Several demographic factors were associated with late presentation on bivariate analyses, including male gender (50% of males presented late vs. 36% of nonpregnant females), nonpregnancy (36% of nonpregnant women presented late vs. 15% of pregnant women), and older age (52%, 41%, and 35% of those aged 46-50, 31-45, and 16-25 years, respectively, presented late).
Socioeconomic factors associated with late presentation were lesser education (42% of those with no secondary education presented late vs. 33% of those with some secondary education or more), non-business occupation (43% of those unemployed, 42% of farmers, and 40% of those with other occupations vs. 33% of those with business employment presented late), no household water source (42% of those without piped water presented late vs. 37% of those with piped water), and more time required to travel to the ISS clinic (44%, 41%, and 35% of those traveling >2 hours, 30-60 minutes, and <30 minutes to clinic, respectively, presented late).
Household-related factors that were associated with late presentation included no children younger than 5 years in the household (46% of those with no children younger than 5 years presented late vs. 36% of those with 1 or more), no other HIV-infected household members (62% of those with no HIV-infected household members presented late vs. 39% of those with 1 or more), and unmarried status (43% of those who were widowed, 49% of those who were separated/divorced vs. 35% of those who were married presented late). Among married patients (n = 1218), factors associated with late presentation in bivariate analyses included proposed non-spousal HIV treatment supporter (45% of those who listed someone other than the patient's spouse vs. 33% of those who listed their spouse presented late), and HIV nondisclosure to spouse (43% of those who disclosed to another person who was not their spouse presented late vs. 34% of those who disclosed to their spouse).
Alcohol consumption in the past year was associated with HIV stage at presentation, with more non-drinkers presenting late (42%, 36%, and 32% of those who reported no alcohol use, moderate alcohol use, and heavy alcohol use, respectively, presented late).
In an era when highly active antiretroviral therapy is not only free but also widely available in Uganda, we found that 40% of new patients in a large HIV clinic had late-stage HIV disease at their initial clinic visit. This figure may represent a lower bound for late-stage presentation because the HIV stage was based on observable clinical signs and may have missed asymptomatic patients with advanced immunological disease. In a study in rural Uganda, 19% of those classified as at stage 1 or 2 HIV disease actually had CD4 counts of below 200 cells per milliliter.48 In addition, low detection of opportunistic infections, a plausible scenario in a busy clinical setting, may also have caused us to underestimate the proportion presenting with late-stage disease. We found that 50% of the men presented with severe disease compared with 36% of the nonpregnant women and 15% of the pregnant women. This suggests that current programs to routinely offer HIV testing and treatment for the prevention of mother-to-child transmission in antenatal clinics in Mbarara are successfully linking most HIV-infected women with HIV care. Prior HIV testing and counseling in prevention of mother-to-child transmission might also explain the lower rate of late presentation in nonpregnant women compared with men. However, other gender-related factors may be at play, as outpatient health service utilization in Uganda is generally higher among women than among men.49 Gender and pregnancy differences in stage at presentation have also been observed in Haiti, Canada, and several countries in Europe.21,26,50-52
Older age was also associated with late-stage presentation, which may be explained in part by the unavailability of HIV treatment in years past. Older people, on average, may have become infected longer ago and may have been more likely to suspend their clinic attendance for lack of treatment options. Another explanation for this finding could be that older people, like other low-risk groups, have a low self-perceived HIV risk, and therefore HIV test later than younger people, although this has not been shown in Africa.10,15,53-55 Other studies conducted in the United States,35 Europe,5,12,20,56-58 Australia,59 and Venezuela60 have shown similar associations of age with stage of HIV disease at presentation. Older age has been shown to compound the negative impact of late presentation on treatment outcomes both in Africa61 and in the Western world.62,63
Several socioeconomic factors were associated with late presentation to the ISS clinic. We found that patients with some secondary education had significantly lower odds of presenting with late-stage disease compared with those with none; this has also been noted in the United States as well as in Venezuela.60,64,65 Similarly, those who were employed were less likely to present late than those who were unemployed. Travel time to clinic was associated with late presentation on bivariate analysis but not on multivariate analyses that controlled for other indicators of economic status and family responsibilities. These findings suggest that there may be structural barriers to seeking care in a rural setting where the travel to the only public hospital may require a substantial investment of time and money.
Several variables related to household and marriage were associated with HIV stage at presentation. Being married was associated with earlier presentation as compared with being single, separated, or widowed, particularly among the women. Patients who had any children younger than 5 years in their household were also less likely to present late. Patients with young children, like pregnant women, may have more contact with the health care system and thus initiate HIV care earlier in the course of their disease. Among the married people, those who did not disclose their HIV status to their spouses were more likely to present late compared with those who disclosed, particularly among men. This suggests that the desire to hide one's HIV-positive status from a spouse may inhibit HIV care-seeking. Studies have shown that the rates of serostatus disclosure among sexual partners in Africa are low,66,67 and our findings suggest that this may discourage participation in HIV treatment programs.
Surprisingly, patients who reported hazardous or moderate alcohol use in the previous year had lower odds of presenting late compared with those who abstained from alcohol for at least 1 year. There may be several explanations for this, including that those who are the most ill, that is, those who are presenting with severe disease, are unlikely to feel healthy enough to consume alcohol. Another explanation could be that alcohol users have a heightened risk perception, a phenomenon similar to that observed among injecting drug users and men who have sex with men in the United States.64 A last possibility is that there is a high mortality rate among HIV positives who consume alcohol, which caused the absence of many would-be late presenters from our sample of alcohol users. Further research is needed to determine the effect of alcohol on access to and receipt of HIV care and treatment.
The biggest limitations of this study are its cross-sectional design and selection bias. Because we did not follow HIV positives prospectively from time of diagnosis and instead drew our sample from a snapshot of clinic attendees, our analyses of delayed presentation do not represent the proportion or characteristics of HIV positives in the catchment area who never attended clinic. In addition, secular trends in the AIDS epidemic could also cause a variety of apparent associations. Last, underdiagnosis of late presentation may have caused bias to the null. However, these data serve as a preliminary examination of the amount of late presentation and factors associated with late presentation in the African setting where it is difficult to conduct large longitudinal studies.
The data we used came solely from information routinely collected during clinical encounters and as a result were lacking several potentially important variables. In particular, the ISS initial visit form did not include any questions regarding perceived or experienced HIV stigma, which has been shown to discourage HIV testing and counseling in sub-Saharan Africa.68,69 Nor did we capture patients' HIV care attitudes and beliefs, for example, perceived eligibility requirements for ART. Because we did not know the date of first positive HIV test, we were unable to determine whether late clinic presentation was attributable to a delay in HIV testing or in accessing treatment upon diagnosis. Therefore, we are limited in our ability to recommend appropriate interventions to hasten the initiation of HIV care.
The level of missing data was higher than in typical analytic studies. However, we felt that it was important to disseminate the findings if the missing data were unlikely to cause significant bias. We created separate categories for missing data and found that these categories were not associated with the outcome, except in 2 instances concerning household composition; it seems that the data were likely missing at random.
Despite these limitations, our study includes a large number of HIV-positive patients in a developing country, providing a preliminary investigation into demographic, psychosocial, and behavioral correlates of late clinic presentation in this context. The associations we observed may provide a framework on which to build a conceptual model of late presentation.
The large percentage of patients with late-stage HIV disease at their initial clinic visit suggests that barriers to HIV care are considerable in Uganda. Delays in HIV care have serious public health implications because opportunities to prevent further transmission through effective treatment with antiretroviral drugs are lost and because initiating treatment for HIV disease at an advanced stage leads to worse treatment outcomes than treatment started earlier. This study reveals a need to develop interventions that facilitate earlier entry into HIV care.
This study also suggests that low CD4 count at ART initiation, as observed in several studies in sub-Saharan Africa, may be due to the high frequency of late-stage presentation among new HIV-positive patients, rather than to selective treatment of patients with late-stage disease. Late presentation poses a significant threat to the success of large-scale ART. More research is needed to determine whether late presentation is due to delayed HIV diagnosis or a delay after diagnosis. Our findings suggest that in southwestern Uganda, potential interventions, whether designed to promote HIV testing or early entry into care, should target men, unmarried women, and older women, and those of lower socioeconomic status. In addition, we speculate that HIV testing programs may help accelerate initiation of HIV care by encouraging HIV serostatus disclosure to partners on positive diagnosis.
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