Abstract

Understanding the natural history of human immunodeficiency virus type 1 (HIV-1) and opportunistic infections in sub-Saharan Africa is necessary to optimize strategies for the prophylaxis and treatment of opportunistic infections and to understand the likely impact of antiretroviral therapy. We undertook a systematic review of the literature on HIV-1 infection in sub-Saharan Africa to assess data from recent cohorts and selected cross-sectional studies to delineate rates of opportunistic infections, associated CD4 cell counts, and associated mortality. We searched the MEDLINE database and the Cochrane Database of Systematic Reviews and Cochrane Clinical Trials Register for English-language literature published from 1990 through April 2002. Tuberculosis, bacterial infections, and malaria were identified as the leading causes of HIV-related morbidity across sub-Saharan Africa. Of the few studies that reported CD4 cell counts, the range of cell counts at the time of diagnosis of opportunistic infections was wide. Policies regarding the type and timing of opportunistic infection prophylaxis may be region specific and urgently require further study.

Once infected with HIV-1, the progression to AIDS and premature death is the reality for people in most poor countries [1, 2]. Infection has spread to >20% of the population in 7 sub-Saharan countries, and several others are close behind [3]. This disease burden resulted in >2 million HIV-related deaths in 2001 and has reduced the average life expectancy in sub-Saharan Africa from an anticipated 62 years to ∼47 years today [2]. On the basis of current trends, a 15-year-old Zimbabwean, born in 1997, will have a 40%–50% risk of acquiring HIV infection and early death [4]. The impact on individuals, families, and the economies of Africa is profound [5, 6].

Although behavioral prevention efforts continue, increasing attention is being given to the treatment of those already infected with HIV-1 [7]. Trimethoprim-sulfamethoxazole (TMP-SMZ) therapy, the mainstay of Pneumocystis carinii pneumonia (PCP) prophylaxis in North America, Europe, and Australia, has shown promising results, especially in the prevention of serious bacterial infections [8–10]. There is also a growing body of knowledge regarding the role of tuberculosis prophylaxis, prophylaxis against Cryptococcus species, and the use of vaccines [11]. In addition, the use of HAART in Côte d'Ivoire, Senegal, Uganda, and other low-income countries demonstrates the promise of further significant reductions in HIV-1–related morbidity and mortality [12–14].

The existing framework of clinical care and policy in the United States and Europe was developed by use of cohort studies delineating rates of opportunistic infections and the role of laboratory testing in determining susceptibility to opportunistic pathogens and in survival [10, 15–18]. In sub-Saharan Africa and most low-income settings, the relationships of these parameters are far less clear, in part because of the scarcity of cohorts with complete laboratory testing and diagnostic capabilities [19, 20].

Here, we review the existing literature on individual HIV-1–associated opportunistic infections sub-Saharan Africa, with an emphasis on recent cross-sectional studies and cohorts providing incidence rates, CD4 cell counts at the time at which opportunistic infections occurred, and survival associated with specific infections. We discuss the implications of these data for the prophylaxis of opportunistic infections and the introduction of HAART, and we discuss directions for future areas of research.

Methods

Literature search. We searched the MEDLINE database and the Cochrane Database of Systematic Reviews and Cochrane Clinical Trials Register for English-language literature published from 1990 through April 2002. Database search terms included “Africa,” “HIV,” “AIDS,” “bacteremia,”“Candida,” “candidiasis,”“Cryptococcus neoformans,” “cryptococcosis,” “Cryptosporidium,” “cytomegalovirus,” “diarrhea,” “enteritis,” “herpes zoster,” “Isospora belli,” “isosporiasis,” “malaria,” “meningitis,” “Microsporidium,” “Mycobacterium avium complex,” “Mycobacterium tuberculosis,” “Pneumocystis carinii pneumonia”(PCP), “pneumonia,” “Salmonella,” “Streptococcus pneumoniae,” “Toxoplasma gondii,” “toxoplasmosis,” and “varicella zoster virus.” We also conducted a manual search of references from publications and consulted experts in the field. Two reviewers (C.B.H. and E.L.) reviewed the lists of titles and abstracts and used the inclusion criteria to select potentially relevant articles for full review.

Inclusion criteria. To assess the incidence of opportunistic infections in HIV-1-infected adults, we included observational cohort studies of HIV-1-infected patients and placebo arms of randomized, controlled trials of preventive therapy or vaccine trials performed in sub-Saharan Africa. Studies selected were assessed for reported CD4 cell counts at or near the time of infection and for mortality. Cross-sectional studies were assessed for 1 of the following 3 study designs: consecutive or systematic selection of HIV-1-infected patients admitted to the hospital or clinic, yielding prevalence of an opportunistic infection; consecutive HIV-1-infected patients presenting to health care facilities with a symptom complex (e.g., cough and fever), yielding the prevalence of an opportunistic infection in patients presenting with that symptom complex (e.g., pneumococcal pneumonia); or autopsy studies of consecutive deaths of HIV-1-infected individuals, yielding the prevalence of an opportunistic infection.

Results

For each of the opportunistic infections described in this section, prevalence rates are presented first, followed by incidence rates, CD4 cell data, and data on mortality. The countries in which studies of specific infections have been performed are also shown (figure 1).

Figure 1

The location of selected opportunistic infection studies in sub-Saharan Africa. C, Cryptococcus neoformans; CA, Candida albicans; CM, cytomegalovirus; CS, Cryptosporidium species; I, Isospora belli; M, malaria; MA, Mycobacterium avium complex; MS, Microsporidium species; P, Pneumocystis carinii pneumonia; S, Salmonella species; SP, Streptococcus pneumoniae; T, toxoplasmosis; TB, Mycobacterium tuberculosis; V, varicella zoster virus.

Mycobacterial Infections

M. tuberculosis. Tuberculosis was diagnosed in 27%–34% of consecutive HIV-1-infected patients admitted to hospitals in Kenya [21] and South Africa [22], 39% of rural Tanzanians presenting with respiratory symptoms [23], and 61% of Burundian patients with AIDS [24]. Tuberculosis was diagnosed by smear or culture of a sputum sample and/or bronchoalveolar lavage or transbronchial biopsy in 23% of smear-negative Rwandan patients [25], 27% of inpatients in Burundi [26], 51% of patients in a respiratory ward in Abidjan [27], and 69% of highly selected patients in Tanzania [28]. The incidence of tuberculosis varied widely among cohorts of HIV-infected patients (table 1) [29–40].

Table 1

Incidence of Mycobacterium tuberculosis disease among HIV-infected patients.

Median CD4 cell counts from cross-sectional studies of inpatients among whom all forms of tuberculosis were diagnosed had a range of 27–191 cells/µL in 2 studies from Côte d'Ivoire [27, 41] and were similar in cohort studies (table 1) [29, 31, 34, 36, 37]. Ambulatory patients who had pulmonary tuberculosis diagnosed had median CD4 cell counts of 317 cells/µL in the Democratic Republic of Congo [42] and from 198 cells/µL (patients with extrapulmonary tuberculosis) to 257 cells/µL (patients with pulmonary tuberculosis) in Côte d'Ivoire [43]. Autopsy studies of HIV-1-infected patients from medical wards in Côte d'Ivoire [44] and Kenya [45] found tuberculosis to be the primary cause of death in 32% and 47% of deaths, respectively.

M. aviumcomplex. In cross-sectional studies involving acutely ill HIV-1-infected patients, the prevalence of M. avium complex bacteremia was 0%–6% of inpatients in Zambia [46], Kenya [47, 48], Malawi [49], Tanzania [50], and Uganda [51, 52], and it was as high as 10% in a study of patients who met criteria for suspected tuberculosis in South Africa [53]. The mean CD4 cell count at the time of diagnosis of disseminated M. avium complex was 10–23 cells/µL in Kenyan [47] and South African studies [53].

The rate of in-hospital mortality associated with M. avium complex bacteremia was 67% (2 patients) in Kenya [47], 14% (1 patient) in South Africa [53], and was not reported in most studies. Autopsy studies from Côte d'Ivoire and Kenya did not show M. avium complex as a cause of death [44, 45].

Bacterial Infections

S. pneumoniae. The prevalence of S. pneumoniae infection found by blood and sputum cultures ranged from 25% of cases of pneumonia in Cameroon [54] to 31% in Uganda [55]. By use of examination of transthoracic lung aspirates, thoracentesis, and bronchoscopy in selected patients, the prevalence was found to be 30% in Côte d'Ivoire [27] and 44% in Kenya [56]. Incidence rates of pneumonia and pneumococcal disease are presented in table 2 [29, 57, 58].

Table 2

Incidence of other opportunistic infections among HIV-infected patients.

Of consecutive, febrile, HIV-1-infected patients with bloodstream infections, 5% had pneumococcal infection in Tanzania (during the rainy season) [50], 17% had infection in Uganda [52], and 34% had infection in Malawi (during the dry season) [49]. The prevalence of S. pneumoniae bacteremia among patients with bloodstream infections in Côte d'Ivoire ranged from 10% in an infectious disease ward [41] to 36% in a respiratory ward [27]; it was 26%–28% among HIV-1-infected bacteremic patients admitted to the general medicine service at a central hospital in Kenya [21, 65].

Pyogenic pneumonia was the primary cause of 8% of inpatient deaths in Côte d'Ivoire [44] and of 27% inpatient deaths in Kenya [45]. The case-fatality rate for invasive pneumococcal disease was 0% among community-based patients in a Kenyan research cohort [58], 7% in Cameroon [54], 21%–29% in Kenya [21, 65], and 43% (3 deaths) among inpatients in Côte d'Ivoire [27].

Salmonellaspecies. Episodes of bacterial enteritis in HIV-1-infected patients accounted for 7% of admissions to an infectious disease ward in Côte d'Ivoire [41]. In HIV-1-infected inpatients with acute diarrhea, nontyphoidal Salmonella (Salmonella enteritidis and S. enteritidis serotype Typhimurium) were the most frequently recovered bacterial stool isolates in Bangui, Central African Republic [66], and Kenya [67]. Nontyphoidal Salmonella enteritis was an infrequent cause of hospital admissions (<1 case per 100 person-years of observation) in 2 cohorts [29, 60].

Of febrile, HIV-1-infected patients with bloodstream infection, nontyphoidal Salmonella bacteremia was detected in 18%–20% in Tanzania [50], Malawi [49], and Uganda [52]. It was detected via blood culture in 7%–12% of patients admitted to hospitals in Kenya [21] and Côte d'Ivoire [27, 41]. In the studies that provided in-hospital mortality data, 7% of patients with bacterial enteritis died in Abidjan [41], whereas 17% of inpatients with nontyphoidal Salmonella bacteremia died in Kenya [21].

Fungal Infections

C. neoformans. In studies of suspected cases of meningitis in HIV-1-infected patients, the prevalence of cryptococcal meningitis was 0% in Ghana (using only India ink staining for diagnosis) [68], 25% in Ethiopia [69], and 12%–50% in South Africa (determined by means of staining, latex agglutination testing, and culture) [70, 71]. Six percent of patients admitted to a general medicine ward in the Democratic Republic of Congo were diagnosed [72]. Incidence rates are shown in table 2 [29, 59, 60].

The median CD4 cell count in patients with C. neoformans and HIV coinfection was 16 cells/µL in South African [70] and Ugandan meningitis studies [59], and it was 70 cells/µL among consecutive patients in a Zimbabwean cohort [73]. Cryptococcal meningitis was the cause of 2% of deaths in a Côte d'Ivoire autopsy study [44] and 11% of deaths in an HIV-1-infected cohort in Uganda [74]. In a cohort from South Africa with a lower background mortality rate, cryptococcal meningitis accounted for 44% of deaths [29].

PCP. Among HIV-1-infected patients with respiratory disease, the prevalence of PCP was 1%–4% in Tanzanian studies (determined by examination of induced sputum and bronchoalveolar lavage specimens, in some cases) [23, 28], 5% in Burundi [26], and 22% in a study from Zimbabwe (in this study, nearly all patients underwent bronchoscopy) [75]. By use of bronchoalveolar lavage and/or transbronchial biopsy in patients with pulmonary disease that failed to respond to standard antibiotic therapy and with normal findings of initial tuberculosis diagnostic evaluations, studies in Rwanda [25], Malawi [76], Zambia [77], and the Democratic Republic of Congo [78] found a prevalence of 5%–11%. The prevalence was 27% in South Africa [79] and 33% in Zimbabwe; in the latter study, patients were required to have classic radiographic findings of PCP [80]. The incidence of PCP was low in cohort trials (table 2), although variable diagnostic modalities were used [29, 61].

The median CD4 cell count at the time of diagnosis of PCP was 134 cells/µL in Zimbabwe [80] and was not reported in other studies. PCP was the primary cause of death in 0%–2% of HIV-1-infected patients in autopsy series from Kenya [45] and Côte d'Ivoire [44].

Candidaspecies. The prevalence of oral and esophageal candidiasis ranged from 14% in pregnant women with HIV [81] to 67% of Senegalese inpatients with AIDS [22, 24, 82, 83]. Incidence rates are presented in table 2 [30, 31, 38]. Candida infection was not a cause of death in these studies or in autopsy studies [44, 45].

Parasitic Infections

Malaria. Multiple cross-sectional studies performed across sub-Saharan Africa showed no association between malaria and HIV-1 infection [19, 84–86]. Two subsequent cross-sectional studies of pregnant women from Malawi found that the prevalence of malaria parasitemia on the first prenatal visit was higher among HIV-1-infected women (32% and 54%, respectively) than among HIV-1-seronegative women (19% and 42%, respectively), a trend more pronounced with multigravidity [87, 88].

The risk of clinically diagnosed malaria (parasitemia and fever) was also significantly higher in HIV-1-infected patients in a cohort of Ugandan adults [63]. In this cohort, and in the placebo arm of a Ugandan vaccine trial, rates of clinical malaria were inversely related to CD4 cell counts (table 2) [62].

Toxoplasma gondii. Four percent of HIV-1-infected inpatients in Côte d'Ivoire received a confirmed diagnosis of cerebral toxoplasmosis, as assessed via CT scan and/or a therapeutic response to treatment [41]. The incidence of toxoplasmosis was low in cohorts with available data (table 2) [60, 61]. The median CD4 cell count in inpatients in Côte d'Ivoire was 44 cells/µL, and 60% of these patients died during that hospital admission [41]. An autopsy study from Côte d'Ivoire found toxoplasmosis to be a likely cause of death in 10% of HIV-infected patients [44], and toxoplasmosis was noted incidentally in 3% of autopsies in Kenya [45].

Cryptosporidium parvum, Microsporidiumspecies, andI. belli. The prevalence of Cryptosporidium infection among patients with chronic diarrhea varied from lows of 6%–9% in studies from the Central African Republic [66], Tanzania [89], and Zimbabwe [90] to 17% in Kenya [67], 25%–32% in Zambian studies (which examined multiple specimens, including small bowel biopsy specimens) [91, 92], and 35%–42% in rural Tanzanian studies [93, 94] and among Ugandan and Ethiopian patients with AIDS [95, 96]. Cryptosporidiosis was the primary cause of 1% of inpatient deaths in Côte d'Ivoire [44] and was not identified as a cause of death in Kenya [45].

Among patients with chronic diarrhea, Microsporidium infection (most commonly due to Enterocytozoon bieneusi) had a prevalence of 3%–5% (determined by trichrome staining or fluorescent examination of stool specimens) in Tanzania [89], Kenya [67], and the Central African Republic [66], and the prevalence was 11% (determined by water-ether sedimentation technique) in Zimbabwe [97]. In Zimbabwe, the prevalence was found to be 18% by trichrome staining, and it was found to be 51% by PCR [90]; in a Zambian study in which small bowel samples were obtained by biopsy, the prevalence was 35% [91].

The prevalence of I. belli infection ranged from 1% (urban patients) to 21% (rural patients) in Tanzania [89, 94]. The prevalence was 3% in the Central African Republic [66], and the prevalence was 16%–28% in a study from Zambia in which small bowel biopsy specimens were examined [91, 92]. Table 2 provides incidence data for Côte d'Ivoire [31]. The median CD4 cell count among inpatients was 105 cells/µL in Côte d'Ivoire, and 11% of these inpatients died while hospitalized [41].

Viral Infections

Varicella zoster virus. Among consecutive HIV-1-infected persons, herpes zoster was clinically diagnosed in 13% of outpatients in Botswana [98] and 24% of inpatients in Zimbabwe [99]. The incidence in cohorts from Uganda and Rwanda is shown in table 2 [38, 64]. After controlling for CD4 cell count and age, herpes zoster was not a predictor of early mortality in Uganda [64].

Cytomegalovirus. Several cross-sectional studies performed eye exams on HIV-infected individuals to identify cytomegalovirus retinitis. No cases were found among 120 HIV-1-infected patients in The Gambia [100], 2 cases of cytomegalovirus retinitis were diagnosed among 154 patients in Burundi [24], and 1 case was diagnosed among 99 Malawian patients with AIDS [101]. Cytomegalovirus pneumonitis was a primary cause of death in 4% of Kenyan inpatients [45], and disseminated cytomegalovirus disease caused 2% of deaths among inpatients in Côte d'Ivoire [44].

Discussion

Burden of illness. Data from studies performed across sub-Saharan Africa demonstrate the many infections to which HIV-1-infected individuals are susceptible in this region. Across studies, tuberculosis, bacterial infections, and malaria were the most common serious infections diagnosed in HIV-1-infected individuals. Tuberculosis not only caused a high proportion of cases of respiratory disease [23, 25–28], it contributed substantially to the overall burden of disease, as measured in autopsy studies [44, 45]. Bacterial diseases, including S. pneumoniae and Salmonella infections, also accounted for a great deal of morbidity in this population [27, 54–56]. The mortality rates for S. pneumoniae bacteremia in the research cohort setting [58] were much lower than the rates for hospital admissions elsewhere, which may demonstrate the advantages of early diagnosis and institution of appropriate therapy [21, 27, 54, 58, 65]. The evidence that malaria is a pathogen that differentially affects HIV-infected patients is strengthening, bolstered by several recent trials [62, 63, 87, 88]. Although autopsy studies show that malaria is not a frequent cause of death in HIV-infected patients [44, 45], any association between malaria and HIV infection could have important public health consequences as a result of their respective prevalences.

C. neoformans caused a high proportion of cases of meningitis among HIV-1-infected patients, and the high associated case-fatality rate reflects, in part, the absence of affordable treatment [69–71, 73]. Although PCP did not have a similar impact on mortality (as assessed by autopsy data), it was probably underdiagnosed as a result of the limited invasive testing in sub-Saharan Africa [25, 76–78] and may often be partially treated, given the frequency of use of TMP-SMZ and other antibiotics in the region. Parasites, such as Cryptosporidium, Microsporidium, and Isospora species, caused the majority of cases of chronic diarrhea in cross-sectional studies, and infections with these parasites have an increased incidence among HIV-infected patients.

M. avium complex was found infrequently in the sickest patients and was associated with high mortality rates, although studies were few and limited in size [47, 48, 53]. Toxoplasmosis was also rarely noted, but it was the cause of nearly 10% of deaths among HIV-1-infected patients in Côte d'Ivoire [44], indicating its lethality and likely underdiagnosis—the result of its insidious development and lack of diagnostic modalities. Limited studies assessed patients for cytomegalovirus infection and found very few cases [24, 100, 101]. Candida infection and herpes zoster were both frequently diagnosed, likely because of the high prevalence of infection and the relative ease of diagnosis.

Limitations. Although investigators have made a great deal of progress in understanding HIV disease in sub-Saharan Africa, data on prevalence and incidence in the literature are constrained by several major shortcomings: first, there are few studies from sub-Saharan Africa that observe HIV-infected patients from the time of seroconversion and that record data on CD4 cell counts and opportunistic infections over long periods of time. Even fewer studies perform active follow-up; most rely on passive follow-up to diagnose infections. Loss to follow-up was often substantial. Second, many opportunistic infections may be substantially underdiagnosed because of clinical and laboratory limitations. Third, many of the studies that do exist have widely varying methodologies and include small populations. Although we have attempted to highlight the features of studies that may account for the variable results, comparisons between studies and countries must be made with caution.

Implications for prophylaxis and HAART. Maximizing effective prophylaxis to reduce the incidence of opportunistic infections is the current medical strategy in many areas where HAART is not yet widely available [9, 11]. Given the burden of tuberculosis among HIV-1-infected Africans, the use of preventive therapy for tuberculosis has been the subject of multiple studies [102, 103]. A recent meta-analysis of tuberculosis prophylaxis trials in HIV-1-infected patients showed a reduction in tuberculosis by more than one-half only in skin test-positive patients, and there was no mortality-related benefit [103].

Trials of TMP-SMZ involving HIV-1-infected patients have found variable reductions in the incidence of severe events, such as bacterial pneumonia, Isospora enteritis, nontyphoidal Salmonella infection, and febrile parasitemia [8, 9]. Control of these high-impact infections with a simple, relatively well-tolerated regimen is attractive. However, this intervention may be limited by the threat of resistance. Rates of TMP-SMZ resistance in nontyphoidal Salmonella species are low in Côte d'Ivoire [9, 104] but are ⩾50% among Salmonella species in Kenya [105], Dakar [106], and Malawi [107]. Rates of S. pneumoniae resistance are similarly variable [107–109]. The clinical effect of these resistance patterns remains unclear [110], and there is further concern about cross-resistance with other drugs [107]. Although widely used in the United States, an initial trial of pneumococcal vaccine in sub-Saharan Africa showed an increase in the rate of morbidity that was associated with the vaccine [57].

Several preliminary studies show that HAART can improve immune function and decrease HIV RNA levels in sub-Saharan Africa [12–14]. The incidence of opportunistic infections in that region will likely decrease as a result, as has been observed with the introduction of antiretroviral therapy in the United States [16]. However, as efforts to implement these therapies are being developed, prophylaxis for opportunistic infections is an important concomitant step in preventing associated morbidity and mortality.

Many pressing questions remain about the risk of HIV-1-associated opportunistic infections in sub-Saharan Africa. How will widespread use of prophylactic regimens change the distribution of opportunistic infections, and what competing risks will emerge? What will be the effects of increasing antibiotic use on resistance patterns? How can initial efforts involving HAART be rapidly expanded to decrease the incidence of both opportunistic infections and mortality? Finally, what combination of vaccination, opportunistic infection prophylaxis, and HAART will be optimal? Combining observational data with ongoing intervention studies will help answer these questions.

Acknowledgements

We thank Jonathon Kaplan, M.D., for his assistance with this project and manuscript.

References

1
Morgan
D
Whitworth
J
The natural history of HIV-1 infection in Africa
Nat Med
2001
, vol. 
7
 (pg. 
143
-
5
)
2
UNAIDS/World Health Organization
AIDS epidemic update, December
2001
 
UNAIDS/01.74E-WHO/CDS/CSR/NCS/2001.2. Available at: http://www.unaids.org/epidemic_update/report_dec01/index.html. Accessed 12 April 2002
3
Piot
P
Bartos
M
Ghys
PD
Walker
N
Schwartlander
B
The global impact of HIV/AIDS
Nature
2001
, vol. 
410
 (pg. 
968
-
73
)
4
UNAIDS
Report on the global HIV/AIDS epidemic, June
2000
 
UNAIDS/00.13E. Available at: http://www.unaids.org/epidemic_update/report_june00/index.html. Accessed 12 April 2002
5
Urassa
M
Boerma
JT
Isingo
R
, et al. 
The impact of HIV/AIDS on mortality and household mobility in rural Tanzania
AIDS
2001
, vol. 
15
 (pg. 
2017
-
23
)
6
Dixon
S
McDonald
S
Roberts
J
The impact of HIV and AIDS on Africa's economic development
BMJ
2002
, vol. 
324
 (pg. 
232
-
4
)
7
Farmer
P
Leandre
F
Mukherjee
JS
, et al. 
Community-based approaches to HIV treatment in resource-poor settings
Lancet
2001
, vol. 
358
 (pg. 
404
-
9
)
8
Badri
M
Ehrlich
R
Wood
R
Maartens
G
Initiating co-trimoxazole prophylaxis in HIV-infected patients in Africa: an evaluation of the provisional WHO/UNAIDS recommendations
AIDS
2001
, vol. 
15
 (pg. 
1143
-
8
)
9
Anglaret
X
Chene
G
Attia
A
, et al. 
Early chemoprophylaxis with trimethoprim-sulphamethoxazole for HIV-1-infected adults in Abidjan, Cote d'Ivoire: a randomised trial. Cotrimo-CI Study Group
Lancet
1999
, vol. 
353
 (pg. 
1463
-
8
)
10
Guidelines for preventing opportunistic infections among HIV-infected persons—2002: recommendations of the US Public Health Service and the Infectious Diseases Society of America
MMWR Morb Mortal Wkly Rep
2002
, vol. 
51
 
(RR-8)
(pg. 
1
-
60
)
11
Grant
AD
Kaplan
JE
De Cock
KM
Preventing opportunistic infections among human immunodeficiency virus-infected adults in African countries
Am J Trop Med Hyg
2001
, vol. 
65
 (pg. 
810
-
21
)
12
Laurent
C
Diakhate
N
Gueye
NF
, et al. 
The Senegalese government's highly active antiretroviral therapy initiative: an 18-month follow-up study
AIDS
2002
, vol. 
16
 (pg. 
1363
-
70
)
13
Diop
Y
Bonard
D
Ba-Gomis
O
, et al. 
Prospective trial of CBV + IBV in West Africa [abstract 492]
Programs and abstracts of the 8th Conference on Retroviruses and Opportunistic Infections (Chicago)
2001
 
14
Landman
R
Schiemann
R
Thiam
S
, et al. 
Evaluation at 6 months of a once-a-day HAART regimen in treatment-naive HIV-1-infected adults in Denegal (ANRS 12-04 Study) [abstract 491]
Programs and abstracts of the 8th Conference on Retroviruses and Opportunistic Infections (Chicago)
2001
 
15
Enger
C
Graham
N
Peng
Y
, et al. 
Survival from early, intermediate, and late stages of HIV infection
JAMA
1996
, vol. 
275
 (pg. 
1329
-
34
)
16
Moore
RD
Chaisson
RE
Natural history of HIV infection in the era of combination antiretroviral therapy
AIDS
1999
, vol. 
13
 (pg. 
1933
-
42
)
17
Chaisson
RE
Gallant
JE
Keruly
JC
Moore
RD
Impact of opportunistic disease on survival in patients with HIV infection
AIDS
1998
, vol. 
12
 (pg. 
29
-
33
)
18
Panel on Clinical Practices for Treatment of HIV Infection
Guidelines for the use of antiretroviral agents in HIV-infected adults and adolescents, 2002. 4 February
2002
 
Available at: http://aidsinfo.nih.gov/guidelines/adult/AAMay23.pdf; accessed on 20 May 2002
19
Colebunders
RL
Latif
AS
Natural history and clinical presentation of HIV-1 infection in adults
AIDS
1991
, vol. 
5
 (pg. 
103
-
12
)
20
Grant
AD
Djomand
G
De Cock
KM
Natural history and spectrum of disease in adults with HIV/AIDS in Africa
AIDS
1997
, vol. 
11
 (pg. 
43
-
54
)
21
Arthur
G
Nduba
VN
Kariuki
SM
Kimari
J
Bhatt
SM
Gilks
CF
Trends in bloodstream infections among human immunodeficiency virus-infected adults admitted to a hospital in Nairobi, Kenya, during the last decade
Clin Infect Dis
2001
, vol. 
33
 (pg. 
248
-
56
)
22
Colvin
M
Dawood
S
Kleinschmidt
I
Mullick
S
Lallo
U
Prevalence of HIV and HIV-related diseases in the adult medical wards of a tertiary hospital in Durban, South Africa
Int J STD AIDS
2001
, vol. 
12
 (pg. 
386
-
9
)
23
Atzori
C
Bruno
A
Chichino
G
Gatti
S
Scaglia
M
Pneumocystis carinii pneumonia and tuberculosis in Tanzanian patients infected with HIV
Trans R Soc Trop Med Hyg
1993
, vol. 
87
 (pg. 
55
-
6
)
24
Cochereau
I
Mlika-Cabanne
N
Godinaud
P
, et al. 
AIDS related eye disease in Burundi, Africa
Br J Ophthalmol
1999
, vol. 
83
 (pg. 
339
-
42
)
25
Batungwanayo
J
Taelman
H
Lucas
S
, et al. 
Pulmonary disease associated with the human immunodeficiency virus in Kigali, Rwanda: a fiberoptic bronchoscopic study of 111 cases of undetermined etiology
Am J Respir Crit Care Med
1994
, vol. 
149
 (pg. 
1591
-
6
)
26
Kamanfu
G
Mlika-Cabanne
N
Girard
PM
, et al. 
Pulmonary complications of human immunodeficiency virus infection in Bujumbura, Burundi
Am Rev Respir Dis
1993
, vol. 
147
 (pg. 
658
-
63
)
27
Grant
A
Sidibe
K
Domoua
K
, et al. 
Spectrum of disease among HIV-infected adults hospitalised in a respiratory medicine unit in Abidjan, Cote d'Ivoire
Int J Tuberc Lung Dis
1998
, vol. 
2
 (pg. 
926
-
34
)
28
Daley
CL
Mugusi
F
Chen
LL
, et al. 
Pulmonary complications of HIV infection in Dar es Salaam, Tanzania: role of bronchoscopy and bronchoalveolar lavage
Am J Respir Crit Care Med
1996
, vol. 
154
 (pg. 
105
-
10
)
29
Corbett
EL
Churchyard
GJ
Charalambos
S
, et al. 
Morbidity and mortality in South African gold miners: impact of untreated disease due to human immunodeficiency virus
Clin Infect Dis
2002
, vol. 
34
 (pg. 
1251
-
8
)
30
Morgan
D
Mahe
C
Mayanja
B
Whitworth
JA
Progression to symptomatic disease in people infected with HIV-1 in rural Uganda: prospective cohort study
BMJ
2002
, vol. 
324
 (pg. 
193
-
6
)
31
Attia
A
Huet
C
Anglaret
X
, et al. 
HIV-1-related morbidity in adults, Abidjan, Cote d'Ivoire: a nidus for bacterial diseases
J Acquir Immune Defic Syndr
2001
, vol. 
28
 (pg. 
478
-
86
)
32
Quigley
MA
Mwinga
A
Hosp
M
, et al. 
Long-term effect of preventive therapy for tuberculosis in a cohort of HIV-infected Zambian adults
AIDS
2001
, vol. 
15
 (pg. 
215
-
22
)
33
Corbett
EL
Churchyard
GJ
Clayton
TC
, et al. 
HIV infection and silicosis: the impact of two potent risk factors on the incidence of mycobacterial disease in South African miners
AIDS
2000
, vol. 
14
 (pg. 
2759
-
68
)
34
Wood
R
Maartens
G
Lombard
CJ
Risk factors for developing tuberculosis in HIV-1-infected adults from communities with a low or very high incidence of tuberculosis
J Acquir Immune Defic Syndr
2000
, vol. 
23
 (pg. 
75
-
80
)
35
Whalen
CC
Johnson
JL
Okwera
A
, et al. 
A trial of three regimens to prevent tuberculosis in Ugandan adults infected with the human immunodeficiency virus. Uganda-Case Western Reserve University Research Collaboration
N Engl J Med
1997
, vol. 
337
 (pg. 
801
-
8
)
36
Hawken
MP
Meme
HK
Elliott
LC
, et al. 
Isoniazid preventive therapy for tuberculosis in HIV-1-infected adults: results of a randomized controlled trial
AIDS
1997
, vol. 
11
 (pg. 
875
-
82
)
37
Gilks
CF
Godfrey-Faussett
P
Batchelor
BI
, et al. 
Recent transmission of tuberculosis in a cohort of HIV-1-infected female sex workers in Nairobi, Kenya
AIDS
1997
, vol. 
11
 (pg. 
911
-
8
)
38
Leroy
V
Msellati
P
Lepage
P
, et al. 
Four years of natural history of HIV-1 infection in African women: a prospective cohort study in Kigali (Rwanda), 1988–1993
J Acquir Immune Defic Syndr Hum Retrovirol
1995
, vol. 
9
 (pg. 
415
-
21
)
39
Braun
MM
Badi
N
Ryder
RW
, et al. 
A retrospective cohort study of the risk of tuberculosis among women of childbearing age with HIV infection in Zaire
Am Rev Respir Dis
1991
, vol. 
143
 (pg. 
501
-
4
)
40
Allen
S
Batungwanayo
J
Kerlikowske
K
, et al. 
Two-year incidence of tuberculosis in cohorts of HIV-infected and uninfected urban Rwandan women
Am Rev Respir Dis
1992
, vol. 
146
 (pg. 
1439
-
44
)
41
Grant
AD
Djomand
G
Smets
P
, et al. 
Profound immunosuppression across the spectrum of opportunistic disease among hospitalized HIV-infected adults in Abidjan, Cote d'Ivoire
AIDS
1997
, vol. 
11
 (pg. 
1357
-
64
)
42
Mukadi
Y
Perriens
JH
St Louis
ME
, et al. 
Spectrum of immunodeficiency in HIV-1-infected patients with pulmonary tuberculosis in Zaire
Lancet
1993
, vol. 
342
 (pg. 
143
-
6
)
43
Ackah
AN
Coulibaly
D
Digbeu
H
, et al. 
Response to treatment, mortality, and CD4 lymphocyte counts in HIV-infected persons with tuberculosis in Abidjan, Cote d'Ivoire
Lancet
1995
, vol. 
345
 (pg. 
607
-
10
)
44
Lucas
SB
Hounnou
A
Peacock
C
, et al. 
The mortality and pathology of HIV infection in a West African city
AIDS
1993
, vol. 
7
 (pg. 
1569
-
79
)
45
Rana
FS
Hawken
MP
Mwachari
C
, et al. 
Autopsy study of HIV-1-positive and HIV-1-negative adult medical patients in Nairobi, Kenya
J Acquir Immune Defic Syndr
2000
, vol. 
24
 (pg. 
23
-
9
)
46
Waddell
RD
Lishimpi
K
von Reyn
CF
, et al. 
Bacteremia due to Mycobacterium tuberculosis or M. bovis, bacille Calmette-Guerin (BCG) among HIV-positive children and adults in Zambia
AIDS
2001
, vol. 
15
 (pg. 
55
-
60
)
47
Gilks
CF
Brindle
RJ
Mwachari
C
, et al. 
Disseminated Mycobacterium avium infection among HIV-infected patients in Kenya
J Acquir Immune Defic Syndr Hum Retrovirol
1995
, vol. 
8
 (pg. 
195
-
8
)
48
Fordham von Reyn
C
Arbeit
RD
Tosteson
AN
, et al. 
The international epidemiology of disseminated Mycobacterium avium complex infection in AIDS. International MAC Study Group
AIDS
1996
, vol. 
10
 (pg. 
1025
-
32
)
49
Archibald
LK
McDonald
LC
Nwanyanwu
O
, et al. 
A hospital-based prevalence survey of bloodstream infections in febrile patients in Malawi: implications for diagnosis and therapy
J Infect Dis
2000
, vol. 
181
 (pg. 
1414
-
20
)
50
Archibald
LK
den Dulk
MO
Pallangyo
KJ
Reller
LB
Fatal Mycobacterium tuberculosis bloodstream infections in febrile hospitalized adults in Dar es Salaam, Tanzania
Clin Infect Dis
1998
, vol. 
26
 (pg. 
290
-
6
)
51
Okello
DO
Sewankambo
N
Goodgame
R
, et al. 
Absence of bacteremia with Mycobacterium avium-intracellulare in Ugandan patients with AIDS
J Infect Dis
1990
, vol. 
162
 (pg. 
208
-
10
)
52
Ssali
FN
Kamya
MR
Wabwire-Mangen
F
, et al. 
A prospective study of community-acquired bloodstream infections among febrile adults admitted to Mulago Hospital in Kampala, Uganda
J Acquir Immune Defic Syndr Hum Retrovirol
1998
, vol. 
19
 (pg. 
484
-
9
)
53
von Gottberg
A
Sacks
L
Machala
S
Blumberg
L
Utility of blood cultures and incidence of mycobacteremia in patients with suspected tuberculosis in a South African infectious disease referral hospital
Int J Tuberc Lung Dis
2001
, vol. 
5
 (pg. 
80
-
6
)
54
Koulla-Shiro
S
Kuaban
C
Belec
L
Acute community-acquired bacterial pneumonia in human immunodeficiency virus (HIV) infected and non-HIV-infected adult patients in Cameroon: aetiology and outcome
Tuber Lung Dis
1996
, vol. 
77
 (pg. 
47
-
51
)
55
Yoshimine
H
Oishi
K
Mubiru
F
, et al. 
Community-acquired pneumonia in Ugandan adults: short-term parenteral ampicillin therapy for bacterial pneumonia
Am J Trop Med Hyg
2001
, vol. 
64
 (pg. 
172
-
7
)
56
Scott
JA
Hall
AJ
Muyodi
C
, et al. 
Aetiology, outcome, and risk factors for mortality among adults with acute pneumonia in Kenya
Lancet
2000
, vol. 
355
 (pg. 
1225
-
30
)
57
French
N
Nakiyingi
J
Carpenter
LM
, et al. 
23-Valent pneumococcal polysaccharide vaccine in HIV-1-infected Ugandan adults: double-blind, randomised and placebo controlled trial
Lancet
2000
, vol. 
355
 (pg. 
2106
-
11
)
58
Gilks
CF
Ojoo
SA
Ojoo
JC
, et al. 
Invasive pneumococcal disease in a cohort of predominantly HIV-1 infected female sex-workers in Nairobi, Kenya
Lancet
1996
, vol. 
347
 (pg. 
718
-
23
)
59
French
N
Gray
K
Watera
C
, et al. 
Cryptococcal infection in a cohort of HIV-1-infected Ugandan adults
AIDS
2002
, vol. 
16
 (pg. 
1031
-
8
)
60
Wiktor
SZ
Sassan-Morokro
M
Grant
AD
, et al. 
Efficacy of trimethoprim-sulphamethoxazole prophylaxis to decrease morbidity and mortality in HIV-1-infected patients with tuberculosis in Abidjan, Cote d'Ivoire: a randomised controlled trial
Lancet
1999
, vol. 
353
 (pg. 
1469
-
75
)
61
Maynart
M
Lievre
L
Sow
PS
, et al. 
Primary prevention with cotrimoxazole for HIV-1-infected adults: results of the pilot study in Dakar, Senegal
J Acquir Immune Defic Syndr
2001
, vol. 
26
 (pg. 
130
-
6
)
62
French
N
Nakiyingi
J
Lugada
E
Watera
C
Whitworth
JA
Gilks
CF
Increasing rates of malarial fever with deteriorating immune status in HIV-1-infected Ugandan adults
AIDS
2001
, vol. 
15
 (pg. 
899
-
906
)
63
Whitworth
J
Morgan
D
Quigley
M
, et al. 
Effect of HIV-1 and increasing immunosuppression on malaria parasitaemia and clinical episodes in adults in rural Uganda: a cohort study
Lancet
2000
, vol. 
356
 (pg. 
1051
-
6
)
64
Morgan
D
Mahe
C
Malamba
S
Okongo
M
Mayanja
B
Whitworth
J
Herpes zoster and HIV-1 infection in a rural Ugandan cohort
AIDS
2001
, vol. 
15
 (pg. 
223
-
9
)
65
Gilks
CF
Brindle
RJ
Otieno
LS
, et al. 
Life-threatening bacteraemia in HIV-1 seropositive adults admitted to hospital in Nairobi, Kenya
Lancet
1990
, vol. 
336
 (pg. 
545
-
9
)
66
Germani
Y
Minssart
P
Vohito
M
, et al. 
Etiologies of acute, persistent, and dysenteric diarrheas in adults in Bangui, Central African Republic, in relation to human immunodeficiency virus serostatus
Am J Trop Med Hyg
1998
, vol. 
59
 (pg. 
1008
-
14
)
67
Mwachari
C
Batchelor
BI
Paul
J
Waiyaki
PG
Gilks
CF
Chronic diarrhoea among HIV-infected adult patients in Nairobi, Kenya
J Infect
1998
, vol. 
37
 (pg. 
48
-
53
)
68
Frimpong
EH
Lartey
RA
Study of the aetiologic agents of meningitis in Kumasi, Ghana, with special reference to Cryptococcus neoformans
East Afr Med J
1998
, vol. 
75
 (pg. 
516
-
9
)
69
Aseffa
A
Rahlenbeck
S
Alemu
S
Cryptococcosis in AIDS patients in Ethiopia
J Infect
1997
, vol. 
35
 (pg. 
323
-
4
)
70
Silber
E
Sonnenberg
P
Ho
KC
, et al. 
Meningitis in a community with a high prevalence of tuberculosis and HIV infection
J Neurol Sci
1999
, vol. 
162
 (pg. 
20
-
6
)
71
Schutte
CM
Van der Meyden
CH
Magazi
DS
The impact of HIV on meningitis as seen at a South African Academic Hospital (1994 to 1998)
Infection
2000
, vol. 
28
 (pg. 
3
-
7
)
72
Perriens
JH
Mussa
M
Luabeya
MK
, et al. 
Neurological complications of HIV-1-seropositive internal medicine inpatients in Kinshasa, Zaire
J Acquir Immune Defic Syndr
1992
, vol. 
5
 (pg. 
333
-
40
)
73
Heyderman
RS
Gangaidzo
IT
Hakim
JG
, et al. 
Cryptococcal meningitis in human immunodeficiency virus-infected patients in Harare, Zimbabwe
Clin Infect Dis
1998
, vol. 
26
 (pg. 
284
-
9
)
74
Okongo
M
Morgan
D
Mayanja
B
Ross
A
Whitworth
J
Causes of death in a rural, population-based human immunodeficiency virus type 1 (HIV-1) natural history cohort in Uganda
Int J Epidemiol
1998
, vol. 
27
 (pg. 
698
-
702
)
75
McLeod
DT
Neill
P
Gwanzura
L
, et al. 
Pneumocystis carinii pneumonia in patients with AIDS in Central Africa
Respir Med
1990
, vol. 
84
 (pg. 
225
-
8
)
76
Hargreaves
NJ
Kadzakumanja
O
Phiri
S
, et al. 
What causes smear-negative pulmonary tuberculosis in Malawi, an area of high HIV seroprevalence?
Int J Tuberc Lung Dis
2001
, vol. 
5
 (pg. 
113
-
22
)
77
Machiels
G
Urban
MI
Pneumocystis carinii as a cause of pneumonia in HIV-infected patients in Lusaka, Zambia
Trans R Soc Trop Med Hyg
1992
, vol. 
86
 (pg. 
399
-
400
)
78
Carme
B
Mboussa
J
Andzin
M
Mbouni
E
Mpele
P
Datry
A
Pneumocystis carinii is rare in AIDS in Central Africa
Trans R Soc Trop Med Hyg
1991
, vol. 
85
 pg. 
80
 
79
Mahomed
AG
Murray
J
Klempman
S
, et al. 
Pneumocystis carinii pneumonia in HIV infected patients from South Africa
East Afr Med J
1999
, vol. 
76
 (pg. 
80
-
4
)
80
Malin
AS
Gwanzura
LK
Klein
S
Robertson
VJ
Musvaire
P
Mason
PR
Pneumocystis carinii pneumonia in Zimbabwe
Lancet
1995
, vol. 
346
 (pg. 
1258
-
61
)
81
Skalsky
J
Ndumbe
PM
Characteristics of HIV/AIDS patients attending a rural hospital in Cameroon. Manyemen HIV/AIDS Team
Ann Soc Belg Med Trop
1993
, vol. 
73
 (pg. 
209
-
16
)
82
Hodgson
TA
HIV-associated oral lesions: prevalence in Zambia
Oral Dis
1997
, vol. 
3
 
(Suppl 1)
(pg. 
46
-
50
)
83
Ndour
M
Sow
PS
Coll-Seck
AM
, et al. 
AIDS caused by HIV1 and HIV2 infection: are there clinical differences? Results of AIDS surveillance 1986–97 at Fann Hospital in Dakar, Senegal
Trop Med Int Health
2000
, vol. 
5
 (pg. 
687
-
91
)
84
Muller
O
Moser
R
The clinical and parasitological presentation of Plasmodium falciparum malaria in Uganda is unaffected by HIV-1 infection
Trans R Soc Trop Med Hyg
1990
, vol. 
84
 (pg. 
336
-
8
)
85
Nwanyanwu
OC
Kumwenda
N
Kazembe
PN
, et al. 
Malaria and human immunodeficiency virus infection among male employees of a sugar estate in Malawi
Trans R Soc Trop Med Hyg
1997
, vol. 
91
 (pg. 
567
-
9
)
86
Allen
S
Van de Perre
P
Serufilira
A
, et al. 
Human immunodeficiency virus and malaria in a representative sample of childbearing women in Kigali, Rwanda
J Infect Dis
1991
, vol. 
164
 (pg. 
67
-
71
)
87
Verhoeff
FH
Brabin
BJ
Hart
CA
Chimsuku
L
Kazembe
P
Broadhead
RL
Increased prevalence of malaria in HIV-infected pregnant women and its implications for malaria control
Trop Med Int Health
1999
, vol. 
4
 (pg. 
5
-
12
)
88
Steketee
RW
Wirima
JJ
Bloland
PB
, et al. 
Impairment of a pregnant woman's acquired ability to limit Plasmodium falciparum by infection with human immunodeficiency virus type-1
Am J Trop Med Hyg
1996
, vol. 
55
 (pg. 
42
-
9
)
89
Cegielski
JP
Ortega
YR
McKee
S
, et al. 
Cryptosporidium, Enterocytozoon, and Cyclospora infections in pediatric and adult patients with diarrhea in Tanzania
Clin Infect Dis
1999
, vol. 
28
 (pg. 
314
-
21
)
90
Gumbo
T
Sarbah
S
Gangaidzo
IT
, et al. 
Intestinal parasites in patients with diarrhea and human immunodeficiency virus infection in Zimbabwe
AIDS
1999
, vol. 
13
 (pg. 
819
-
21
)
91
Kelly
P
Baboo
KS
Wolff
M
Ngwenya
B
Luo
N
Farthing
MJ
The prevalence and aetiology of persistent diarrhoea in adults in urban Zambia
Acta Trop
1996
, vol. 
61
 (pg. 
183
-
90
)
92
Conlon
CP
Pinching
AJ
Perera
CU
Moody
A
Luo
NP
Lucas
SB
HIV-related enteropathy in Zambia: a clinical, microbiological, and histological study
Am J Trop Med Hyg
1990
, vol. 
42
 (pg. 
83
-
8
)
93
Gomez Morales
MA
Atzori
C
Ludovisi
A
Rossi
P
Scaglia
M
Pozio
E
Opportunistic and non-opportunistic parasites in HIV-positive and negative patients with diarrhoea in Tanzania
Trop Med Parasitol
1995
, vol. 
46
 (pg. 
109
-
14
)
94
Atzori
C
Bruno
A
Chichino
G
, et al. 
HIV-1 and parasitic infections in rural Tanzania
Ann Trop Med Parasitol
1993
, vol. 
87
 (pg. 
585
-
93
)
95
Ravera
M
Reggiori
A
Cocozza
E
Prevalence of Cryptosporidium parvum in AIDS and immunocompetent patients in Uganda
Int J STD AIDS
1994
, vol. 
5
 (pg. 
302
-
3
)
96
Mengesha
B
Cryptosporidiosis among medical patients with the acquired immunodeficiency syndrome in Tikur Anbessa Teaching Hospital, Ethiopia
East Afr Med J
1994
, vol. 
71
 (pg. 
376
-
8
)
97
van Gool
T
Luderhoff
E
Nathoo
KJ
Kiire
CF
Dankert
J
Mason
PR
High prevalence of Enterocytozoon bieneusi infections among HIV-positive individuals with persistent diarrhoea in Harare, Zimbabwe
Trans R Soc Trop Med Hyg
1995
, vol. 
89
 (pg. 
478
-
80
)
98
Edhonu-Elyetu
Y
Significance of herpes zoster in HIV/AIDS in Kweneng district, Botswana
East Afr Med J
1998
, vol. 
75
 (pg. 
379
-
81
)
99
Denhe
K
Dhlakama
D
Richter
C
Mawadza
M
McClean
D
Huss
R
Pattern of HIV-infection in Hurungwe district, Mashonaland West, Zimbabwe
Cent Afr J Med
1992
, vol. 
38
 (pg. 
139
-
43
)
100
Jaffar
S
Ariyoshi
K
Frith
P
, et al. 
Retinal manifestations of HIV-1 and HIV-2 infections among hospital patients in The Gambia, West Africa
Trop Med Int Health
1999
, vol. 
4
 (pg. 
487
-
92
)
101
Lewallen
S
Kumwenda
J
Maher
D
Harries
AD
Retinal findings in Malawian patients with AIDS
Br J Ophthalmol
1994
, vol. 
78
 (pg. 
757
-
9
)
102
Godfrey-Faussett
P
Tuberculosis preventive therapy in people living with HIV in sub-Saharan Africa
AIDS
1999
, vol. 
13
 (pg. 
1581
-
2
)
103
Bucher
HC
Griffith
LE
Guyatt
GH
, et al. 
Isoniazid prophylaxis for tuberculosis in HIV infection: a meta-analysis of randomized controlled trials
AIDS
1999
, vol. 
13
 (pg. 
501
-
7
)
104
Anglaret
X
Sylla-Koko
F
Bonard
D
, et al. 
Susceptibilities to co-trimoxazole of pathogens isolated from blood and stool specimens in Abidjan, Ivory Coast, 1994 to 1996
J Clin Microbiol
1997
, vol. 
35
 pg. 
1915
 
105
Kariuki
S
Gilks
C
Corkill
J
, et al. 
Multi-drug resistant non-typhi salmonellae in Kenya
J Antimicrob Chemother
1996
, vol. 
38
 (pg. 
425
-
34
)
106
Sow
AI
Faye Niang
MA
Dieng
M
, et al. 
Sensitivity to cotrimoxazole of bacteria isolated at the Central University Hospital of Fann, Dakar
Dakar Med
1999
, vol. 
44
 (pg. 
20
-
4
)
107
Boeree
MJ
Harries
AD
Zijlstra
EE
Taylor
TE
Molyneux
ME
Co-trimoxazole in HIV-1 infection
Lancet
1999
, vol. 
354
 (pg. 
334
-
[discussion on 335]
)
108
Feldman
C
Glatthaar
M
Morar
R
, et al. 
Bacteremic pneumococcal pneumonia in HIV-seropositive and HIV-seronegative adults
Chest
1999
, vol. 
116
 (pg. 
107
-
14
)
109
Karstaedt
AS
Khoosal
M
Crewe-Brown
HH
Pneumococcal bacteremia in adults in Soweto, South Africa, during the course of a decade
Clin Infect Dis
2001
, vol. 
33
 (pg. 
610
-
4
)
110
Anglaret
X
Trimethoprim-sulfamethoxazole prophylaxis in sub-Saharan Africa
Lancet
2001
, vol. 
358
 (pg. 
1027
-
8
)

Financial support: National Institute of Allergy and Infectious Disease (grants R01 AI42006, K23 AI01794, K25 AI50436, and CFAR 1P30AI42851) and Centers for Disease Control and Prevention (grant CCU/U64 119525).

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