JAIDS Journal of Acquired Immune Deficiency Syndromes:
Epidemiology and Social Science
Late-Disease Stage at Presentation to an HIV Clinic in the Era of Free Antiretroviral Therapy in Sub-Saharan Africa
Kigozi, Isaac M MBChB, Msc*; Dobkin, Loren M MPH†; Martin, Jeffrey N MD, MPH‡; Geng, Elvin H MD, MPH†; Muyindike, Winnie MBChB, Mmed§; Emenyonu, Nneka I MPH¶; Bangsberg, David R MD, MPH¶; Hahn, Judith A PhD, MA†
From the *Uganda Research Initiative, Uganda; †Division of Infectious Diseases, San Francisco General Hospital, University of California, San Francisco, San Francisco, CA; ‡Department of Epidemiology and Biostatistics, University of California, San Francisco, San Francisco, CA; §Faculty of Medicine, Mbarara University of Science and Technology, Mbarara, Uganda; and ¶Massachusetts General Hospital, Harvard School of Medicine, Harvard Initiative on Global Health, Boston, MA.
Received for publication November 4, 2008; accepted March 12, 2009.
Supported by the US National Institutes of Health grants R25 MH064712, P30 MH062246, U01 AI069911, P30 AI027763, and R01 MH054907; the Starr Foundation AIDS International Scholarship Fund; the International AIDS Society HIV Research Trust; the East Africa International Epidemiologic Databases to Evaluate AIDS (IeDEA) Consortium; the Antiretroviral Treatment in Lower Income Countries (ARTLINC) Collaboration; and Mark and Lisa Schwartz.
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Correspondence to: Judith A. Hahn, PhD, MA, Division of Infectious Diseases, San Francisco General Hospital, University of California, San Francisco, UCSF Box 0811, San Francisco, CA 94143-0811 (e-mail: firstname.lastname@example.org).
Background: Access to free antiretroviral therapy in sub-Saharan Africa has been steadily increasing, and the success of large-scale antiretroviral therapy programs depends on early initiation of HIV care. However, little is known about the stage at which those infected with HIV present for treatment in sub-Saharan Africa.
Methods: We conducted a cross-sectional analysis of initial visits to the Immune Suppression Syndrome Clinic of the Mbarara University Teaching Hospital, including patients who had their initial visit between February 2007 and February 2008 (N = 2311).
Results: The median age of the patients was 33 years (range 16-81 years), and 64% were female. More than one third (40%) were categorized as late presenters, that is, World Health Organization disease stage 3 or 4. Male gender, age 46-60 years (vs. younger), lower education level, being unemployed, living in a household with others, being unmarried, and lack of spousal HIV status disclosure were independently associated with late presentation, whereas being pregnant, having young children, and consuming alcohol in the prior year were associated with early presentation.
Conclusions: Targeted public health interventions to facilitate earlier entry into HIV care are needed, as well as additional study to determine whether late presentation is due to delays in testing vs. delays in accessing care.
Sub-Saharan Africa remains the most affected region in the global AIDS epidemic, with an estimated 22.5 million people living with HIV in 2007. Increasing numbers of patients are receiving free HIV antiretroviral therapy (ART) in this region, with 1.7 million treated under the President's Emergency Plan for AIDS Relief.1 Approximately 37% of HIV positives in Uganda who meet eligibility criteria for HIV ART, based on either CD4 count ≤200 cells per milliliter or clinical diagnosis of World Health Organization (WHO) stage 3 or 4,2 are currently receiving ART.3
The health status of patients at the time of ART initiation plays a crucial role in the success of treatment. Patients with advanced HIV disease at the time of ART initiation are less likely to respond to treatment, are more likely to place financial strain on health services, and have a higher mortality rate compared with those who initiate earlier.4-12 In addition, late presentation poses a higher cumulative risk of HIV transmission to others, considering that earlier presentation and HIV-suppressing treatment might otherwise reduce viral load and risk of transmission.12-16
A large proportion of HIV-infected individuals in the developed world, roughly 15%-43%, present at clinics for care with advanced or severe disease (WHO stage 3 or 4, CDC Category B or C, or CD4 ≤200 cells/mL).5,7,17-26 Characteristics associated with late presentation in the developed world include older age, male sex, risk behavior (including injection drug and alcohol use), lower income, and low degree of education.17,27-34 However, little is known in low-income countries, particularly those in sub-Saharan Africa, about the proportion or characteristics of HIV-infected individuals who present late for care at clinics. A study of 31 patients in Haiti reported that 65% presented with a CD4 count less than 350 cells per milliliter.35 Several studies from sub-Saharan Africa have shown that a large number of patients have low CD4 cell counts at ART initiation36-39; however, it is not possible to determine how much of this is attributable to the sickest patients being prioritized for treatment. We are unaware of any other published studies that have examined HIV stage at presentation for care in low-income countries.
Quantifying the proportion of HIV-positive patients who present at clinics at WHO HIV disease stage 3 or 4 and identifying correlates of late presentation in sub-Saharan Africa may assist health professionals in allocating resources to different types of HIV care services, and in designing interventions to overcome barriers to early HIV care. We therefore conducted an analysis of medical records from patients' initial visit to the HIV clinic of a large referral hospital in southwestern Uganda to estimate the proportion of patients presenting at WHO stage 3 or 4, and to identify demographic, psychosocial, and behavioral correlates of late presentation. We also examined whether correlates of late presentation vary by sex.
Our sample included all patients who attended the Mbarara University Teaching Hospital Immune Suppression Syndrome (ISS) clinic for the first time between February 1, 2007, and February 29, 2008, and were accessing HIV care for the first time. The Mbarara University Teaching Hospital is the regional referral hospital for a population of 1.2 million in southwestern Uganda. As of February 29, 2008, the ISS clinic had 6381 active HIV-positive patients, 3939 of whom were receiving ART.
Data for this study were the patient information that is routinely collected at initial clinic visit on a standard form that was adapted from the Open Medical Record System, an electronic medical record system framework developed by Moi University and Indiana University for use in developing countries. The ISS initial visit form includes socio-demographic, behavioral, and clinical information, including physical examination findings, medication history, symptoms, WHO stage, and HIV treatment plan. The socio-demographic and behavioral data are collected by counselors, whereas the clinical data are collected by physicians. The data from this form are entered into the OpenMRS data management system (www.openmrs.org). Quality control checks are performed on 5% of entered records, through which electronic records are compared variable by variable with the original source document; entry errors occur in less than 1% of the data.
We used WHO stage at initial clinic visit as the outcome variable for these analyses. The WHO HIV staging system40 applies clinical conditions to measure disease progression and is widely used in resource-limited settings including sub-Saharan Africa, where laboratory values of disease stage (ie, CD4+ T-cell counts and plasma HIV RNA levels) are not always readily available. This staging system has been shown to reliably predict survival time and subsequent disease progression.41-45 We categorized WHO stage dichotomously as not severe (stages 1 and 2) or severe (stages 3 and 4), and clinic presentation as early or late, respectively.
Independent variables included socio-demographic information recorded on the ISS initial visit form such as gender, pregnancy, age, tribe, religion, socioeconomic status (ie, education level, occupation, monthly income, in-house running water), household composition (ie, number of children and adults), and marital status. We also examined variables directly related to HIV care, such as the time required to travel to the ISS clinic, the number of HIV-infected household members, the number of those receiving HIV care, and among the married patients, whether they had disclosed their HIV status to their spouse, whether the spouse was HIV-infected, and whether the spouse was identified as the primary treatment supporter. We assessed alcohol use in the prior year using the Alcohol Use Disorders Identification Test-C (AUDIT-C),46 a shortened and validated version of the WHO-developed AUDIT.47
We calculated summary statistics to describe the general socio-demographic, medical, and behavioral features of the population. Where more than 2.5% of the data were missing for any independent variable, we created a separate category for the missing values. We used χ2 tests of association for nominal variables and χ2 trend tests for ordinal variables to compare patients missing WHO stage with those with WHO stage data. We similarly conducted unadjusted analyses and performed multivariable logistic regression to identify independent correlates of late presentation. Given our large sample size and the exploratory nature of the study, we included all variables in the model, except the number of HIV-infected household members and the number of household members in HIV care, because these variables were collinear with the total number of household members.
We also conducted multivariable analyses stratified by sex because we hypothesized that the psychosocial correlates of late presentation might differ by sex. Several variables were relevant to only the married participants, so we conducted additional analyses among the married participants only. In those analyses, we were unable to include whether the participants' spouses were identified as their HIV treatment supporters in the model due to collinearity with whether the participants had disclosed their HIV status to their spouses.
The study was approved by the ISS clinic data sharing committee and the Institutional Review Boards of Mbarara University of Science and Technology and the University of California, San Francisco.
Of the 2584 unique patients who presented to the ISS clinic between February 1, 2007, and February 29, 2008, we excluded 58 who had received prior HIV care elsewhere. For 216 patient records, no WHO stage or specific clinical condition was checked on the ISS initial visit form to indicate WHO stage. We compared patients who had WHO stage information (n = 2311) with those who had none (n = 216) and found the 2 groups to be similar (P > 0.05) in all analyzed characteristics: gender, age, tribe, religion, level of education, occupation, income, household water source, alcohol use, time required to travel to ISS clinic, number of children younger than 5 years, number of household members, number of HIV-positive household members and number receiving HIV care, marital status, treatment supporter, HIV status of spouse, and disclosure of HIV status to spouse.
We therefore analyzed the records with WHO stage of 2311 unique patients. The median age of the patients was 33 years (range 16-81 years) (Table 1). The sample was 64% female, including 4% who were pregnant. Fifty-five percent of the total sample reported being married. Twenty-two percent reported having had some secondary school education and 7% reported at least some college education. The majority (80%) reported a monthly income that is the equivalent of US $60 or less and 38% were farmers. More than one third (40%) presented at the ISS clinic late, that is, at a severe WHO disease stage (35% stage 3 and 5% stage 4), whereas 60% were presented early (23% stage 1 and 37% stage 2).
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- and Family-Related Factors
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).
We also conducted multivariate analyses (Table 2) using all the variables studied except the number of HIV-infected household members and the number of household members in HIV care because of collinearity with the total number of household members. We found that male gender, older age, local tribal identity (Munyankole), having no secondary school education, being unemployed, having no children younger than 5 years, not reporting living alone, and being unmarried or missing marital status were independently associated with presenting late at WHO stage 3 or 4, whereas being pregnant and reporting some alcohol use in the past year were independently associated with presenting early at WHO stage 1 or 2.
In multivariate analyses stratified by sex (Table 2), we found that among women, older age, having no children younger than 5 years and being unmarried remained independently associated with late presentation, and being pregnant and reporting hazardous alcohol use in the past year remained independently associated with early presentation. Among men, local tribal identity (Munyankole), having no secondary education, having no children younger than 5 years, and missing marital status remained independently associated with late presentation, whereas moderate or hazardous alcohol use in the past year remained independently associated with early presentation. Having no piped tap water at home was independently associated with late presentation among women, whereas it was associated with early presentation among men.
When we conducted analyses among the married participants only (Table 3), we included all variables used in the multivariate analyses listed above, and HIV status of spouse and HIV disclosure to spouse. We found that compared with patients who disclosed their HIV status to their spouses, patients who did not disclose the HIV status to their spouses were significantly more likely to present late, after controlling for all other variables. Other multivariate odds ratios among married patients were similar to those for the whole sample.
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.
1. The Power of Partnerships: Latest PEPFAR Results (June 2008). Government of the United States; 2008.
2. National Antiretroviral Treatment and Care Guidelines for Adults and Children. 2nd ed. 2008. Ministry of Health; Kampala, Uganda.
3. UNGASS Country Progress Report Uganda, January 2006 to December 2007. Government of Uganda, Kampala, Uganda.
4. Badri M, Lawn SD, Wood R. Short-term risk of AIDS or death in people infected with HIV-1 before antiretroviral therapy in South Africa: a longitudinal study. Lancet. 2006;368:1254-1259.
5. Castilla J, Sobrino P, de la Fuente L, et al. Late diagnosis of HIV infection in the era of highly active antiretroviral therapy: consequences for AIDS incidence. AIDS. 2002;16:1945-1951.
6. Chadborn TR, Baster K, Delpech VC, et al. No time to wait: how many HIV-infected homosexual men are diagnosed late and consequently die? (England and Wales, 1993-2002). AIDS. 2005;19:513-520.
7. Chadborn TR, Delpech VC, Sabin CA, et al. The late diagnosis and consequent short-term mortality of HIV-infected heterosexuals (England and Wales, 2000-2004). AIDS. 2006;20:2371-2379.
8. Egger M, May M, Chene G, et al. Prognosis of HIV-1-infected patients starting highly active antiretroviral therapy: a collaborative analysis of prospective studies. Lancet. 2002;360:119-129.
9. Hocking JS, Rodger AJ, Rhodes DG, et al. Late presentation of HIV infection associated with prolonged survival following AIDS diagnosis-characteristics of individuals. Int J STD AIDS. 2000;11:503-508.
10. Krentz HB, Auld MC, Gill MJ. The high cost of medical care for patients who present late (CD4<200 cells/μL) with HIV infection. HIV Med. 2004;5:93-98.
11. Lawn SD, Myer L, Harling G, et al. Determinants of mortality and nondeath losses from an antiretroviral treatment service in South Africa: implications for program evaluation. Clin Infect Dis. 2006;43:770-776.
12. Sabin CA, Smith CJ, Gumley H, et al. Late presenters in the era of highly active antiretroviral therapy: uptake of and responses to antiretroviral therapy. AIDS. 2004;18:2145-2151.
13. Bunnell R, Mermin J, De Cock KM. HIV prevention for a threatened continent: implementing positive prevention in Africa. JAMA. 2006;296:855-858.
14. Castilla J, Del Romero J, Hernando V, et al. Effectiveness of highly active antiretroviral therapy in reducing heterosexual transmission of HIV. J Acquir Immune Defic Syndr. 2005;40:96-101.
15. Girardi EMD, Sabin CAP, Monforte AD. Late diagnosis of HIV infection: epidemiological features, consequences and strategies to encourage earlier testing. J Acquir Immune Defic Syndr. 2007;46(Suppl):S3-S8.
16. Lima VD, Johnston K, Hogg RS, et al. Expanded access to highly active antiretroviral therapy: a potentially powerful strategy to curb the growth of the HIV epidemic. J Infect Dis. 2008;198:59-67.
17. Gay CL, Napravnik S, Eron JJ Jr. Advanced immunosuppression at entry to HIV care in the southeastern United States and associated risk factors. AIDS. 2006;20:775-778.
18. Gupta SB, Gilbert RL, Brady AR, et al, on behalf of the CDSSAG. CD4 cell counts in adults with newly diagnosed HIV infection: results of surveillance in England and Wales, 1990-1998. AIDS. 2000;14:853-861.
19. Girardi EMD, Aloisi MSB, Arici CMD, et al, for the IBESG. Delayed presentation and late testing for HIV: demographic and behavioral risk factors in a multicenter study in Italy. J Acquir Immune Defic Syndr. 2004;36:951-959.
20. Couturier E, Schwoebel V, Michon C, et al. Determinants of delayed diagnosis of HIV infection in France, 1993-1995. AIDS. 1998;12:795-800.
21. Samet JH, Retondo MJ, Freedberg KA, et al. Factors associated with initiation of primary medical care for HIV-infected persons. Am J Med. 1994;97:347-353.
22. Girardi E, Sampaolesi A, Gentile M, et al. Increasing proportion of late diagnosis of HIV infection among patients with AIDS in Italy following introduction of combination antiretroviral therapy. J Acquir Immune Defic Syndr. 2000;25:71-76.
23. Mugavero MJ, Castellano C, Edelman D, et al. Late diagnosis of HIV infection: the role of age and sex. Am J Med. 2007;120:370-373.
24. Schwarcz S, Hsu L, Dilley JW, et al. Late diagnosis of HIV infection: trends, prevalence, and characteristics of persons whose HIV diagnosis occurred within 12 months of developing AIDS. J Acquir Immune Defic Syndr. 2006;43:491-494.
25. McDonald AM, Li Y, Dore GJ, et al. Late HIV presentation among AIDS cases in Australia, 1992-2001. Aust N Z J Public Health. 2003;27:608-613.
26. Samet JH, Freedberg KA, Stein MD, et al. Trillion virion delay: time from testing positive for HIV to presentation for primary care. Arch Intern Med. 1998;158:734-740.
27. Chow KY, Ang LW, Verghesse I, et al. Measurable predictive factors for progression to AIDS among HIV-infected patients in Singapore. Ann Acad Med Singapore. 2005;34:84-89.
28. Gardner LI Jr., Brundage JF, McNeil JG, et al. Predictors of HIV-1 disease progression in early- and late-stage patients: the U.S. Army Natural History Cohort. Military Medical Consortium for Applied Retrovirology. J Acquir Immune Defic Syndr. 1992;5:782-793.
29. Girardi E, Sabin CA, Monforte AD. Late diagnosis of HIV infection: epidemiological features, consequences and strategies to encourage earlier testing. J Acquir Immune Defic Syndr. 2007;46(Suppl 1):S3-S8.
30. Hocking JS, Rodger AJ, Rhodes DG, et al. Late presentation of HIV infection associated with prolonged survival following AIDS diagnosis-characteristics of individuals. Int J STD AIDS. 2000;11:503-508.
31. Lanoy E, Mary-Krause M, Tattevin P, et al. Frequency, determinants and consequences of delayed access to care for HIV infection in France. Antivir Ther. 2007;12:89-96.
32. Masson CL, Sorensen JL, Phibbs CS, et al. Predictors of medical service utilization among individuals with co-occurring HIV infection and substance abuse disorders. AIDS Care. 2004;16:744-755.
33. Mugavero MJ, Castellano C, Edelman D, et al. Late diagnosis of HIV infection: the role of age and sex. Am J Med. 2007;120:370-373.
34. Samet JH, Freedberg KA, Savetsky JB, et al. Understanding delay to medical care for HIV infection: the long-term non-presenter. AIDS. 2001;15:77-85.
35. Louis C, Ivers LC, Smith Fawzi MC, et al. Late presentation for HIV care in central Haiti: factors limiting access to care. AIDS Care. 2007;19:487-491.
36. Braitstein P, Brinkhof MW, Dabis F, et al. Mortality of HIV-1-infected patients in the first year of antiretroviral therapy: comparison between low-income and high-income countries. Lancet. 2006;367:817-824.
37. Calmy A, Pinoges L, Szumilin E, et al. Generic fixed-dose combination antiretroviral treatment in resource-poor settings: multicentric observational cohort. AIDS. 2006;20:1163-1169.
38. Ferradini L, Jeannin A, Pinoges L, et al. Scaling up of highly active antiretroviral therapy in a rural district of Malawi: an effectiveness assessment. Lancet. 2006;367:1335-1342.
39. Stringer JSA, Zulu I, Levy J, et al. Rapid scale-up of antiretroviral therapy at primary care sites in Zambia: feasibility and early outcomes. JAMA. 2006;296:782-793.
40. WHO. Interim WHO Clinical Staging of HIV/AIDS and HIV/AIDS Case Definitions for Surveillance. Geneva, Switzerland: World Health Organization; 2005.
41. Vandenbruaene M, Colebunders R, Goeman J, et al. Evaluation of two staging systems for HIV infection for use in developing countries. AIDS. 1993;7:1613-1615.
42. Kassa E, Rinke de Wit TF, Hailu E, et al. Evaluation of the World Health Organization staging system for HIV infection and disease in Ethiopia: association between clinical stages and laboratory markers. AIDS. 1999;13:381-389.
43. Malamba SS, Morgan D, Clayton T, et al. The prognostic value of the World Health Organisation staging system for HIV infection and disease in rural Uganda. AIDS. 1999;13:2555-2562.
44. Ghate MV, Mehendale SM, Mahajan BA, et al. Relationship between clinical conditions and CD4 counts in HIV-infected persons in Pune, Maharashtra, India. Natl Med J India. 2000;13:183-187.
45. Teck R, Ascurra O, Gomani P, et al. WHO clinical staging of HIV infection and disease, tuberculosis and eligibility for antiretroviral treatment: relationship to CD4 lymphocyte counts. Int J Tuberc Lung Dis. 2005;9:258-262.
46. Bush K, Kivlahan DR, McDonell MB, et al, for the Ambulatory Care Quality Improvement Project. The AUDIT Alcohol Consumption Questions (AUDIT-C): an effective brief screening test for problem drinking. Arch Intern Med. 1998;158:1789-1795.
47. Saunders JB, Aasland OG, Babor TF, et al. Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO Collaborative Project on Early Detection of Persons with Harmful Alcohol Consumption-II. Addiction. 1993;88:791-804.
48. Kagaayi J, Makumbi F, Nakigozi G, et al. WHO HIV clinical staging or CD4 cell counts for antiretroviral therapy eligibility assessment? An evaluation in rural Rakai district, Uganda. AIDS. 2007;21:1208-1210.
49. Nabyonga J, Desmet M, Karamagi H, et al. Abolition of cost-sharing is pro-poor: evidence from Uganda. Health Policy Plan. 2005;20:100-108.
50. Biber CL, Jaker MA, Kloser P, et al. A study of sex differences in presentation for care of HIV. AIDS Patient Care STDS. 1999;13:103-110.
51. Guenter CD, Gill MJ, Samet JH, et al. A population with short delay from diagnosis of human immunodeficiency virus to medical care. Arch Intern Med. 1999;159:758-759.
52. Klein H, Elifson KW, Sterk CE. “At risk” women who think that they have no chance of getting HIV: self-assessed perceived risks. Women Health. 2003;38:47-63.
53. Del Pierre C, Cuzin L, Lauwes-Cances V, et al. High-risk groups for late diagnosis of HIV infection: A need for rethinking testing policy in the general population. AIDS Patient Care and STDS. 2006;20:838-847.
54. Manavi K, McMillan A, Ogilvie M, et al. Heterosexual men and women with HIV test positive at a later stage of infection than homo- or bisexual men. Int J STD AIDS. 2004;15:811-814.
55. Samet JH, Retondo MJ, Freedberg KA, et al. Factors associated with initiation of primary medical care for HIV-infected persons. Am J Med. 1994;97:347-353.
56. Girardi E, Sampaolesi A, Gentile M, et al. Increasing proportion of late diagnosis of HIV infection among patients with AIDS in Italy following introduction of combination antiretroviral therapy. J Acquir Immune Defic Syndr. 2000;25:71-76.
57. Gupta SB, Gilbert RL, Brady AR, et al. CD4 cell counts in adults with newly diagnosed HIV infection: results of surveillance in England and Wales, 1990-1998. CD4 Surveillance Scheme Advisory Group. AIDS. 2000;14:853-861.
58. Porter K, Wall PG, Evans BG. Factors associated with lack of awareness of HIV infection before diagnosis of AIDS. BMJ. 1993;307:20-23.
59. Gillieatt SJ, Mallal SA, French MA, et al. Epidemiology of late presentation of HIV infection in Western Australia. Med J Aust. 1992;157:117-118.
60. Bonjour M, Montagne M, Zambrano M, et al. Determinants of late disease-stage presentation at diagnosis of HIV infection in Venezuela: a case-case comparison. AIDS Res Ther. 2008;5:6.
61. Toure S, Kouadio B, Seyler C, et al. Rapid scaling-up of antiretroviral therapy in 10,000 adults in Cote d'Ivoire: 2-year outcomes and determinants. AIDS. 2008;22:873-882.
62. Egger M, May M, Chêne G, et al. Prognosis of HIV-1-infected patients starting highly active antiretroviral therapy: a collaborative analysis of prospective studies. Lancet. 2002;360:119-129.
63. The Antiretroviral Therapy Cohort C. Prognosis of HIV-1-infected patients up to 5 years after initiation of HAART: collaborative analysis of prospective studies. AIDS. 2007;21:1185-1197.
64. CDC. Late versus early testing of HIV-16 Sites, United States, 2000-2003. MMWR Morb Mortal Wkly Rep. 2003;52:581-586.
65. Schoenborn CA, Marsh SL, Hardy AM. AIDS knowledge and attitudes for 1992. Data from the National Health Interview Survey. Adv Data. 1994;23:1-16.
66. Antelman G, Smith Fawzi MC, Kaaya S, et al. Predictors of HIV-1 serostatus disclosure: a prospective study among HIV-infected pregnant women in Dar es Salaam, Tanzania. AIDS. 2001;15:1865-1874.
67. Medley A, Garcia-Moreno C, McGill S, et al. Rates, barriers and outcomes of HIV serostatus disclosure among women in developing countries: implications for prevention of mother-to-child transmission programmes. Bull World Health Organ. 2004;82:299-307.
68. Kalichman SC, Simbayi LC. HIV testing attitudes, AIDS stigma, and voluntary HIV counselling and testing in a black township in Cape Town, South Africa. Sex Transm Infect. 2003;79:442-447.
69. Weiser SD, Heisler M, Leiter K, et al. Routine HIV testing in Botswana: a population-based study on attitudes, practices, and human rights concerns. PLoS Med. 2006;3:e261.
This article has been cited 17 time(s).
Journal of the International AIDS SocietyHow a masculine work ethic and economic circumstances affect uptake of HIV treatment: experiences of men from an artisanal gold mining community in rural eastern UgandaJournal of the International AIDS Society
Plos OneHIV Prevention in Care and Treatment Settings: Baseline Risk Behaviors among HIV Patients in Kenya, Namibia, and TanzaniaPlos One
AIDS Research and Human RetrovirusesTreatment Outcomes of HIV-Infected Adolescents Attending Public-Sector HIV Clinics Across Gauteng and Mpumalanga, South AfricaAIDS Research and Human Retroviruses
AIDS and BehaviorPredictors of Late Presentation for HIV Diagnosis: A Literature Review and Suggested Way ForwardAIDS and Behavior
AIDS and BehaviorEarly Uptake of HIV Clinical Care After Testing HIV-Positive During Home-Based Testing and Counseling in Western KenyaAIDS and Behavior
AIDS and BehaviorNo Association Found Between Traditional Healer Use and Delayed Antiretroviral Initiation in Rural UgandaAIDS and Behavior
Global Health ActionMedical causes of admissions to hospital among adults in Africa: a systematic reviewGlobal Health Action
AIDS and BehaviorHow Does Antiretroviral Treatment Attenuate the Stigma of HIV? Evidence from a Cohort Study in Rural UgandaAIDS and Behavior
Plos OneRisk Factors for Late-Stage HIV Disease Presentation at Initial HIV Diagnosis in Durban, South AfricaPlos One
Hiv MedicineAssociation of injecting drug use and late enrolment in HIV medical care in Odessa Region, UkraineHiv Medicine
Plos OneSensitivity of Five Rapid HIV Tests on Oral Fluid or Finger-Stick Whole Blood: A Real-Time Comparison in a Healthcare SettingPlos One
Journal of the International AIDS SocietyFactors associated with loss to clinic among HIV patients not yet known to be eligible for antiretroviral therapy (ART) in MozambiqueJournal of the International AIDS Society
Journal of Health Care for the Poor and Underserved
The Problem of Late ART Initiation in Sub-Saharan Africa: A Transient Aspect of Scale-up or a Long-term Phenomenon?
Journal of Health Care for the Poor and Underserved, 24(1):
Ajar-African Journal of AIDS ResearchOlder people living with HIV in Uganda: understanding their experience and needsAjar-African Journal of AIDS Research
Social Science & MedicineDividuality, masculine respectability and reputation: How masculinity affects men's uptake of HIV treatment in rural eastern UgandaSocial Science & Medicine
Journal of Antimicrobial ChemotherapyFactors associated with late antiretroviral therapy initiation in Cameroon: a representative multilevel analysisJournal of Antimicrobial Chemotherapy
Bmc International Health and Human RightsHIV testing and care in Burkina Faso, Kenya, Malawi and Uganda: ethics on the groundBmc International Health and Human Rights
antiretroviral therapy; access; sub-Saharan Africa; late presentation
© 2009 Lippincott Williams & Wilkins, Inc.
Highlight selected keywords in the article text.