Tuberculosis (TB) is the main cause of morbidity and mortality among human immunodeficiency virus (HIV) infected persons worldwide [
The Democratic Republic of Congo (DRC) carries the 9th highest burden of TB worldwide and 14% of patients with TB in DRC are also infected with HIV. Coverage of CPT and ART among HIV/TB patients in DRC substantially lags behind the regional and international averages though 70% and 48% of them were initiated on CPT and ART, respectively, in 2013, compared to 24% and 6% in 2010 [
The aims of this study were to assess the impact of the WHO 2010 guidelines and the remaining role of centralized HIV services on ART initiation among HIV/TB patients in the Democratic Republic of Congo (DRC).
In 2010, the Schools of Public Health of the University of North Carolina at Chapel Hill (UNC) and of the University of Kinshasa (KSPH) with funding from the President’s Emergency Plan For AIDS Relief (PEPFAR) through the US Centers for Disease Control and Prevention (CDC) and in collaboration with the DRC’s National TB Program (PNLT) and the National AIDS Control Program (PNLS) started providing operational and logistical support to TB clinics in Kinshasa and in Kisangani, the capital of the Oriental Province, for the implementation of HIV/TB collaborative activities. These included provider initiated counseling and testing for all patients seeking care in the clinics with symptoms suggestive of TB, provision of CPT, and linkage to HIV services for HIV/TB infected patients.
In addition to anti-TB medications, all TB patients diagnosed with HIV were initiated on CPT immediately. As of January 2012 in Kisangani and March 2012 in Kinshasa, the supported TB clinics started implementing the 2010 WHO ART initiation recommendations instead of the 2006 guidelines [
For monitoring purposes, at the end of each month, the TB nurse (in charge of TB treatment and HIV/TB registry) used information from the integrated TB and HIV registry in each clinic to report the number of new TB patients diagnosed during the month, the number of those with known HIV status prior to TB diagnosis, the number of those with unknown HIV status counseled and tested for HIV, the number of HIV/TB coinfected patients, the number of coinfected patients initiated on CPT, the number of coinfected patients with at least two weeks of anti-TB treatment that were referred for HIV care and treatment, and the number of those referred who were known (returned the counter referral form) to have been initiated on ART. The aggregated data was verified and validated each month by a member of UNC/KSPH technical team during their monthly supervision visit to each clinic. Validation consisted of verifying the reports to make sure there was no double counting and getting updated information on referral and uptake of referral for patients that remained active in the clinic. The validated report was taken back to the central monitoring and evaluation team and entered into an electronic database that was used for this analysis.
The main indicator of interest in this analysis was the proportion of HIV/TB patients initiated on ART before the end of their TB treatment. This proportion was calculated as the number of HIV/TB coinfected patients reported to have been initiated on ART divided by the total number of HIV/TB patients referred for HIV care and treatment. We also calculated and reported the proportion of HIV/TB coinfected patients initiated on CPT as the number of HIV/TB patients initiated on CPT divided by the total number of HIV/TB coinfected patients registered.
Another key variable that was used in this analysis as a measure of decentralization of HIV services was the integration of HIV and TB services in each clinic. TB clinics were classified in two groups based on presence or absence of onsite (located in the same health facility) HIV clinic with ART services.
Two periods were considered in the analysis: the period before and after implementation initiation of 2010 WHO guidelines, that is, before and after January 2012 in Kisangani and March 2012 in Kinshasa.
A Log-binomial regression model was used to calculate the proportion ratios (PR) and their 95% confidence intervals (95% CI) as a measure of impact of onsite ART services and that of implementation of 2010 WHO guidelines on the proportions of patients initiated on ART. Separate analyses were done for Kinshasa and Kisangani. All analyses were performed using SAS 9.3 (Cary, NC) and all tests were performed at a 0.05 significance level.
The routine data collection was approved by the University of North Carolina at Chapel Hill Institutional Review Board and the Kinshasa School of Public Health Ethical Committee.
Between November 2010 and June 2013, 20,912 TB cases were reported from 65 TB clinics in Kinshasa (Table
Numbers of TB cases counseled and tested for HIV by quarter and proportions of HIV+ cases initiated on cotrimoxazole prophylaxis and ART in Kisangani and Kinshasa.
Quarter | Number of clinics |
Total TB cases | With known HIV status |
Number tested |
HIV positive |
Initiated on CXT |
Total referred |
Initiated on ART |
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Q4 2010 | 20 | 844 | Na | 769 (91.1) | 119 (15.5) | 106 (89.1) | 77 | 62 (80.5) |
Q1 2011 | 20 | 1294 | Na | 1221 (94.4) | 187 (15.3) | 187 (100.0) | 119 | 118 (99.2) |
Q2 2011 | 20 | 1251 | 53 (4.2) | 1150 (96.0) | 109 (9.5) | 162 (100.0) | 90 | 77 (85.6) |
Q3 2011 | 20 | 1359 | 57 (4.2) | 1244 (95.5) | 135 (10.9) | 190 (99.0) | 136 | 77 (56.6) |
Q4 2011 | 32 | 1338 | 54 (4.0) | 1164 (90.7) | 111 (9.5) | 161 (97.6) | 82 | 62 (75.6) |
Q1 2012 | 32 | 2054 | 73 (3.6) | 1822 (92.0) | 195 (10.7) | 242 (90.3) | 129 | 89 (69.0) |
Q2 2012 | 32 | 2224 | 56 (2.5) | 2067 (95.3) | 206 (10.0) | 260 (99.2) | 167 | 141 (84.4) |
Q3 2012 | 65 | 2361 | 35 (1.5) | 2239 (96.3) | 253 (11.3) | 281 (97.6) | 212 | 185 (87.3) |
Q4 2012 | 65 | 2691 | 57 (2.1) | 2596 (98.6) | 269 (10.4) | 325 (99.7) | 233 | 216 (92.7) |
Q1 2013 | 65 | 2776 | 54 (1.9) | 2559 (94.0) | 299 (11.7) | 348 (98.6) | 274 | 251 (91.6) |
Q2 2013 | 65 | 2720 | 68 (2.5) | 2518 (94.9) | 298 (11.8) | 363 (99.2) | 280 | 268 (95.7) |
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Q2 2011 | 3 | 189 | 13 (6.9) | 149 (84.7) | 33 (13.4) | 44 (95.7) | 22 | 16 (72.7) |
Q3 2011 | 6 | 270 | 18 (6.7) | 248 (98.4) | 44 (10.5) | 58 (93.5) | 28 | 17 (60.7) |
Q4 2011 | 6 | 252 | 24 (9.5) | 207 (90.8) | 53 (14.0) | 53 (68.8) | 32 | 16 (50.0) |
Q1 2012 | 6 | 305 | 36 (11.8) | 221 (82.2) | 73 (16.7) | 69 (63.3) | 38 | 20 (52.6) |
Q2 2012 | 6 | 327 | 33 (10.1) | 229 (77.9) | 65 (14.0) | 63 (64.3) | 44 | 16 (36.4) |
Q3 2012 | 13 | 371 | 11 (3.0) | 348 (96.7) | 66 (15.8) | 73 (94.8) | 60 | 43 (58.9) |
Q4 2012 | 13 | 406 | 20 (4.9) | 385 (99.7) | 74 (14.0) | 93 (98.9) | 65 | 59 (90.8) |
Q1 2013 | 13 | 368 | 9 (2.4) | 350 (97.5) | 80 (20.3) | 88 (98.9) | 71 | 70 (98.6) |
Q2 2013 | 13 | 500 | 11 (2.2) | 489 (100.0) | 78 (13.7) | 89 (100.0) | 58 | 54 (93.1) |
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In Kisangani, 2,988 TB cases were reported between April 2011 and June 2013 in 13 TB clinics. The clinics were added in waves of three, three, and seven in the Q2 2011, Q3 2011, and Q3 2012, respectively (Table
Overall, prior to the implementation of the WHO 2010 guidelines, whether in Kinshasa or in Kisangani, the proportion of HIV/TB patients referred for HIV care who were initiated on ART fluctuated from quarter to quarter. However, in general, a greater proportion of coinfected patients in clinics with onsite ART services were initiated on ART compared to patients in clinics without onsite ART services. After implementation of the WHO 2010 guidelines, the gap between clinics with and without onsite ART services narrowed substantially (Figures
Proportions of HIV/TB coinfected patients initiated on ART by the end of TB treatment in clinics with and without onsite HIV services in Kinshasa.
Proportions of HIV/TB coinfected patients initiated on ART by the end of TB treatment in clinics with and without onsite HIV services in Kisangani.
Specifically, in Kinshasa, of the 1,799 HIV/TB patients referred for HIV care, 633 had been referred before implementation of the new guidelines including 507 from clinics with onsite ART and 126 from clinics without onsite ART services. Of those, 401 (79.1%) and 63 (50%), respectively, were reported to have been initiated on ART. The PR comparing ART initiation in clinics with that of clinics without onsite ART services was 1.58 (95% CI 1.32, 1.89) (Table
Effect of the WHO 2010 guidelines and that of decentralization of HIV services on ART initiation among HIV/TB patients in TB clinics in Kinshasa and Kisangani, Democratic Republic of Congo.
TB type | Population |
Period before |
PR (95% CI) |
Period after |
PR (95% CI) |
PR 95% CI | ||
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Eligible |
Initiated on ART | Eligible |
Initiated on ART | |||||
Kinshasa | Onsite ART | 507 | 401 (79.1) | 1.58 (1.32, 1.89) | 795 | 714 (89.8) | 0.97 (0.93, 1.00) | 1.14 (1.08, 1.19) |
No onsite ART | 126 | 63 (50.0) | 1 | 371 | 345 (93.0) | 1 | 1.86 (1.56, 2.22) | |
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Kisangani | Onsite ART | 76 | 53 (69.7) | 2.10 (1.40, 3.16) | 152 | 135 (88.8) | 1.22 (1.09, 1.37) | 1.27 (1.09, 1.49) |
No onsite ART | 44 | 16 (36.4) | 1 | 146 | 106 (72.6) | 1 | 2.00 (1.33, 2.99) |
Similarly, in Kisangani, of the 418 HIV/TB patients referred for HIV care, 120 were before the implementation of the WHO 2010 guidelines including 76 from clinics with onsite ART and 44 from clinics without onsite ART services. Of those, 53 (69.7%) and 16 (36.4%), respectively, were reported to have been initiated on ART: PR 2.10 (95% CI 1.40, 3.16) (Table
Following implementation of the 2010 guidelines, in Kinshasa, 1,166 HIV/TB patients including 795 and 371, respectively, from clinics with and without onsite ART services were referred for HIV care. Of those, 714 (89.8%) and 345 (93.0%), respectively, were initiated on ART. There was no statistical difference in the proportion of HIV/TB patients initiated on ART in TB clinics with and without onsite ART services after implementation of the 2010 guidelines in Kinshasa: PR = 0.97 (95% CI 0.93, 1.00).
In Kisangani, after implementation of the new guidelines, 298 HIV/TB patients including 152 and 146, respectively, from clinics with and without onsite ART service were referred for HIV care. Of those, 135 (88.8%) and 106 (72.6%), respectively, were initiated on ART. Despite having narrowed down substantially, compared to clinics without onsite ART services, ART initiation remained significantly higher in clinics with onsite services: PR = 1.22 (95% CI 1.09, 1.37) (Table
Overall, implementation of the 2010 WHO guidelines resulted in significant increase in the proportion of TB/HIV patients initiated on ART whether in Kinshasa or in Kisangani. Comparing the proportions of coinfected patients initiated on ART during the period following implementation to the proportion of those initiated during the period before, in Kinshasa, the proportion ratios were 1.14 (95% CI 1.08, 1.19) in clinics with onsite ART services and 1.86 (95% CI 1.56, 2.22) in clinics without onsite ART services. In Kisangani, the proportion ratios were 1.27 (95% CI 1.09, 1.49) and 2.00 (95% CI 1.33, 2.99), respectively, in clinics with and without onsite ART services (Table
Our aim was to assess the impact of removing the need for CD4 count evaluation before ART initiation brought about by the WHO 2010 guidelines and that of HIV services decentralization on the proportion of HIV/TB patients initiated on ART before the end of TB treatment. Our results show that implementation of the 2010 WHO guidelines resulted in substantial and statistically significant increased proportions of HIV/TB patients who were initiated on ART. The increase was sufficient to erase the statistically significant difference in the proportions of HIV/TB initiated on ART in clinics with and without ART services in Kinshasa. However, in Kisangani, clinics without onsite ART services continued to perform significantly lower in their ART initiation coverage.
To the best of our knowledge, this is the first study evaluating the impact of the 2010 change in WHO guidelines on access to ART among HIV/TB patients. Our finding that removal of the need for a CD4 count before initiation ART substantially increased the proportion of HIV/TB patients that were initiated on ART supports the public health goal of those recommendations and may appear obvious. However, despite the substantial and significant increase, the proportions of HIV/TB patients initiated on ART remained below those initiated on CPT even in clinics with onsite ART services and far below the 100% target particularly in the more provincial town of Kisangani. This is consistent with previous observations of substantial delays in ART initiation even in clinics with integrated TB and HIV services due to the lack of implementation fidelity to treatment guidelines [
Previous studies from South Africa showed that nonintegrated HIV and TB services negatively affect the timing of ART, mainly because of prolonged referral times in moving between TB and ART services [
The limitations of our study include the use of aggregated data. This prevented us from assessing the exact timing of ART initiation among patients. The proportion of patients initiated on ART should be interpreted as the proportion initiated before the end of TB treatment: six or eight months for new or retreatment cases. We do not know if all patients who were not referred were still in their first eight weeks of TB treatment. Moreover, we also lack information on why some patients who were referred for HIV services were never initiated on ART even in clinics with onsite services. However, it is unlikely that loss to follow-up played an important role given the high TB treatment success rate in the country [
In conclusion, implementation of the 2010 WHO guidelines that removed the need for CD4 counts before ART initiation resulted in substantial increases in the proportion of HIV/TB patients initiated on ART and narrowed the initiation gap between clinics with and without onsite ART services. However, ART initiation remained below that of CPT and below the 100% target, particularly in clinics without onsite ART services.
Meetings at which parts of the data were presented were held at 44th Union World Conference on Lung Health, Paris, France, on 30 October–3 November 2013. No funding bodies had any role in study design, data collection and analysis, decision to publish, or preparation of the paper.
The authors declare that they have no competing interests.
Implementation of TB and HIV programs in Kinshasa and Kisangani was conducted in collaboration with the Kinshasa School of Public Health, the National AIDS Control Program (PNLS), the National TB Program (PNLT), and the Provincial Coordination of PNLS and PNLT and was funded by the President’s Emergency Plan for AIDS Relief through the Centers for Disease Control and Prevention [Grant no. 5U2GPS001179-01]. Sources of support are Centers for Disease Control and Prevention, President’s Emergency Plan for AIDS Relief, Global Fund to Fight AIDS, Tuberculosis, and Malaria, and National Institutes of Health. Marcel Yotebieng is partially supported by a Grant from NICHD (R01HD075171) and another from NIAID (U01AI096299).