexual intercourse, we observed significant increases in the proportion of intercourse occasions protected by condoms. There were no indications of greater condom use among seroconverters compared with persistently HIV-negative participants at the 1-year follow-up. This same pattern was observed for condom use at most recent sexual intercourse, where 22 (78%) seroconverters had used a condom during most recent intercourse at baseline as did 66 (59%) of the persistently seronegative participants, with nonsignificant differences for increases in this behavior for seroconverters (n = 26; 90%) and seronegative participants (n = 59; 77%) at follow-up (OR = 2.3; 95% CI = 0.7, 7.6).

DISCUSSION

Individuals who contract STIs in southern Africa are among the highest-risk populations for HIV infection in the world. We observed 5% of STI clinic patients who were initially HIV-negative subsequently test HIV-positive during 1 year of observation. The only demographic characteristic that distinguished patients who tested HIV-positive was gender; women were significantly more likely to test positive at follow-up than men. There were few differences in HIV-risk history characteristics, substance use, and baseline sexual risk behaviors. One behavioral risk characteristic that did differentiate people who seroconverted was engaging in sexual activity that involved blood. Lifetime coital bleeding, as well as coital bleeding within a month of the baseline, was significantly associated with subsequently testing HIV-positive. Previous research has shown that genital bleeding during sexual intercourse is common among South African STI clinic patients, with as many as 1 in 3 patients reporting coital bleeding, particularly menstrual bleeding, during intercourse.^17,18 Genital ulcers also facilitate HIV transmission and may bleed during sexual intercourse. However, to our knowledge, this is the first prospective cohort study to show an association between coital bleeding regardless of the source and HIV seroconversion in STI clinic patients in Africa.

Research conducted with people living with HIV/AIDS in southern Africa has shown that even years after testing HIV-positive a significant minority of HIV-infected men and women continue HIV-transmission risk practices.^19,20 Substance use and a history of other STIs are consistently associated with HIV infection²¹ and more women are HIV-infected than are men.²² These findings converge with the current study of newly diagnosed HIV-positive STI clinic patients. Among populations diagnosed with HIV, STI clinic patients are a priority for prevention interventions because of their known risks for transmission and likely dangerous state of infectiousness.²³

Our findings also indicate significant reductions in sexual risk behaviors over the year following an STI clinic visit. The observed reductions in risk behaviors were not greater among people who tested HIV-positive than they were among patients who persistently tested HIV-negative. The lack of differences between groups for reductions in sexual risk behaviors was surprising; we expected greater reductions in high-risk behaviors among people who tested HIV-positive because of their known potential risks for transmitting HIV to partners. However, with the exception of unprotected anal intercourse, people who tested HIV-positive did not reduce their sexual risk behaviors to a greater degree than people who persistently tested HIV-negative. We observed a similar pattern for the proportion of intercourse occasions protected by condoms, with significant increases over time and no differences between groups. These findings suggest an urgent need for HIV-risk reduction interventions for STI clinic patients who test HIV-positive.

The current study findings should be interpreted in light of their methodological limitations. This study was conducted in a single STI clinic in Cape Town. We therefore caution against the generalization of these results to other clinics as well as to other regions within South Africa. The generalizability of our findings is further limited by the number of participants that we could not confirm were retested HIV-negative at follow-up. We excluded a large number of participants to increase internal validity of the study at the expense of potentially reducing the generalizability of our findings. In addition, we relied on self-report for behavioral assessments, although we used the ACASI method, which is more reliable than interviewing.¹¹ Our behavioral measures are subject to self-report biases and therefore represent lower-bound estimates of risk behaviors. Our observation period for monitoring the cohort was relatively brief, constricting our ability to consider long-term predictors of HIV infection. Finally, because only a portion of the cohort elected to receive HIV testing, we cannot make inferences about the HIV prevalence or incidence in the clinic. With these limitations in mind, we believe that our findings have important implications for HIV prevention in STI clinic settings.

The most common intervention for reducing HIV transmission risks among people who test HIV-positive is partner notification.²⁴ In addition, people who test HIV-positive are routinely referred for HIV treatment and care services. There is also now widespread encouragement for interventions designed for people who have tested HIV-positive, termed positive prevention.^25,26 Our findings illustrate that positive prevention interventions should be implemented at the time a person tests HIV-positive and should include aggressive diagnosis and treatment of STIs.²⁷ In addition, brief HIV-risk reduction counseling can be tailored for people with HIV infection, therefore offering opportunities to intervene in STI clinic settings.²⁸ The STI clinics offer unique opportunities to identify people at high risk for HIV, those recently infected with HIV, and people chronically infected with HIV who contract other STIs. However, because few baseline characteristics distinguished people who tested HIV-positive, and because of the high HIV prevalence in clinic populations, South Africa's generalized HIV epidemic, and the low HIV testing uptake among STI clinic patients, we conclude that intensive HIV prevention interventions are urgently needed for all South African STI clinic patients, not just those who test HIV-positive.