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Decentralization of HIV care in Cameroon: Increased access to antiretroviral treatment and associated persistent barriers
Health Policy 92 (2009) 165–173
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Decentralization of HIV care in Cameroon: Increased access to antiretroviral treatment and associated persistent barriers Sandrine Loubiere a,b,c,∗ , Sylvie Boyer a,b,c , Camélia Protopopescu a,b,c , Cécile Renée Bonono d , Séverin-Cécile Abega d , Bruno Spire a,b,c , Jean-Paul Moatti a,b,c a b c d
INSERM, U912 (SE4S), Marseille, France Université Aix Marseille, IRD, UMR-S912, Marseille, France ORS PACA, Observatoire Régional de la Santé Provence Alpes Côte d’Azur, Marseille, France Socio-anthropological Research Institute (IRSA) - Catholic University of Central African States, Yaoundé, Cameroon
a r t i c l e
i n f o
Keywords: HIV/AIDS Decentralization Cameroon Antiretroviral treatment Health services
a b s t r a c t Context: The national antiretroviral treatment (ART) program in Cameroon has reached one of the highest rate of coverage in Western and Central Africa (58% of the estimated eligible HIV-infected population in June 2008). Objectives: To assess the extent to which decentralized delivery of HIV care at the district level has contributed to increased access to ART. Methods: Comparison of ART-treated and non-ART-treated in the sub-sample of medically eligible HIV-positive patients (n = 2566) in the cross-sectional ANRS-EVAL survey was carried out among patients seeking HIV care in 14 hospitals at central level (Yaoundé, Douala and capitals of 8 provinces) and 13 at district levels. Logistic regressions and multivariate analysis were carried out to identify factors related to non-access to ART at both levels of care. Results: Only 7% of eligible patients did not have access to ART. After adjustment for time since initial HIV diagnosis and CD4 counts (at initiation of treatment for those ART-treated and at time of survey for those who were not), younger and male patients, as well as those who only had a primary level education were less likely to be ART-treated at central but not at district level, whereas those who were unemployed were less likely to be treated at both levels. Patients were less likely to be treated in central hospitals with higher workload per medical staff member and absence of task shifting policy, and in district hospitals with non-availability of equipment for CD4 counts and larger size (150 beds or more). Conclusion: Main persisting barriers in access to ART in Cameroon are rather due to insufficient access to HIV testing and difficulties in patients’ referral to ART delivery centers after HIV diagnosis, since the overwhelming majority of eligible patients already seeking HIV care had effective access. However, health systems strengthening (HSS) is still needed to overcome some remaining barriers in access to ART and to guarantee its long-term sustainability. © 2009 Elsevier Ireland Ltd. All rights reserved.
∗ Corresponding author at: INSERM, U912 (SE4S), 23, rue Stanislas Torrents, 13006 Marseille, France. Tel.: +33 04 96 10 28 83; fax: +33 04 96 10 28 99. E-mail address: [email protected] (S. Loubiere). 0168-8510/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.healthpol.2009.03.006
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1. Introduction The scaling-up of antiretroviral treatment (ART) in lowresource settings has dramatically reduced mortality and morbidity for people living with HIV/AIDS (PLWHA). The feasibility of delivering ART throughout the public sector in low-resource settings has already been demonstrated [1]. Thanks to the financial support of bilateral and multilateral donors, such as the Global Fund against AIDS, Tuberculosis and Malaria (GFATM) and the US presidential initiative (PEPFAR), as well as promoting increased political involvement, a growing number of African countries have improved access to ART for PLWHA using programs based on either price reduction of antiretroviral drugs (ARVs) through public subsidies or drug provision which is free of charge [2–5]. In Cameroon, a key feature of the national ART program, initiated in 2001, has been to use the pre-existing decentralized framework that characterizes the public healthcare system and to follow the public health approach recommended by WHO since 2003 for scaling-up ART in low-resource settings [6]. As early as 1992, the healthcare system in Cameroon was reorganized on the basis of 174 district hospitals, whose individual size comprises between 100 and 200 beds with a minimum of one physician on the permanent staff. These district hospitals play a reference role for primary healthcare centers at a more local level. Larger hospitals (200 beds or more) located in the capital cities of the country’s 10 provinces as well as the 8 national hospitals in the two main cities of Yaoundé and Douala are in charge of supervising the district hospitals [7]. As of June 2008, ART delivery was based in 24 Accredited Treatment Centers (ATCs) located in the main hospitals of Douala (Littoral province) and Yaoundé (Center province) and in each of the capital cities of the 8 other provinces. These ATCs serve as mentors and reference centers for 108 HIV management units (MUs) at district level. Overall, ART delivery facilities were available in 106 out of the 174 district hospitals. This decentralized approach has contributed to the rapid diffusion of access to ART in Cameroon. According to national estimates [8], 58% of the total number of people medically eligible to receive ART in accordance with WHO guidelines (91,000 adults and 10,000 children) had access to it in 2008. This is one of the highest ART coverage rates in Western and Central Africa [9]. However this shows that a significant portion of PLWHA (42%) is still in urgent need of access to treatment, as later initiation of ART has been associated with higher mortality [10–12]. Certain barriers to accessing ART may be related to factors preventing PLWHA being aware of their serostatus [13], or seeking care after HIV diagnosis [14–16]. Additional barriers related to differences in healthcare infrastructure, healthcare providers’ experience and patients’ characteristics, may also negatively affect prompt access to ART among PLWHA already seeking HIV care [17]. The Universities of Yaoundé/French Agency for AIDS Research (ANRS) Eval study is a cross-sectional survey providing an in-depth evaluation of the Cameroonian ART program [18,19]. It gave us the opportunity both to assess the extent to which decentralized HIV care at the district level has contributed to increased access to ART and to iden-
tify persistent barriers to access to ART for eligible PLWHA seeking care at both the central and district levels.
2. Materials and methods 2.1. Data collection The cross-sectional EVAL survey (ANRS12-116) was carried out between September 2006 and March 2007 using a random sample of patients meeting the following three criteria: diagnosed HIV-positive for at least 3 months, aged over 21 and attending HIV services in any one of the 8 national ATCs in Douala and Yaoundé, 6 ATCs located in provinces (Center, Littoral, West, South-West, NorthWest and Far-North) or 13 district hospitals (MUs). In each facility, healthcare workers randomly selected survey participants among eligible patients and refusals to participate were recorded. Patients who accepted to participate had to fill in a written informed consent form. At the end of their consultation they were referred to a trained interviewer who administered a face-to-face questionnaire independently from medical staff. All interviews were conducted in French or English depending on the geographical area. When necessary, interviews were also conducted in local languages by a trained team member. The questionnaire covered the following topics: sociodemographic and economic characteristics of respondents and their households, disease history, perception of treatments and medical follow-up, adherence to ART, detailed healthcare expenditures for the previous month, perception of health status and quality of life, and finally social relationships. After the interviews, blood samples were collected at the hospital laboratory in order to assess patients’ CD4 count at the time of the survey. Clinical data from both clinical examination of patients and retrospective medical files were collected by care providers using medical questionnaires. ART eligibility at the time of the survey was defined using the following criteria: diagnosed HIV-positive for at least 3 months, having AIDS status (using stage C of WHO clinical scale) or a CD4+ T-cell count lower than 200 cells/mm3 . In addition, because of continued uncertainty regarding the optimal guidelines for ART initiation for patients coinfected with tuberculosis (TB) [20–22], those who were actively being treated for TB at the time of the survey were excluded from the present analysis. In addition, data about the characteristics of the 27 healthcare facilities participating in the survey were obtained by each of the survey supervisors, through interviews with hospital managers and nursing staff as well as by performing cross-validation with data included in the administrative reports sent to the National AIDS Control Committee (NACC). Healthcare facility characteristics included the following: legal status, number of hospital beds, availability of equipment and laboratory tests, human resources in charge of PLWHA, number of PLWHA in the clientele and number of ART-treated patients. The existence (or not) of a “task shifting” policy in the facility [23], that is to say the formal delegation of some consultations for HIV care from physicians to nursing staff, was also recorded.
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2.2. Statistical analysis Data entry was performed using MS Access 2007 and analysis with SPSS for Windows version 15.0 (SPSS system). Comparisons between different facilities’ characteristics, between ART and non-ART-treated eligible patients, and between ART-treated patients in ATCs and those in MUs, were performed using Chi-square or Fisher tests for categorical variables and Student’s t-test or Kruskal–Wallis non-parametric test for continuous variables (depending on whether or not they were normally distributed). All p-values quoted here are two sided, with a p-value < 0.05 considered as significant. For the sub-samples of eligible patients at both the central and district levels, multivariate analysis using stepwise logistic regression models was used to identify factors associated with not being ART-treated. The following characteristics, whether belonging to the individual patient or the healthcare facility, were included in the multivariate analysis: CD4+ T-cell count at the time of the patient’s first visit to the facility, age, gender, educational level and time since initial HIV diagnosis as well as all other significant variables at the threshold level p < 0.2. Final models were obtained by backward stepwise selection procedures. 3. Results As shown in Table 1, the total workload (number of new ART initiations per month and ART-treated patients followed-up in the facility) was significantly lower at the district MUs level than in ATCs, as was the workload per
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member of medical staff. Not surprisingly, the availability of laboratory equipment was more limited and task shifting from physicians to nursing staff was more common at district level. Among the 3488 patients approached, 3170 (91%) agreed to participate in the survey, and 99% of those filled out the questionnaire. This led to a total sample of 3151 respondents (global response rate = 90%). Among respondents, 4.3% (136) were being treated for TB and 14.2% (449) had clinical and immunological characteristics that did not make them eligible for ART. Among the 2566 patients eligible for ART, only a minority of 7.0% (180) had not initiated ART at the time of the survey. Information about sociodemographic and clinical characteristics of patients eligible for ART is summarized in Table 2. The majority of this sample were women (71.3%), and had at least secondary level education (55.0%) with a median age of 36.7 years. Most of the patients (70%) were employed with a regular source of income at the time of the study with occupational breakdown as follows: selfemployed or craftsmen (32%), company employee (28%) and subsistence farmers (23%). The median monthly household income was however quite low, circa CFA F 40,000 (EUR 60.4) given that the threshold for the absolute poverty line in Cameroon is CFA F 20,000 (EUR 30.2) (circa US$ 40) [24,25]. About one-third (30.6%) of the sample was receiving care at district level in MUs. ART-treated patients had a lower socio-economic status at district level than those being treated in ATCs: 61.3% had only primary school education in district hospitals vs. 37.0% in ATCs; median household income was CFA F
Table 1 Comparison of characteristics of HIV services (n = 27) according to the level of decentralization of healthcare supply in Cameroon (EVAL survey, ANRS 12-116). Variables HIV Services No. of HIV services or median [IQR] Sector Public Private (for pofit) Private (faith based) No. of hospital beds Laboratory equipment (score ranging from 0 to 10)b Availability of CD4 cell counter (yes) Healthcare staff or HIV care f(nb. of full-time equivalent) Total healthcare staff Physicians Nursing staff Social workers Non-qualified staff No. of ART-treated patients No. of new ART-treated patients per month No. of ART-treated patients per physician No. of ART-treated patients per physician and nurse Task shifting from physicians to nursing staff No Yes
Total (n = 27)
20 2 5 151 [94; 240] 8.0 [7.0; 9.0] 20 14 [10; 18] 3 [2; 4] 5 [3; 6] 3 [2; 4] 3 [1; 4] 540 [225; 976] 31 [15; 51] 214 [65; 410] 72 [32; 144] 6 21
ATCs Central and Provincial (n = 14)
12 2 0 198 [90; 300] 9.0 [8.7; 9.0] 13 18 [13; 19] 4 [2; 5] 5 [3; 6] 4 [2; 6] 4 [1; 5] 920 [524; 1701] 47 [31; 77] 305 [148; 643] 137 [67; 198] 5 9
District MUs (n = 13)
8 0 5 120 [93; 166] 7.0 [4.5; 8.0] 7 12 [9; 15] 3 [2; 3] 4 [3; 6] 2 [1; 3] 2 [1; 4] 225 [101; 537] 15 [10; 28] 75 [43; 221] 32 [18; 73] 1 12
p-Valuea
0.01
0.168 0.08 0.021 0.033 0.081 0.89 0.031 0.203 0.019 0.009 0.035 0.015 0.08
IQR = interquartile range. a Chi-square test and Fisher’s exact test for categorical variables, and Kruskal–Wallis test for continuous variables. b Technical equipment level was assessed by the availability of performing the 10 following laboratory tests on site: complete cell blood count, CD4 cell count, transaminases, glycemia, creatinemia, amylasemia, pregnancy test, viral load, triglycerides and cholesterol.
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Table 2 Comparison of ART and non-ART-treated patients among a sample of HIV-infected patients eligible for treatment in Cameroon (n = 2566). p-Valuea (2) vs. (3)
(1) Total n = 2566
(2) ART-treated n = 2386 (93%)
(3) Non-ART-treated n = 180 (7%)
Age: median (IQR)
36.7 (31.4; 40.0)
36.8 (31.4; 44.4)
34.8 (29.0; 42.0)
0.007
Gender Female Male
1,830 (71.3) 736 (28.7)
1,705 (71.5) 681 (28.5)
125 (69.4) 55 (30.6)
0.56
Secondary or higher education level Yes No
1,427 (55.6) 1,139 (44.4)
1,059 (44.4) 1,327 (55.6)
80 (44.4) 100 (55.6)
0.98
Marital status Single or divorced Married Living in couple but not married
1,383 (53.9) 918 (35.8) 265 (10.3)
1,294 (54.2) 863 (36.2) 229 (9.6)
89 (49.4) 55 (30.6) 36 (20.0)
<0.0001
Employed Yes No
1,797 (70.0) 769 (30.0)
1,693 (71.0) 693 (29.0)
104 (57.8) 76 (42.2)
<0.0001
40,000 (20,000; 74,000) 7,000 (3,700; 11,000)
40,000 (20,200; 73,600) 7,000 (3,800; 11,000)
36,500 (20,000; 75,000) 5,600 (1,600; 17,800)
0.38 0.001
17 (8; 38)
17 (8; 37)
11 (3; 53)
0.09
329 (199; 433) 22 (12; 40)
343 (218; 447) 23 (12; 41)
127 (45; 228) 14 (6; 27)
<0.0001 <0.0001
Time between initial HIV diagnosis and first consultation for HIV care ≤1 month 1,457 (56.8) >1 month 1,109 (43.2)
1,378 (57.8) 1,008 (42.2)
79 (43.9) 101 (56.1)
<0.0001
Obtained initial HIV diagnosis in the same hospital than current follow-up Yes No 1,400 (54.6) 1,166 (45.4)
1,331 (55.8) 1,055 (44.2)
69 (38.3) 111 (61.7)
<0.0001
Declares that “making an appointment with the hospital physician is” Very or quite difficult 559 (21.8) Very or quite easy 2,007 (78.2)
507 (21.2) 1,879 (78.8)
52 (28.9) 128 (71.1)
0.017
Consulted a traditional healer in the prior 6 months Yes No
239 (9.3) 2,327 (90.7)
212 (8.9) 2,174 (91.1)
27 (15.0) 153 (85.0)
0.006
170 (120; 300) 82 (48; 181)
170 (120; 300) 82 (53; 181)
213 (110; 300) 112 (38; 187)
<0.0001 0.074
577 (22.5) 1,989 (77.5)
517 (21.7) 1,869 (78.3)
60 (33.3) 120 (66.7)
<0.0001
CD4 count facility at hospitalb Yes No
2,236 (87.1) 330 (12.9)
2,092 (87.7) 294 (12.3)
144 (80.0) 36 (20.0)
0.003
Structure providing careb ATCs District MUs
1,780 (69.4) 786 (30.6)
1,663 (69.7) 723 (30.3)
117 (65.0) 63 (35.0)
0.18
Household monthly income (CFAF): median (IQR) Monthly out-of-pocket expenditures (CFAF): median (IQR) % of health expenditures in household income median (IQR) CD4+ T-cell counts (cells/mm3 ): median (IQR) Time since HIV diagnosis (months): median (IQR)
No. of hospital bedsb : median (IQR) No. of HIV+ patients per medical staffb : median (IQR) Task shifting from physician to nursesb No Yes
a b
p-Value for the Pearson’s 2 for categorical row variables (and ANOVA t- or Kruskal–Wallis test for continuous variables). Characteristics of the facilities in which patients were followed.
30,000 (IQR: 15,800; 50,000) in district hospitals vs. CFA F 46,500 (IQR: 25,000; 82,600) in ATCs. Monthly out-ofpocket payments for HIV care and ART were significantly lower at the district level (median 5400 [3600; 8500] vs. 7500 [4000; 12,000], respectively; p < 0.0001). However, because household income was significantly lower at district level, the proportion of income devoted to HIV care was similar among ART-treated patients in district MUs and those in ATCs (17% vs. 18%, respectively; p = 0.836). More-
over, delays between HIV diagnosis and first consultation after diagnosis were significantly shorter at district level than for ATCs (62.4% vs. 55.7% with a delay of less than 1 month; p = 0.003). CD4 counts at ART initiation were significantly higher for patients being treated at district level (mean = 146 vs. 130 cell/mm3 ; p < 0.0001). Table 2 shows that among all the patients eligible for treatment at time of the survey, quite logically, ARTtreated patients had significantly higher CD4 cell counts
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than their non-ART-treated counterparts. However, these latter had been HIV diagnosed for a shorter period of time (Table 2) and their CD4 counts (median = 127; IQR: 45–228) were significantly higher when compared with those evaluated for the ART-treated patients when they first started treatment (median = 125; IQR: 67–180) (p < 0.0001). Whereas the gender distribution was similar in both the ART and non-ART-treated groups, Table 2 shows that nonART-treated patients tended to be younger and of lower socio-income status (i.e. lower household income and lower rate of employment). They were also more likely to be living in a couple but not married to their partner. NonART-treated patients also seemed to face more difficulties in their relationship with the healthcare delivery system. A higher proportion among non-ART-treated patients than their ART-treated counterparts were being followed in a facility different from the one where they obtained their initial HIV diagnosis. Moreover, they had waited for more
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than 1 month before seeking HIV care after their diagnosis, expressed having more difficulties when trying to make an appointment to consult with medical staff of the healthcare facility and were also more likely to consult traditional healers. Table 2 shows that non-ART-treated patients devoted a lower share of their income to out-ofpocket healthcare expenditures, although this difference did not reach statistical significance. Detailed analysis of out-of-pocket healthcare expenditures however reveals that once ARV drugs were excluded from the calculation, non-ART-treated patients tended to spend significantly more on all components of HIV care (median = CFA F 5600 vs. 2500, respectively; p < 0.0001). Transportation costs to HIV care centers were similar however among ART and non-ART-treated patients (median = CFA F 1000 vs. 800, respectively; p = 0.23). In addition, Table 2 shows that overall, the proportion of non-ART-treated patients among all those eligible for
Table 3 Factors associated with non-being ART-treated in a sample of HIV-infected patients eligible for treatment according to level of HIV care delivery (multivariate logistic regression analyses) (n = 2566) (EVAL survey, ANRS 12-116). ATCs
p
District MUs
Odds ratio [95% CI]
p
Odds ratio [95% CI]
Age
0.96 [0.94; 0.98]
0.001
1.01 [0.97; 1.03]a
0.951
Gender Female Male
1 1.74 [1.10; 2.79]
0.020
1a 1.02 [0.51; 2.02]
0.959
Secondary or higher education level Yes No
1 2.11 [1.37; 3.23]
0.001
1* 0.67 [0.38; 1.20]
0.183
Marital status Single or divorced Married Living in couple but not married
NS
Employment Yes No
1 1.68 [1.12; 2.52]
% of health expenditures in household income CD4+ T-cell countsb Time since initial HIV diagnosis
NS 1.004 [1.002; 1.006] 0.98 [0.97; 0.99]
1 0.84 [0.44; 1.60] 2.82 [1.08; 7.35] 0.014
<0.001 <0.001
Time between initial HIV diagnosis and first consultation for HIV care <1 month NS >1 month Obtained initial HIV diagnosis in the hospital of current follow-up Yes 1 No 2.60 [1.70; 4.02]
<0.001
1 1.80 [1.07; 3.30]
0.05
1.005 [1.002; 1.007] 1.001 [0.97; 1.03]a 0.96 [0.94; 0.98]
0.003 0.526 0.001
1 2.70 [1.53; 4.77]
0.001
NS
Patients treated in an hospital with no. of hospital beds: <150 >150
NS
No. of HIV+ patients per medical staff
1.008 [1.005; 1.011]
<0.001
–a
Task shifting from physician to nurses None or little Quite a lot or a lot
3.41 [2.17; 5.36] 1
<0.001
–a
CD4 count facility at hospital Yes No
1 2.51 [1.30; 4.87]
NS
95% CI: confidence interval, p = 0.95. a This variable was forced in the final model. b At the time of ART initiation vs. at the time of the survey for ART eligible but untreated patients.
0.600 0.034
1 2.79 [1.48; 5.25]
0.006
0.001
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treatment did not significantly differ between district and ATCs levels, but that it was significantly higher in healthcare facilities where equipment for performing CD4 counts was not available (i.e. mostly in district MUs, see Table 1). The proportion of non-ART-treated patients was also significantly higher in larger facilities, as well as in facilities where the workload per medical staff member was higher and those where no task shifting policy existed. These latter two characteristics were more frequent in ATCs (see Table 1). After adjustment for both time since initial HIV diagnosis and CD4 counts (at initiation of treatment for those ART-treated and at the time of survey for those who were not), the socio-economic factors associated with a lack of access to ART in the multiple regression models differed depending on the level of care (see Table 3). The only exception to this was being unemployed. Younger and male patients, as well as those who only had a primary educational level were less likely to be ART-treated in ATCs. However, these factors were not associated with nonART-treated patients followed at district level. The only socio-economic characteristic which appeared to be associated with a lack of access to ART in MUs, but not in ATCs, was the fact of living in a couple without being married. Specific healthcare behaviors, such as a longer delay between HIV diagnosis and first medical consultation for HIV care, as well as a higher proportion of income being devoted to health expenditures were associated with a lack of access to ART in MUs but not in ATCs. On the other hand, patients who had changed HIV care center after their HIV diagnosis were less likely to be treated with ART when they sought care in ATCs. Characteristics of facilities which seemed to play a negative role in access to ART were also different at central and district levels. Not surprisingly, for patients followed-up in district MUs, the lack of availability of equipment for CD4 counts was associated with a lower likelihood of getting access to ART. Access to ART was also lower in MUs located in the larger district hospitals (150 hospital beds or more). On the contrary, the size of the hospital did not seem to influence access to ART in ATCs. Among patients followed in ATCs, a higher workload for medical staff members and the absence of task shifting were significantly associated with lower access to ART. 4. Discussion The EVAL survey was representative of PLWHA seeking HIV care in six of the ten provinces of Cameroon at the end of 2006-beginning of 2007. Survey results confirm a remarkable achievement for the national ART program in Cameroon, since the overwhelming majority (93%) of eligible patients had effective access to this life-saving therapy. The minority (7%) of non-ART-treated eligible patients tended to have been diagnosed for HIV later than those already on ART. They also tended to have had higher CD4 counts at the time of the survey when compared with those of their ART-treated counterparts taken at the time of ART initiation. These two points suggest that one can be quite optimistic that these patients will ultimately obtain access to ART. In contrast with results from studies conducted in
other low-resource settings [25,26], transportation costs and difficulties in making appointments with physicians were not found to be associated with delays in initiating ART in multivariate analysis. These positive achievements have clearly been facilitated by the scaling-up of access to ART, not only in the main cities of the country but also at the decentralized district level. Considering the epidemiological situation of Cameroon where individuals with a greater level of education are more likely to be HIV-infected [28], results also show that the decentralization of ART delivery has increased access for PLWHA from the lower socio-economic groups who are likely to be hit harder by the downstream impacts of AIDS [29]. Since it is estimated that 42% of the total number of PLWHA in urgent need of ART were not yet provided for as of June 2008, the EVAL survey suggests that the main persisting barriers to access ART in Cameroon concern insufficient access to HIV testing [13], difficulties in patients’ referral from HIV counseling and testing to ART delivery centers [30,31], and delays between HIV diagnosis and access to HIV care [14,15]. Some limitations of the EVAL survey should be acknowledged as they may have led to some underestimation of the difficulties encountered in the process of ART delivery at national level. Indeed, three of the four provinces not included in the survey (Adamoua, South and East) have the lowest estimated rates of ART coverage (<40%). Patients with active TB treatment at the time of the survey were also excluded from the present analysis, while difficulties in optimal management of HIV care for coinfected patients could have increased delays in access to ART [32]. In Cameroon, the management of TB in the context of ART is based on the Directly Observed Treatment, Short-Course (DOTS) program and anti-TB drugs are available free of charge at the point of care delivery. Treatment guidelines consist in initiating ART 2 months after initiating anti-TB treatment. However, difficulties in the supply of anti-TB drugs combined with a lack of adherence to antiTB treatment often increase the delay in initiating HAART in co-infected patients [21,22]. In addition, several studies have shown that treating TB patients who are also HIV-positive may be less cost-effective than treating HIVnegative ones [33,34]. On the other hand, the financial barrier to accessing ART was lowered further in Cameroon after the EVAL survey was completed. In Cameroon, as in many African countries, outof-pocket payments by households at the point of services delivery still provide the main contribution to healthcare financing (circa 70.0% of total health expenditures) [35]. These out-of-pocket expenditures, associated with a loss in income due to HIV-related morbidity, often constitute a major barrier to accessing ART in low-resource settings [27,36]. The continued requirement of user fees in order to access HIV services and medications has been shown to be detrimental to long-term adherence and clinical effectiveness of ART in many African countries including Cameroon [37–40]. At the time of the EVAL survey, ARV drugs were already heavily subsidized in Cameroon thanks to support from international donors, such as the Global Fund to fight AIDS, TB and Malaria, but patients still had to contribute a fraction of the drug costs: monthly out-of-pocket payments amounted to 3000 FCFA, circa 6 US$, for the generic
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Triomune regimen, and 7000 FCFA, circa 14 US$, for other first-line regimens [41]. These costs partly explain not only why patients devoted a significant portion of their household income to healthcare in the EVAL study but also how this payment constituted a barrier to ART access for certain groups of non-ART-treated patients, notably at district level. In May 2007, the national ART program introduced a new policy guaranteeing access to free of charge ARVs to all PLWHA eligible for treatment. This policy has already contributed to increased diffusion of ART (between June 2007 and June 2008, the national rate of ART coverage increased by circa 10%). However, it should be acknowledged that this policy does not suppress all financial barriers as patient out-of-pocket payments are still required for other components of HIV care (laboratory tests, medical consultations, transportation costs, etc.) [42,43]. Indeed, the fact that eligible non-ART-treated patients in the EVAL survey tended to have higher out-of-pocket payments than those treated with ART (excluding ARV drugs payments) suggests that the persistence of financial barriers to accessing ART will not be fully overcome by free of charge ARV drugs. In addition to out-of-pocket costs associated with ART, the EVAL survey has identified a number of factors, either related to patients’ individual characteristics or to bottlenecks within the HIV care delivery system, which persist in delaying access to ART even for PLWHA who are aware of their serostatus and who already have access to HIV care. Although, as already mentioned, these factors do not impede the great majority of medically eligible PLWHA from accessing ART, they still need to be overcome, as scaling-up ART coverage may exacerbate them. The high proportion of women in the EVAL sample could be related to the epidemiological situation in Cameroon: according to national estimates, there is a higher proportion of women than men in the total HIV-infected population and in the population eligible for ART (circa 62%) [44]. In addition, national ART coverage is significantly higher among women (62.5% vs. 51.1% for men). The EVAL survey suggests that this lower rate of coverage among male PLWHA may not only be due to greater reluctance to be HIV tested and to seek care, but could also be related to additional difficulties in accessing ART, particularly in ATCs. Of course, individual characteristics like age, male gender, lower educational level and lower income which were all found to be associated with a lower likelihood of access to ART in eligible patients may to some extent reflect the variability of patients’ preferences in their willingness to access treatment. However, the fact that these factors played a role in ACTs but not in district MUs suggests that male patients, as well as patients with a lower socioeconomic status, are less likely to have their treatment needs adequately recognized in the larger hospitals which have a higher burden of HIV care than in district ones which are in closer proximity to local communities. Conversely, the fact that PLWHA living in non-married couples had less access to ART at district level suggests that they may face specific difficulties due to pressures related to their close social environment, and may possibly be less willing to disclose their serostatus to their local community [2]. Finally, a pressing challenge to achieving universal access to HAART in sub-Saharan Africa is to provide basic
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but efficient HIV care infrastructure [45]. The experience of Cameroon strongly supports the idea that decentralization of ART delivery is a feasible solution to that problem. However, health systems strengthening (HSS) is still needed to overcome some remaining barriers to accessing ART and, more importantly, to guarantee its long-term sustainability. As suggested by the EVAL survey, HSS priorities should be adapted to the practical issues faced at each level of care. Indeed, the increased number of people seeking HIV care in proportion to the lack of highly qualified personnel may impede the ability to start ART-eligible patients on treatment, notably in the larger hospitals based in the main cities [46]. Although the World Health Organization recommends the promotion of task shifting within HIV services delivery in resource limited settings [23], Cameroon does not yet have a defined national task-shifting strategy in the scaling-up of its ART program and initiative on this matter is left to each individual healthcare facility. Standardized guidelines on task shifting may be especially useful in ATCs at central level where both the number of healthcare professionals involved in HIV care and the number of HIVinfected patients is the highest. At district level, there is a need to provide every facility with appropriate laboratory test equipment for diagnosis, treatment initiation and follow-up in order to keep patients in the same location [47]. A complementary alternative would be to promote a more optimal use of simplified algorithms for HIV care and treatment at the more decentralized level: in accordance with the WHO recommendations for scaling-up ART in lowresource settings, national guidelines in Cameroon allow district hospitals without CD4 count machines to initiate ART on the basis of clinical examination and total lymphocyte count [6]. The performance of this WHO “public health” approach is currently being evaluated in a Ministry of Public Health of Cameroon/ANRS randomized trial (STRATALL ANRS 12120) [41]. The cross-sectional design of the EVAL survey did not facilitate an in-depth investigation of time dependent factors in the evaluation of the Cameroonian national ART program. It remains to be seen, through longitudinal data collection, or at least through repetition at other points in time of cross-sectional surveys using a similar methodology to EVAL, the extent to which the significant progress obtained in access to ART in this country will further expand to reach universal coverage and if it will continue in the long term. Conflicts of interest None declared. Acknowledgements We would like to thank the Cameroonian Ministry of Public Health for its support together with the French National Agency for Research on AIDS and Hepatitis (ANRS). We would also like to thank all 27 participating hospitals and their medical teams for their involvement in the survey. Finally, we would like to thank all the patients who accepted to take part in the study.
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Funding: This work was supported by the French National Agency for Research on AIDS and Hepatitis. The authors declare that they have not entered into any agreement with the funding organization which may have limited their ability to complete the research as planned, and state that they have had full control of all primary data.
References [1] Bertozzi S, Gutierrez JP, Opuni M, Walker N, Schwartlander B. Estimating resource needs for HIV/AIDS health care services in low-income and middle-income countries. Health Policy 2004;69: 189–200. [2] Desclaux A, Ciss M, Taverne B, Sow PS, Egrot M, Faye MA, et al. Access to antiretroviral drugs and AIDS management in Senegal. AIDS 2003;17(Suppl. 3):S95–101. [3] Lawn SD, Myer L, Orrell C, Bekker LG, Wood R. Early mortality among adults accessing a community-based antiretroviral service in South Africa: implications for programme design. AIDS 2005;19:2141–8. [4] Susman E. Botswana gears up to treat HIV patients in Africa’s largest program. AIDS 2004;18:N1–2. [5] Katzenstein D, Laga M, Moatti JP. The evaluation of the HIV/AIDS drug access initiatives in Cote d’Ivoire, Senegal and Uganda: how access to antiretroviral treatment can become feasible in Africa. AIDS 2003;17(Suppl. 3):S1–4. [6] Gilks CF, Crowley S, Ekpini R, Gove S, Perriens J, Souteyrand Y, et al. The WHO public-health approach to antiretroviral treatment against HIV in resource-limited settings. Lancet 2006;368:505–10. [7] Gruenais M, editor. Changing a health system: the case of Cameroon. In: Euro-African Association for the Anthropology of Social Change and Development. APAD Report no. 21. Paris; 2002. [8] Ministry of Public Health & National AIDS Control Committee. Towards universal access to care and treatment for adults and children living with HIV/AIDS in Cameroo [in French]. In: Progress Report no. 11. Yaoundé, Cameroon; 2008. [9] UNAIDS. Report on the global AIDS epidemic. In: UNAIDS. Geneva; 2008. [10] Badri M, Bekker LG, Orrell C, Pitt J, Cilliers F, Wood R. Initiating highly active antiretroviral therapy in sub-Saharan Africa: an assessment of the revised World Health Organization scaling-up guidelines. AIDS 2004;18:1159–68. [11] Chadborn TR, Baster K, Delpech VC, Sabin CA, Sinka K, Rice BD, 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;19:513–20. [12] Rosen S, Fox MP, Gill CJ. Patient retention in antiretroviral therapy programs in sub-Saharan Africa: a systematic review. PLoS Medicine 2007;4:e298. [13] De Cock KM, Mbori-Ngacha D, Marum E. Shadow on the continent: public health and HIV/AIDS in Africa in the 21st century. Lancet 2002;360:67–72. [14] Girardi E, Sabin CA, Monforte AD. Late diagnosis of HIV infection: epidemiological features, consequences and strategies to encourage earlier testing. Journal of Acquired Immune Deficiency Syndromes 2007;46(Suppl. 1):S3–8. [15] Person AK, Ramadhani HO, Thielman NM. Antiretroviral treatment strategies in resource-limited settings. Current HIV/AIDS Reports 2007;4:73–9. [16] Marcellin F, Abe C, Loubiere S, Boyer S, Blanche J, Koulla-Shiro S, et al. Delayed first consultation after diagnosis of HIV infection in Cameroon. AIDS; Apr 1. [Epub ahead of print]. [17] Sow PS, Otieno LF, Bissagnene E, Kityo C, Bennink R, Clevenbergh P, et al. Implementation of an antiretroviral access program for HIV1-infected individuals in resource-limited settings: clinical results from 4 African countries. Journal of Acquired Immune Deficiency Syndromes 2007;44:262–7. [18] Boyer S, Marcellin F, Ongolo-Zogo P, Abega S, Nantchouang R, Spire B, et al. Financial difficulties in accessing HIV care in Yaoundé, Cameroon: first results from the national cross-sectional survey EVAL-ANRS 12-116. Bulletin World Health Organization 2009;87:279–87. [19] Marcellin F, Boyer S, Protopopescu C, Carrieri MP, Ongolo-Zogo P, Abega SC, et al. Risk of antiretroviral treatment interruption among people living with HIV in Yaoundé, Cameroon (EVAL survey ANRS 12116): determinants, recommendations and possible interventions. Tropical Medicine and International Health 2008;13:1470–8.
[20] Lawn SD, Myer L, Bekker LG, Wood R. Tuberculosis-associated immune reconstitution disease: incidence, risk factors and impact in an antiretroviral treatment service in South Africa. AIDS 2007;21: 335–41. [21] Lawn SD, Wood R. Impact of antituberculosis treatment on virological response to highly active antiretroviral therapy: implications for resource-limited settings? Journal of Infectious Diseases 2006;194:1467–8, author reply 1468. [22] Wood R. The case for integrating tuberculosis and HIV treatment services in South Africa. Journal of Infectious Diseases 2007;196(Suppl. 3):S497–9. [23] Samb B, Celletti F, Holloway J, Van Damme W, De Cock KM, Dybul M. Rapid expansion of the health workforce in response to the HIV epidemic. New England Journal of Medicine 2007;357:2510–4. [24] Direction de la Statistique et de la Comptabilité Nationale. Enquête à indicateurs multiples, 2000 (MICS 2000) (in French). In: DSCN, Ministère de l’Economie et des Finances. Yaoundé, Cameroun; 2001. [25] Institut National de la Statistique. Deuxième enquête camerounaise auprès des ménages en 2001 (ECAM II 2001)—Conditions de vie des populations et profil de pauvreté au Cameroun en 2001—Rapport principal de l’enquête (in French). In: INS, Ministère de l’Economie et des Finances, République du Cameroun. Yaoundé, Cameroun; 2002. [26] Mukherjee JS, Ivers L, Leandre F, Farmer P, Behforouz H. Antiretroviral therapy in resource-poor settings. Decreasing barriers to access and promoting adherence. Journal of Acquired Immune Deficiency Syndromes 2006;43(Suppl. 1):S123–6. [27] Rosen S, Ketlhapile M, Sanne I, DeSilva MB. Cost to patients of obtaining treatment for HIV/AIDS in South Africa. South African Medicine Journal 2007;97:524–9. [28] Fortson JG. The gradient in sub-Saharan Africa: socioeconomic status and HIV/AIDS. Demography 2008;45:303–22. [29] Barnett T, Whiteside A, Khodakevich L, Kruglov Y, Steshenko V. The HIV/AIDS epidemic in Ukraine: its potential social and economic impact. Social Science and Medicine 2000;51:1387–403. [30] Tantchou Yakam J. New actors in the fight against HIV/AIDS: overlapping and competition between existing structures [in French]. La Medicina Tropical 2008;68:300–5. [31] Tantchou-Yakam J, Gruenais M. Involving new actors to achieve ART scaling up: difficulties in an HIV/AIDS testing and counselling centre in Cameroon. International Nurse Reviews 2009;56:50–7. [32] Ainsworth M, Beyrer C, Soucat A. AIDS and public policy: the lessons and challenges of “success” in Thailand. Health Policy 2003;64:13–37. [33] El-Sony AI. The cost to health services of human immunodeficiency virus (HIV) co-infection among tuberculosis patients in Sudan. Health Policy 2006;75:272–9. [34] Murray CJ, DeJonghe E, Chum HJ, Nyangulu DS, Salomao A, Styblo K. Cost effectiveness of chemotherapy for pulmonary tuberculosis in three sub-Saharan African countries. Lancet 1991;338:1305–8. [35] WHO. Working together for health. In: The World health report 2006. Geneva; 2006. [36] Hardon AP, Akurut D, Comoro C, Ekezie C, Irunde HF, Gerrits T, et al. Hunger, waiting time and transport costs: time to confront challenges to ART adherence in Africa. AIDS Care 2007;19:658–65. [37] Boyer S, Blanche J, Protopopescu C, Bonono CR, Marcellin F, OngoloZogo P, et al. Impact of the structural characteristics of healthcare supply in antiretroviral treatment interruption in Cameroon. In: XVII International AIDS Conference. 2008. [38] Laniece I, Ciss M, Desclaux A, Diop K, Mbodj F, Ndiaye B, et al. Adherence to HAART and its principal determinants in a cohort of Senegalese adults. AIDS 2003;17(Suppl. 3):S103–8. [39] Weiser S, Wolfe W, Bangsberg D, Thior I, Gilbert P, Makhema J, et al. Barriers to antiretroviral adherence for patients living with HIV infection and AIDS in Botswana. Journal of Acquired Immune Deficiency Syndromes 2003;34:281–8. [40] Braitstein P, Brinkhof MW, Dabis F, Schechter M, Boulle A, Miotti P, 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;367:817–24. [41] Koulla-Shiro S, Delaporte E. The public health approach to antiretroviral treatment: the case of Cameroon. In: Coriat B, editor. The political Economy of HIV/AIDS in developing countries (TRIPS, public health systems and free access). UK: Edward Elgar, Cheltenham; 2008. p. 259–71. [42] Bernell SL, Shinogle JA. The relationship between HAART use and employment for HIV-positive individuals: an empirical analysis and policy outlook. Health Policy 2005;71:255–64. [43] Joy R, Druyts EF, Brandson EK, Lima VD, Rustad CA, Zhang W, et al. Impact of Neighborhood-Level Socioeconomic Status on HIV Disease Progression in a Universal Health Care Setting. Journal of Acquired Immune Deficiency Syndromes 2008;47:500–5.
S. Loubiere et al. / Health Policy 92 (2009) 165–173 [44] UNAIDS. Epidemiological fact sheets on HIV/AIDS and sexually transmitted infections. Cameroon 2006 update. Geneva: UNAIDS; 2006. [45] Dunne M. Antiretroviral drug development: the challenge of cost and access. AIDS 2007;21(Suppl. 4):S73–9. [46] Vassall A, Compernolle P. Estimating the resource needs of scalingup HIV/AIDS and tuberculosis interventions in sub-Saharan Africa: a
173
systematic review for national policy makers and planners. Health Policy 2006;79:1–15. [47] Gimbel-Sherr SO, Micek MA, Gimbel-Sherr KH, Koepsell T, Hughes JP, Thomas KK, et al. Using nurses to identify HAART eligible patients in the Republic of Mozambique: results of a time series analysis. Human Resource Health 2007;5:7.
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Health Policy journal homepage: www.elsevier.com/locate/healthpol
Decentralization of HIV care in Cameroon: Increased access to antiretroviral treatment and associated persistent barriers Sandrine Loubiere a,b,c,∗ , Sylvie Boyer a,b,c , Camélia Protopopescu a,b,c , Cécile Renée Bonono d , Séverin-Cécile Abega d , Bruno Spire a,b,c , Jean-Paul Moatti a,b,c a b c d
INSERM, U912 (SE4S), Marseille, France Université Aix Marseille, IRD, UMR-S912, Marseille, France ORS PACA, Observatoire Régional de la Santé Provence Alpes Côte d’Azur, Marseille, France Socio-anthropological Research Institute (IRSA) - Catholic University of Central African States, Yaoundé, Cameroon
a r t i c l e
i n f o
Keywords: HIV/AIDS Decentralization Cameroon Antiretroviral treatment Health services
a b s t r a c t Context: The national antiretroviral treatment (ART) program in Cameroon has reached one of the highest rate of coverage in Western and Central Africa (58% of the estimated eligible HIV-infected population in June 2008). Objectives: To assess the extent to which decentralized delivery of HIV care at the district level has contributed to increased access to ART. Methods: Comparison of ART-treated and non-ART-treated in the sub-sample of medically eligible HIV-positive patients (n = 2566) in the cross-sectional ANRS-EVAL survey was carried out among patients seeking HIV care in 14 hospitals at central level (Yaoundé, Douala and capitals of 8 provinces) and 13 at district levels. Logistic regressions and multivariate analysis were carried out to identify factors related to non-access to ART at both levels of care. Results: Only 7% of eligible patients did not have access to ART. After adjustment for time since initial HIV diagnosis and CD4 counts (at initiation of treatment for those ART-treated and at time of survey for those who were not), younger and male patients, as well as those who only had a primary level education were less likely to be ART-treated at central but not at district level, whereas those who were unemployed were less likely to be treated at both levels. Patients were less likely to be treated in central hospitals with higher workload per medical staff member and absence of task shifting policy, and in district hospitals with non-availability of equipment for CD4 counts and larger size (150 beds or more). Conclusion: Main persisting barriers in access to ART in Cameroon are rather due to insufficient access to HIV testing and difficulties in patients’ referral to ART delivery centers after HIV diagnosis, since the overwhelming majority of eligible patients already seeking HIV care had effective access. However, health systems strengthening (HSS) is still needed to overcome some remaining barriers in access to ART and to guarantee its long-term sustainability. © 2009 Elsevier Ireland Ltd. All rights reserved.
∗ Corresponding author at: INSERM, U912 (SE4S), 23, rue Stanislas Torrents, 13006 Marseille, France. Tel.: +33 04 96 10 28 83; fax: +33 04 96 10 28 99. E-mail address: [email protected] (S. Loubiere). 0168-8510/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.healthpol.2009.03.006
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1. Introduction The scaling-up of antiretroviral treatment (ART) in lowresource settings has dramatically reduced mortality and morbidity for people living with HIV/AIDS (PLWHA). The feasibility of delivering ART throughout the public sector in low-resource settings has already been demonstrated [1]. Thanks to the financial support of bilateral and multilateral donors, such as the Global Fund against AIDS, Tuberculosis and Malaria (GFATM) and the US presidential initiative (PEPFAR), as well as promoting increased political involvement, a growing number of African countries have improved access to ART for PLWHA using programs based on either price reduction of antiretroviral drugs (ARVs) through public subsidies or drug provision which is free of charge [2–5]. In Cameroon, a key feature of the national ART program, initiated in 2001, has been to use the pre-existing decentralized framework that characterizes the public healthcare system and to follow the public health approach recommended by WHO since 2003 for scaling-up ART in low-resource settings [6]. As early as 1992, the healthcare system in Cameroon was reorganized on the basis of 174 district hospitals, whose individual size comprises between 100 and 200 beds with a minimum of one physician on the permanent staff. These district hospitals play a reference role for primary healthcare centers at a more local level. Larger hospitals (200 beds or more) located in the capital cities of the country’s 10 provinces as well as the 8 national hospitals in the two main cities of Yaoundé and Douala are in charge of supervising the district hospitals [7]. As of June 2008, ART delivery was based in 24 Accredited Treatment Centers (ATCs) located in the main hospitals of Douala (Littoral province) and Yaoundé (Center province) and in each of the capital cities of the 8 other provinces. These ATCs serve as mentors and reference centers for 108 HIV management units (MUs) at district level. Overall, ART delivery facilities were available in 106 out of the 174 district hospitals. This decentralized approach has contributed to the rapid diffusion of access to ART in Cameroon. According to national estimates [8], 58% of the total number of people medically eligible to receive ART in accordance with WHO guidelines (91,000 adults and 10,000 children) had access to it in 2008. This is one of the highest ART coverage rates in Western and Central Africa [9]. However this shows that a significant portion of PLWHA (42%) is still in urgent need of access to treatment, as later initiation of ART has been associated with higher mortality [10–12]. Certain barriers to accessing ART may be related to factors preventing PLWHA being aware of their serostatus [13], or seeking care after HIV diagnosis [14–16]. Additional barriers related to differences in healthcare infrastructure, healthcare providers’ experience and patients’ characteristics, may also negatively affect prompt access to ART among PLWHA already seeking HIV care [17]. The Universities of Yaoundé/French Agency for AIDS Research (ANRS) Eval study is a cross-sectional survey providing an in-depth evaluation of the Cameroonian ART program [18,19]. It gave us the opportunity both to assess the extent to which decentralized HIV care at the district level has contributed to increased access to ART and to iden-
tify persistent barriers to access to ART for eligible PLWHA seeking care at both the central and district levels.
2. Materials and methods 2.1. Data collection The cross-sectional EVAL survey (ANRS12-116) was carried out between September 2006 and March 2007 using a random sample of patients meeting the following three criteria: diagnosed HIV-positive for at least 3 months, aged over 21 and attending HIV services in any one of the 8 national ATCs in Douala and Yaoundé, 6 ATCs located in provinces (Center, Littoral, West, South-West, NorthWest and Far-North) or 13 district hospitals (MUs). In each facility, healthcare workers randomly selected survey participants among eligible patients and refusals to participate were recorded. Patients who accepted to participate had to fill in a written informed consent form. At the end of their consultation they were referred to a trained interviewer who administered a face-to-face questionnaire independently from medical staff. All interviews were conducted in French or English depending on the geographical area. When necessary, interviews were also conducted in local languages by a trained team member. The questionnaire covered the following topics: sociodemographic and economic characteristics of respondents and their households, disease history, perception of treatments and medical follow-up, adherence to ART, detailed healthcare expenditures for the previous month, perception of health status and quality of life, and finally social relationships. After the interviews, blood samples were collected at the hospital laboratory in order to assess patients’ CD4 count at the time of the survey. Clinical data from both clinical examination of patients and retrospective medical files were collected by care providers using medical questionnaires. ART eligibility at the time of the survey was defined using the following criteria: diagnosed HIV-positive for at least 3 months, having AIDS status (using stage C of WHO clinical scale) or a CD4+ T-cell count lower than 200 cells/mm3 . In addition, because of continued uncertainty regarding the optimal guidelines for ART initiation for patients coinfected with tuberculosis (TB) [20–22], those who were actively being treated for TB at the time of the survey were excluded from the present analysis. In addition, data about the characteristics of the 27 healthcare facilities participating in the survey were obtained by each of the survey supervisors, through interviews with hospital managers and nursing staff as well as by performing cross-validation with data included in the administrative reports sent to the National AIDS Control Committee (NACC). Healthcare facility characteristics included the following: legal status, number of hospital beds, availability of equipment and laboratory tests, human resources in charge of PLWHA, number of PLWHA in the clientele and number of ART-treated patients. The existence (or not) of a “task shifting” policy in the facility [23], that is to say the formal delegation of some consultations for HIV care from physicians to nursing staff, was also recorded.
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2.2. Statistical analysis Data entry was performed using MS Access 2007 and analysis with SPSS for Windows version 15.0 (SPSS system). Comparisons between different facilities’ characteristics, between ART and non-ART-treated eligible patients, and between ART-treated patients in ATCs and those in MUs, were performed using Chi-square or Fisher tests for categorical variables and Student’s t-test or Kruskal–Wallis non-parametric test for continuous variables (depending on whether or not they were normally distributed). All p-values quoted here are two sided, with a p-value < 0.05 considered as significant. For the sub-samples of eligible patients at both the central and district levels, multivariate analysis using stepwise logistic regression models was used to identify factors associated with not being ART-treated. The following characteristics, whether belonging to the individual patient or the healthcare facility, were included in the multivariate analysis: CD4+ T-cell count at the time of the patient’s first visit to the facility, age, gender, educational level and time since initial HIV diagnosis as well as all other significant variables at the threshold level p < 0.2. Final models were obtained by backward stepwise selection procedures. 3. Results As shown in Table 1, the total workload (number of new ART initiations per month and ART-treated patients followed-up in the facility) was significantly lower at the district MUs level than in ATCs, as was the workload per
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member of medical staff. Not surprisingly, the availability of laboratory equipment was more limited and task shifting from physicians to nursing staff was more common at district level. Among the 3488 patients approached, 3170 (91%) agreed to participate in the survey, and 99% of those filled out the questionnaire. This led to a total sample of 3151 respondents (global response rate = 90%). Among respondents, 4.3% (136) were being treated for TB and 14.2% (449) had clinical and immunological characteristics that did not make them eligible for ART. Among the 2566 patients eligible for ART, only a minority of 7.0% (180) had not initiated ART at the time of the survey. Information about sociodemographic and clinical characteristics of patients eligible for ART is summarized in Table 2. The majority of this sample were women (71.3%), and had at least secondary level education (55.0%) with a median age of 36.7 years. Most of the patients (70%) were employed with a regular source of income at the time of the study with occupational breakdown as follows: selfemployed or craftsmen (32%), company employee (28%) and subsistence farmers (23%). The median monthly household income was however quite low, circa CFA F 40,000 (EUR 60.4) given that the threshold for the absolute poverty line in Cameroon is CFA F 20,000 (EUR 30.2) (circa US$ 40) [24,25]. About one-third (30.6%) of the sample was receiving care at district level in MUs. ART-treated patients had a lower socio-economic status at district level than those being treated in ATCs: 61.3% had only primary school education in district hospitals vs. 37.0% in ATCs; median household income was CFA F
Table 1 Comparison of characteristics of HIV services (n = 27) according to the level of decentralization of healthcare supply in Cameroon (EVAL survey, ANRS 12-116). Variables HIV Services No. of HIV services or median [IQR] Sector Public Private (for pofit) Private (faith based) No. of hospital beds Laboratory equipment (score ranging from 0 to 10)b Availability of CD4 cell counter (yes) Healthcare staff or HIV care f(nb. of full-time equivalent) Total healthcare staff Physicians Nursing staff Social workers Non-qualified staff No. of ART-treated patients No. of new ART-treated patients per month No. of ART-treated patients per physician No. of ART-treated patients per physician and nurse Task shifting from physicians to nursing staff No Yes
Total (n = 27)
20 2 5 151 [94; 240] 8.0 [7.0; 9.0] 20 14 [10; 18] 3 [2; 4] 5 [3; 6] 3 [2; 4] 3 [1; 4] 540 [225; 976] 31 [15; 51] 214 [65; 410] 72 [32; 144] 6 21
ATCs Central and Provincial (n = 14)
12 2 0 198 [90; 300] 9.0 [8.7; 9.0] 13 18 [13; 19] 4 [2; 5] 5 [3; 6] 4 [2; 6] 4 [1; 5] 920 [524; 1701] 47 [31; 77] 305 [148; 643] 137 [67; 198] 5 9
District MUs (n = 13)
8 0 5 120 [93; 166] 7.0 [4.5; 8.0] 7 12 [9; 15] 3 [2; 3] 4 [3; 6] 2 [1; 3] 2 [1; 4] 225 [101; 537] 15 [10; 28] 75 [43; 221] 32 [18; 73] 1 12
p-Valuea
0.01
0.168 0.08 0.021 0.033 0.081 0.89 0.031 0.203 0.019 0.009 0.035 0.015 0.08
IQR = interquartile range. a Chi-square test and Fisher’s exact test for categorical variables, and Kruskal–Wallis test for continuous variables. b Technical equipment level was assessed by the availability of performing the 10 following laboratory tests on site: complete cell blood count, CD4 cell count, transaminases, glycemia, creatinemia, amylasemia, pregnancy test, viral load, triglycerides and cholesterol.
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Table 2 Comparison of ART and non-ART-treated patients among a sample of HIV-infected patients eligible for treatment in Cameroon (n = 2566). p-Valuea (2) vs. (3)
(1) Total n = 2566
(2) ART-treated n = 2386 (93%)
(3) Non-ART-treated n = 180 (7%)
Age: median (IQR)
36.7 (31.4; 40.0)
36.8 (31.4; 44.4)
34.8 (29.0; 42.0)
0.007
Gender Female Male
1,830 (71.3) 736 (28.7)
1,705 (71.5) 681 (28.5)
125 (69.4) 55 (30.6)
0.56
Secondary or higher education level Yes No
1,427 (55.6) 1,139 (44.4)
1,059 (44.4) 1,327 (55.6)
80 (44.4) 100 (55.6)
0.98
Marital status Single or divorced Married Living in couple but not married
1,383 (53.9) 918 (35.8) 265 (10.3)
1,294 (54.2) 863 (36.2) 229 (9.6)
89 (49.4) 55 (30.6) 36 (20.0)
<0.0001
Employed Yes No
1,797 (70.0) 769 (30.0)
1,693 (71.0) 693 (29.0)
104 (57.8) 76 (42.2)
<0.0001
40,000 (20,000; 74,000) 7,000 (3,700; 11,000)
40,000 (20,200; 73,600) 7,000 (3,800; 11,000)
36,500 (20,000; 75,000) 5,600 (1,600; 17,800)
0.38 0.001
17 (8; 38)
17 (8; 37)
11 (3; 53)
0.09
329 (199; 433) 22 (12; 40)
343 (218; 447) 23 (12; 41)
127 (45; 228) 14 (6; 27)
<0.0001 <0.0001
Time between initial HIV diagnosis and first consultation for HIV care ≤1 month 1,457 (56.8) >1 month 1,109 (43.2)
1,378 (57.8) 1,008 (42.2)
79 (43.9) 101 (56.1)
<0.0001
Obtained initial HIV diagnosis in the same hospital than current follow-up Yes No 1,400 (54.6) 1,166 (45.4)
1,331 (55.8) 1,055 (44.2)
69 (38.3) 111 (61.7)
<0.0001
Declares that “making an appointment with the hospital physician is” Very or quite difficult 559 (21.8) Very or quite easy 2,007 (78.2)
507 (21.2) 1,879 (78.8)
52 (28.9) 128 (71.1)
0.017
Consulted a traditional healer in the prior 6 months Yes No
239 (9.3) 2,327 (90.7)
212 (8.9) 2,174 (91.1)
27 (15.0) 153 (85.0)
0.006
170 (120; 300) 82 (48; 181)
170 (120; 300) 82 (53; 181)
213 (110; 300) 112 (38; 187)
<0.0001 0.074
577 (22.5) 1,989 (77.5)
517 (21.7) 1,869 (78.3)
60 (33.3) 120 (66.7)
<0.0001
CD4 count facility at hospitalb Yes No
2,236 (87.1) 330 (12.9)
2,092 (87.7) 294 (12.3)
144 (80.0) 36 (20.0)
0.003
Structure providing careb ATCs District MUs
1,780 (69.4) 786 (30.6)
1,663 (69.7) 723 (30.3)
117 (65.0) 63 (35.0)
0.18
Household monthly income (CFAF): median (IQR) Monthly out-of-pocket expenditures (CFAF): median (IQR) % of health expenditures in household income median (IQR) CD4+ T-cell counts (cells/mm3 ): median (IQR) Time since HIV diagnosis (months): median (IQR)
No. of hospital bedsb : median (IQR) No. of HIV+ patients per medical staffb : median (IQR) Task shifting from physician to nursesb No Yes
a b
p-Value for the Pearson’s 2 for categorical row variables (and ANOVA t- or Kruskal–Wallis test for continuous variables). Characteristics of the facilities in which patients were followed.
30,000 (IQR: 15,800; 50,000) in district hospitals vs. CFA F 46,500 (IQR: 25,000; 82,600) in ATCs. Monthly out-ofpocket payments for HIV care and ART were significantly lower at the district level (median 5400 [3600; 8500] vs. 7500 [4000; 12,000], respectively; p < 0.0001). However, because household income was significantly lower at district level, the proportion of income devoted to HIV care was similar among ART-treated patients in district MUs and those in ATCs (17% vs. 18%, respectively; p = 0.836). More-
over, delays between HIV diagnosis and first consultation after diagnosis were significantly shorter at district level than for ATCs (62.4% vs. 55.7% with a delay of less than 1 month; p = 0.003). CD4 counts at ART initiation were significantly higher for patients being treated at district level (mean = 146 vs. 130 cell/mm3 ; p < 0.0001). Table 2 shows that among all the patients eligible for treatment at time of the survey, quite logically, ARTtreated patients had significantly higher CD4 cell counts
S. Loubiere et al. / Health Policy 92 (2009) 165–173
than their non-ART-treated counterparts. However, these latter had been HIV diagnosed for a shorter period of time (Table 2) and their CD4 counts (median = 127; IQR: 45–228) were significantly higher when compared with those evaluated for the ART-treated patients when they first started treatment (median = 125; IQR: 67–180) (p < 0.0001). Whereas the gender distribution was similar in both the ART and non-ART-treated groups, Table 2 shows that nonART-treated patients tended to be younger and of lower socio-income status (i.e. lower household income and lower rate of employment). They were also more likely to be living in a couple but not married to their partner. NonART-treated patients also seemed to face more difficulties in their relationship with the healthcare delivery system. A higher proportion among non-ART-treated patients than their ART-treated counterparts were being followed in a facility different from the one where they obtained their initial HIV diagnosis. Moreover, they had waited for more
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than 1 month before seeking HIV care after their diagnosis, expressed having more difficulties when trying to make an appointment to consult with medical staff of the healthcare facility and were also more likely to consult traditional healers. Table 2 shows that non-ART-treated patients devoted a lower share of their income to out-ofpocket healthcare expenditures, although this difference did not reach statistical significance. Detailed analysis of out-of-pocket healthcare expenditures however reveals that once ARV drugs were excluded from the calculation, non-ART-treated patients tended to spend significantly more on all components of HIV care (median = CFA F 5600 vs. 2500, respectively; p < 0.0001). Transportation costs to HIV care centers were similar however among ART and non-ART-treated patients (median = CFA F 1000 vs. 800, respectively; p = 0.23). In addition, Table 2 shows that overall, the proportion of non-ART-treated patients among all those eligible for
Table 3 Factors associated with non-being ART-treated in a sample of HIV-infected patients eligible for treatment according to level of HIV care delivery (multivariate logistic regression analyses) (n = 2566) (EVAL survey, ANRS 12-116). ATCs
p
District MUs
Odds ratio [95% CI]
p
Odds ratio [95% CI]
Age
0.96 [0.94; 0.98]
0.001
1.01 [0.97; 1.03]a
0.951
Gender Female Male
1 1.74 [1.10; 2.79]
0.020
1a 1.02 [0.51; 2.02]
0.959
Secondary or higher education level Yes No
1 2.11 [1.37; 3.23]
0.001
1* 0.67 [0.38; 1.20]
0.183
Marital status Single or divorced Married Living in couple but not married
NS
Employment Yes No
1 1.68 [1.12; 2.52]
% of health expenditures in household income CD4+ T-cell countsb Time since initial HIV diagnosis
NS 1.004 [1.002; 1.006] 0.98 [0.97; 0.99]
1 0.84 [0.44; 1.60] 2.82 [1.08; 7.35] 0.014
<0.001 <0.001
Time between initial HIV diagnosis and first consultation for HIV care <1 month NS >1 month Obtained initial HIV diagnosis in the hospital of current follow-up Yes 1 No 2.60 [1.70; 4.02]
<0.001
1 1.80 [1.07; 3.30]
0.05
1.005 [1.002; 1.007] 1.001 [0.97; 1.03]a 0.96 [0.94; 0.98]
0.003 0.526 0.001
1 2.70 [1.53; 4.77]
0.001
NS
Patients treated in an hospital with no. of hospital beds: <150 >150
NS
No. of HIV+ patients per medical staff
1.008 [1.005; 1.011]
<0.001
–a
Task shifting from physician to nurses None or little Quite a lot or a lot
3.41 [2.17; 5.36] 1
<0.001
–a
CD4 count facility at hospital Yes No
1 2.51 [1.30; 4.87]
NS
95% CI: confidence interval, p = 0.95. a This variable was forced in the final model. b At the time of ART initiation vs. at the time of the survey for ART eligible but untreated patients.
0.600 0.034
1 2.79 [1.48; 5.25]
0.006
0.001
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treatment did not significantly differ between district and ATCs levels, but that it was significantly higher in healthcare facilities where equipment for performing CD4 counts was not available (i.e. mostly in district MUs, see Table 1). The proportion of non-ART-treated patients was also significantly higher in larger facilities, as well as in facilities where the workload per medical staff member was higher and those where no task shifting policy existed. These latter two characteristics were more frequent in ATCs (see Table 1). After adjustment for both time since initial HIV diagnosis and CD4 counts (at initiation of treatment for those ART-treated and at the time of survey for those who were not), the socio-economic factors associated with a lack of access to ART in the multiple regression models differed depending on the level of care (see Table 3). The only exception to this was being unemployed. Younger and male patients, as well as those who only had a primary educational level were less likely to be ART-treated in ATCs. However, these factors were not associated with nonART-treated patients followed at district level. The only socio-economic characteristic which appeared to be associated with a lack of access to ART in MUs, but not in ATCs, was the fact of living in a couple without being married. Specific healthcare behaviors, such as a longer delay between HIV diagnosis and first medical consultation for HIV care, as well as a higher proportion of income being devoted to health expenditures were associated with a lack of access to ART in MUs but not in ATCs. On the other hand, patients who had changed HIV care center after their HIV diagnosis were less likely to be treated with ART when they sought care in ATCs. Characteristics of facilities which seemed to play a negative role in access to ART were also different at central and district levels. Not surprisingly, for patients followed-up in district MUs, the lack of availability of equipment for CD4 counts was associated with a lower likelihood of getting access to ART. Access to ART was also lower in MUs located in the larger district hospitals (150 hospital beds or more). On the contrary, the size of the hospital did not seem to influence access to ART in ATCs. Among patients followed in ATCs, a higher workload for medical staff members and the absence of task shifting were significantly associated with lower access to ART. 4. Discussion The EVAL survey was representative of PLWHA seeking HIV care in six of the ten provinces of Cameroon at the end of 2006-beginning of 2007. Survey results confirm a remarkable achievement for the national ART program in Cameroon, since the overwhelming majority (93%) of eligible patients had effective access to this life-saving therapy. The minority (7%) of non-ART-treated eligible patients tended to have been diagnosed for HIV later than those already on ART. They also tended to have had higher CD4 counts at the time of the survey when compared with those of their ART-treated counterparts taken at the time of ART initiation. These two points suggest that one can be quite optimistic that these patients will ultimately obtain access to ART. In contrast with results from studies conducted in
other low-resource settings [25,26], transportation costs and difficulties in making appointments with physicians were not found to be associated with delays in initiating ART in multivariate analysis. These positive achievements have clearly been facilitated by the scaling-up of access to ART, not only in the main cities of the country but also at the decentralized district level. Considering the epidemiological situation of Cameroon where individuals with a greater level of education are more likely to be HIV-infected [28], results also show that the decentralization of ART delivery has increased access for PLWHA from the lower socio-economic groups who are likely to be hit harder by the downstream impacts of AIDS [29]. Since it is estimated that 42% of the total number of PLWHA in urgent need of ART were not yet provided for as of June 2008, the EVAL survey suggests that the main persisting barriers to access ART in Cameroon concern insufficient access to HIV testing [13], difficulties in patients’ referral from HIV counseling and testing to ART delivery centers [30,31], and delays between HIV diagnosis and access to HIV care [14,15]. Some limitations of the EVAL survey should be acknowledged as they may have led to some underestimation of the difficulties encountered in the process of ART delivery at national level. Indeed, three of the four provinces not included in the survey (Adamoua, South and East) have the lowest estimated rates of ART coverage (<40%). Patients with active TB treatment at the time of the survey were also excluded from the present analysis, while difficulties in optimal management of HIV care for coinfected patients could have increased delays in access to ART [32]. In Cameroon, the management of TB in the context of ART is based on the Directly Observed Treatment, Short-Course (DOTS) program and anti-TB drugs are available free of charge at the point of care delivery. Treatment guidelines consist in initiating ART 2 months after initiating anti-TB treatment. However, difficulties in the supply of anti-TB drugs combined with a lack of adherence to antiTB treatment often increase the delay in initiating HAART in co-infected patients [21,22]. In addition, several studies have shown that treating TB patients who are also HIV-positive may be less cost-effective than treating HIVnegative ones [33,34]. On the other hand, the financial barrier to accessing ART was lowered further in Cameroon after the EVAL survey was completed. In Cameroon, as in many African countries, outof-pocket payments by households at the point of services delivery still provide the main contribution to healthcare financing (circa 70.0% of total health expenditures) [35]. These out-of-pocket expenditures, associated with a loss in income due to HIV-related morbidity, often constitute a major barrier to accessing ART in low-resource settings [27,36]. The continued requirement of user fees in order to access HIV services and medications has been shown to be detrimental to long-term adherence and clinical effectiveness of ART in many African countries including Cameroon [37–40]. At the time of the EVAL survey, ARV drugs were already heavily subsidized in Cameroon thanks to support from international donors, such as the Global Fund to fight AIDS, TB and Malaria, but patients still had to contribute a fraction of the drug costs: monthly out-of-pocket payments amounted to 3000 FCFA, circa 6 US$, for the generic
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Triomune regimen, and 7000 FCFA, circa 14 US$, for other first-line regimens [41]. These costs partly explain not only why patients devoted a significant portion of their household income to healthcare in the EVAL study but also how this payment constituted a barrier to ART access for certain groups of non-ART-treated patients, notably at district level. In May 2007, the national ART program introduced a new policy guaranteeing access to free of charge ARVs to all PLWHA eligible for treatment. This policy has already contributed to increased diffusion of ART (between June 2007 and June 2008, the national rate of ART coverage increased by circa 10%). However, it should be acknowledged that this policy does not suppress all financial barriers as patient out-of-pocket payments are still required for other components of HIV care (laboratory tests, medical consultations, transportation costs, etc.) [42,43]. Indeed, the fact that eligible non-ART-treated patients in the EVAL survey tended to have higher out-of-pocket payments than those treated with ART (excluding ARV drugs payments) suggests that the persistence of financial barriers to accessing ART will not be fully overcome by free of charge ARV drugs. In addition to out-of-pocket costs associated with ART, the EVAL survey has identified a number of factors, either related to patients’ individual characteristics or to bottlenecks within the HIV care delivery system, which persist in delaying access to ART even for PLWHA who are aware of their serostatus and who already have access to HIV care. Although, as already mentioned, these factors do not impede the great majority of medically eligible PLWHA from accessing ART, they still need to be overcome, as scaling-up ART coverage may exacerbate them. The high proportion of women in the EVAL sample could be related to the epidemiological situation in Cameroon: according to national estimates, there is a higher proportion of women than men in the total HIV-infected population and in the population eligible for ART (circa 62%) [44]. In addition, national ART coverage is significantly higher among women (62.5% vs. 51.1% for men). The EVAL survey suggests that this lower rate of coverage among male PLWHA may not only be due to greater reluctance to be HIV tested and to seek care, but could also be related to additional difficulties in accessing ART, particularly in ATCs. Of course, individual characteristics like age, male gender, lower educational level and lower income which were all found to be associated with a lower likelihood of access to ART in eligible patients may to some extent reflect the variability of patients’ preferences in their willingness to access treatment. However, the fact that these factors played a role in ACTs but not in district MUs suggests that male patients, as well as patients with a lower socioeconomic status, are less likely to have their treatment needs adequately recognized in the larger hospitals which have a higher burden of HIV care than in district ones which are in closer proximity to local communities. Conversely, the fact that PLWHA living in non-married couples had less access to ART at district level suggests that they may face specific difficulties due to pressures related to their close social environment, and may possibly be less willing to disclose their serostatus to their local community [2]. Finally, a pressing challenge to achieving universal access to HAART in sub-Saharan Africa is to provide basic
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but efficient HIV care infrastructure [45]. The experience of Cameroon strongly supports the idea that decentralization of ART delivery is a feasible solution to that problem. However, health systems strengthening (HSS) is still needed to overcome some remaining barriers to accessing ART and, more importantly, to guarantee its long-term sustainability. As suggested by the EVAL survey, HSS priorities should be adapted to the practical issues faced at each level of care. Indeed, the increased number of people seeking HIV care in proportion to the lack of highly qualified personnel may impede the ability to start ART-eligible patients on treatment, notably in the larger hospitals based in the main cities [46]. Although the World Health Organization recommends the promotion of task shifting within HIV services delivery in resource limited settings [23], Cameroon does not yet have a defined national task-shifting strategy in the scaling-up of its ART program and initiative on this matter is left to each individual healthcare facility. Standardized guidelines on task shifting may be especially useful in ATCs at central level where both the number of healthcare professionals involved in HIV care and the number of HIVinfected patients is the highest. At district level, there is a need to provide every facility with appropriate laboratory test equipment for diagnosis, treatment initiation and follow-up in order to keep patients in the same location [47]. A complementary alternative would be to promote a more optimal use of simplified algorithms for HIV care and treatment at the more decentralized level: in accordance with the WHO recommendations for scaling-up ART in lowresource settings, national guidelines in Cameroon allow district hospitals without CD4 count machines to initiate ART on the basis of clinical examination and total lymphocyte count [6]. The performance of this WHO “public health” approach is currently being evaluated in a Ministry of Public Health of Cameroon/ANRS randomized trial (STRATALL ANRS 12120) [41]. The cross-sectional design of the EVAL survey did not facilitate an in-depth investigation of time dependent factors in the evaluation of the Cameroonian national ART program. It remains to be seen, through longitudinal data collection, or at least through repetition at other points in time of cross-sectional surveys using a similar methodology to EVAL, the extent to which the significant progress obtained in access to ART in this country will further expand to reach universal coverage and if it will continue in the long term. Conflicts of interest None declared. Acknowledgements We would like to thank the Cameroonian Ministry of Public Health for its support together with the French National Agency for Research on AIDS and Hepatitis (ANRS). We would also like to thank all 27 participating hospitals and their medical teams for their involvement in the survey. Finally, we would like to thank all the patients who accepted to take part in the study.
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Funding: This work was supported by the French National Agency for Research on AIDS and Hepatitis. The authors declare that they have not entered into any agreement with the funding organization which may have limited their ability to complete the research as planned, and state that they have had full control of all primary data.
References [1] Bertozzi S, Gutierrez JP, Opuni M, Walker N, Schwartlander B. Estimating resource needs for HIV/AIDS health care services in low-income and middle-income countries. Health Policy 2004;69: 189–200. [2] Desclaux A, Ciss M, Taverne B, Sow PS, Egrot M, Faye MA, et al. Access to antiretroviral drugs and AIDS management in Senegal. AIDS 2003;17(Suppl. 3):S95–101. [3] Lawn SD, Myer L, Orrell C, Bekker LG, Wood R. Early mortality among adults accessing a community-based antiretroviral service in South Africa: implications for programme design. AIDS 2005;19:2141–8. [4] Susman E. Botswana gears up to treat HIV patients in Africa’s largest program. AIDS 2004;18:N1–2. [5] Katzenstein D, Laga M, Moatti JP. The evaluation of the HIV/AIDS drug access initiatives in Cote d’Ivoire, Senegal and Uganda: how access to antiretroviral treatment can become feasible in Africa. AIDS 2003;17(Suppl. 3):S1–4. [6] Gilks CF, Crowley S, Ekpini R, Gove S, Perriens J, Souteyrand Y, et al. The WHO public-health approach to antiretroviral treatment against HIV in resource-limited settings. Lancet 2006;368:505–10. [7] Gruenais M, editor. Changing a health system: the case of Cameroon. In: Euro-African Association for the Anthropology of Social Change and Development. APAD Report no. 21. Paris; 2002. [8] Ministry of Public Health & National AIDS Control Committee. Towards universal access to care and treatment for adults and children living with HIV/AIDS in Cameroo [in French]. In: Progress Report no. 11. Yaoundé, Cameroon; 2008. [9] UNAIDS. Report on the global AIDS epidemic. In: UNAIDS. Geneva; 2008. [10] Badri M, Bekker LG, Orrell C, Pitt J, Cilliers F, Wood R. Initiating highly active antiretroviral therapy in sub-Saharan Africa: an assessment of the revised World Health Organization scaling-up guidelines. AIDS 2004;18:1159–68. [11] Chadborn TR, Baster K, Delpech VC, Sabin CA, Sinka K, Rice BD, 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;19:513–20. [12] Rosen S, Fox MP, Gill CJ. Patient retention in antiretroviral therapy programs in sub-Saharan Africa: a systematic review. PLoS Medicine 2007;4:e298. [13] De Cock KM, Mbori-Ngacha D, Marum E. Shadow on the continent: public health and HIV/AIDS in Africa in the 21st century. Lancet 2002;360:67–72. [14] Girardi E, Sabin CA, Monforte AD. Late diagnosis of HIV infection: epidemiological features, consequences and strategies to encourage earlier testing. Journal of Acquired Immune Deficiency Syndromes 2007;46(Suppl. 1):S3–8. [15] Person AK, Ramadhani HO, Thielman NM. Antiretroviral treatment strategies in resource-limited settings. Current HIV/AIDS Reports 2007;4:73–9. [16] Marcellin F, Abe C, Loubiere S, Boyer S, Blanche J, Koulla-Shiro S, et al. Delayed first consultation after diagnosis of HIV infection in Cameroon. AIDS; Apr 1. [Epub ahead of print]. [17] Sow PS, Otieno LF, Bissagnene E, Kityo C, Bennink R, Clevenbergh P, et al. Implementation of an antiretroviral access program for HIV1-infected individuals in resource-limited settings: clinical results from 4 African countries. Journal of Acquired Immune Deficiency Syndromes 2007;44:262–7. [18] Boyer S, Marcellin F, Ongolo-Zogo P, Abega S, Nantchouang R, Spire B, et al. Financial difficulties in accessing HIV care in Yaoundé, Cameroon: first results from the national cross-sectional survey EVAL-ANRS 12-116. Bulletin World Health Organization 2009;87:279–87. [19] Marcellin F, Boyer S, Protopopescu C, Carrieri MP, Ongolo-Zogo P, Abega SC, et al. Risk of antiretroviral treatment interruption among people living with HIV in Yaoundé, Cameroon (EVAL survey ANRS 12116): determinants, recommendations and possible interventions. Tropical Medicine and International Health 2008;13:1470–8.
[20] Lawn SD, Myer L, Bekker LG, Wood R. Tuberculosis-associated immune reconstitution disease: incidence, risk factors and impact in an antiretroviral treatment service in South Africa. AIDS 2007;21: 335–41. [21] Lawn SD, Wood R. Impact of antituberculosis treatment on virological response to highly active antiretroviral therapy: implications for resource-limited settings? Journal of Infectious Diseases 2006;194:1467–8, author reply 1468. [22] Wood R. The case for integrating tuberculosis and HIV treatment services in South Africa. Journal of Infectious Diseases 2007;196(Suppl. 3):S497–9. [23] Samb B, Celletti F, Holloway J, Van Damme W, De Cock KM, Dybul M. Rapid expansion of the health workforce in response to the HIV epidemic. New England Journal of Medicine 2007;357:2510–4. [24] Direction de la Statistique et de la Comptabilité Nationale. Enquête à indicateurs multiples, 2000 (MICS 2000) (in French). In: DSCN, Ministère de l’Economie et des Finances. Yaoundé, Cameroun; 2001. [25] Institut National de la Statistique. Deuxième enquête camerounaise auprès des ménages en 2001 (ECAM II 2001)—Conditions de vie des populations et profil de pauvreté au Cameroun en 2001—Rapport principal de l’enquête (in French). In: INS, Ministère de l’Economie et des Finances, République du Cameroun. Yaoundé, Cameroun; 2002. [26] Mukherjee JS, Ivers L, Leandre F, Farmer P, Behforouz H. Antiretroviral therapy in resource-poor settings. Decreasing barriers to access and promoting adherence. Journal of Acquired Immune Deficiency Syndromes 2006;43(Suppl. 1):S123–6. [27] Rosen S, Ketlhapile M, Sanne I, DeSilva MB. Cost to patients of obtaining treatment for HIV/AIDS in South Africa. South African Medicine Journal 2007;97:524–9. [28] Fortson JG. The gradient in sub-Saharan Africa: socioeconomic status and HIV/AIDS. Demography 2008;45:303–22. [29] Barnett T, Whiteside A, Khodakevich L, Kruglov Y, Steshenko V. The HIV/AIDS epidemic in Ukraine: its potential social and economic impact. Social Science and Medicine 2000;51:1387–403. [30] Tantchou Yakam J. New actors in the fight against HIV/AIDS: overlapping and competition between existing structures [in French]. La Medicina Tropical 2008;68:300–5. [31] Tantchou-Yakam J, Gruenais M. Involving new actors to achieve ART scaling up: difficulties in an HIV/AIDS testing and counselling centre in Cameroon. International Nurse Reviews 2009;56:50–7. [32] Ainsworth M, Beyrer C, Soucat A. AIDS and public policy: the lessons and challenges of “success” in Thailand. Health Policy 2003;64:13–37. [33] El-Sony AI. The cost to health services of human immunodeficiency virus (HIV) co-infection among tuberculosis patients in Sudan. Health Policy 2006;75:272–9. [34] Murray CJ, DeJonghe E, Chum HJ, Nyangulu DS, Salomao A, Styblo K. Cost effectiveness of chemotherapy for pulmonary tuberculosis in three sub-Saharan African countries. Lancet 1991;338:1305–8. [35] WHO. Working together for health. In: The World health report 2006. Geneva; 2006. [36] Hardon AP, Akurut D, Comoro C, Ekezie C, Irunde HF, Gerrits T, et al. Hunger, waiting time and transport costs: time to confront challenges to ART adherence in Africa. AIDS Care 2007;19:658–65. [37] Boyer S, Blanche J, Protopopescu C, Bonono CR, Marcellin F, OngoloZogo P, et al. Impact of the structural characteristics of healthcare supply in antiretroviral treatment interruption in Cameroon. In: XVII International AIDS Conference. 2008. [38] Laniece I, Ciss M, Desclaux A, Diop K, Mbodj F, Ndiaye B, et al. Adherence to HAART and its principal determinants in a cohort of Senegalese adults. AIDS 2003;17(Suppl. 3):S103–8. [39] Weiser S, Wolfe W, Bangsberg D, Thior I, Gilbert P, Makhema J, et al. Barriers to antiretroviral adherence for patients living with HIV infection and AIDS in Botswana. Journal of Acquired Immune Deficiency Syndromes 2003;34:281–8. [40] Braitstein P, Brinkhof MW, Dabis F, Schechter M, Boulle A, Miotti P, 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;367:817–24. [41] Koulla-Shiro S, Delaporte E. The public health approach to antiretroviral treatment: the case of Cameroon. In: Coriat B, editor. The political Economy of HIV/AIDS in developing countries (TRIPS, public health systems and free access). UK: Edward Elgar, Cheltenham; 2008. p. 259–71. [42] Bernell SL, Shinogle JA. The relationship between HAART use and employment for HIV-positive individuals: an empirical analysis and policy outlook. Health Policy 2005;71:255–64. [43] Joy R, Druyts EF, Brandson EK, Lima VD, Rustad CA, Zhang W, et al. Impact of Neighborhood-Level Socioeconomic Status on HIV Disease Progression in a Universal Health Care Setting. Journal of Acquired Immune Deficiency Syndromes 2008;47:500–5.
S. Loubiere et al. / Health Policy 92 (2009) 165–173 [44] UNAIDS. Epidemiological fact sheets on HIV/AIDS and sexually transmitted infections. Cameroon 2006 update. Geneva: UNAIDS; 2006. [45] Dunne M. Antiretroviral drug development: the challenge of cost and access. AIDS 2007;21(Suppl. 4):S73–9. [46] Vassall A, Compernolle P. Estimating the resource needs of scalingup HIV/AIDS and tuberculosis interventions in sub-Saharan Africa: a
173
systematic review for national policy makers and planners. Health Policy 2006;79:1–15. [47] Gimbel-Sherr SO, Micek MA, Gimbel-Sherr KH, Koepsell T, Hughes JP, Thomas KK, et al. Using nurses to identify HAART eligible patients in the Republic of Mozambique: results of a time series analysis. Human Resource Health 2007;5:7.