Abstract
HIV associated tuberculosis (TB) morbidity and mortality is a major concern in sub-Saharan Africa. Understanding the level of HIV infection among TB patients is vital for adequate response. We conducted a systematic review and meta-analysis to estimate the prevalence of HIV in TB patients in sub-Saharan Africa. We searched PubMed, EMBASE, Web of Science and CINAHL databases. A meta-analysis with a random-effects model was performed. Potential sources of heterogeneity in the prevalence estimates were explored using meta-regression analysis. We identified 68 studies that collectively included 62,969 TB patients between 1990 and 2017. The overall estimate of HIV prevalence in TB patients was 31.8% (95% CI 27.8–36.1). There was substantial heterogeneity in the prevalence estimates in Southern, Central, Eastern, and Western sub-Saharan Africa regions (43.7, 41.3, 31.1 and 25.5%, respectively). We noted an apparent reduction in the estimate from 33.7% (95% CI 27.6–40.4) in the period before 2000 to 25.7% (95% CI 17.6–336.6) in the period after 2010. The Eastern and Southern sub-Saharan Africa region had higher prevalence [34.4% (95% CI 29.3–34.4)] than the Western and Central region [27.3% (95% CI 21.6–33.8)]. The prevalence of HIV in TB patients has declined over time in sub-Saharan Africa. We argue that this is due to strengthened HIV prevention and control response and enhanced TB/HIV collaborative activities. Countries and regions with high burdens of HIV and TB should strengthen and sustain efforts in order to achieve the goal of ending both HIV and TB epidemics in line with the Sustainable Development Goals.
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References
World Health Organization. Global Tuberculosis Report 2017. WHO; 2017.
Jacobson LM, de Lourdes Garcia-Garcia M, Hernandez-Avila JE, et al. Changes in the geographical distribution of tuberculosis patients in Veracruz, Mexico, after reinforcement of a tuberculosis control programme. Trop Med Int Health. 2005;10(4):305–11.
World Health Organization. Global tuberculosis report 2013. World Health Organization; 2013.
World Health Organization. WHO policy on collaborative TB/HIV activities: guidelines for national programmes and other stakeholders. Geneva: WHO; 2014.
Unaids U. The gap report. Geneva: Switzerland; 2014.
UNAIDS. UNAIDS Data 2018.
World Health Organization. Tuberculosis (TB). Tuberculosis data; 2017; http://www.who.int/tb/data/en/.
Gao J, Zheng P, Fu H. Prevalence of TB/HIV co-infection in countries except China: a systematic review and meta-analysis. PLoS ONE. 2013;8(5):e64915.
Gao L, Zhou F, Li X, Jin Q. HIV/TB co-infection in mainland China: a meta-analysis. PLoS ONE. 2010;5(5):e10736.
Corbett EL, Marston B, Churchyard GJ, De Cock KM. Tuberculosis in sub-Saharan Africa: opportunities, challenges, and change in the era of antiretroviral treatment. Lancet. 2006;367:926–37.
United Nations (UN). Millennium Summit (6–8 September 2000); 2000.
World Health Organization. Towards universal access by 2010: how WHO is working with countries to scale-up HIV prevention, treatment, care and support. Geneva: World Health Organization; 2006.
Wilkinson D, Davies GR. The increasing burden of tuberculosis in rural South Africa—impact of the HIV epidemic. S Afr Med J. 1997;87(4):447–50.
Modesti PA, Reboldi G, Cappuccio FP, et al. Panethnic differences in blood pressure in Europe: a systematic review and meta-analysis. PLoS ONE. 2016;11(1):e0147601.
Nliwasa M, MacPherson P, Gupta-Wright A, et al. High HIV and active tuberculosis prevalence and increased mortality risk in adults with symptoms of TB: a systematic review and meta-analyses. J Int AIDS Soc. 2018;21(7):e25162.
Barendregt JJ, Doi SA, Lee YY, Norman RE, Vos T. Meta-analysis of prevalence. J Epidemiol Community Health. 2013:jech-2013-203104.
Higgins J, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58.
Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.
Hampel FR, Ronchetti EM, Rousseeuw PJ, Stahel WA. Robust statistics: the approach based on influence functions, vol. 114. New York: Wiley; 2011.
Sutton AJ, Abrams KR, Jones DR, Jones DR, Sheldon TA, Song F. Methods for meta-analysis in medical research. Chichester: Wiley; 2000.
Sterne JA, Egger M, Smith GD. Systematic reviews in health care: investigating and dealing with publication and other biases in meta-analysis. Br Med J. 2001;323(7304):101.
Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.
UNAIDS. AIDS data; 2017. http://www.unaids.org/en/resources/aids_data. Accessed 24 Oct 2017.
UN. Millennium Development Goals database; 2017. https://data.worldbank.org/data-catalog/millennium-development-indicators. Accessed 24 Oct 2017.
Viechtbauer W. Conducting meta-analyses in R with the metafor package. J Stat Softw. 2010;36(3):1–48.
Hailu K, Debrework Z, Bekure D, et al. The prevalence of HIV-1 antibodies in 106 tuberculosis patients. Ethiop J Health Dev. 1990;4(2):197–200.
De Cock KM, Gnaore E, Adjorlolo G, et al. Risk of tuberculosis in patients with HIV-I and HIV-II infections in Abidjan. Ivory Coast. BMJ. 1991;302(6775):496–9.
Migliori GB, Borghesi A, Adriko C, et al. Tuberculosis and HIV infection association in a rural district of northern Uganda: epidemiological and clinical considerations. Tuber Lung Dis. 1992;73(5):285–90.
Pozniak AL, MacLeod GA, Mahari M, Legg W, Weinberg J. The influence of HIV status on single and multiple drug reactions to antituberculous therapy in Africa. Aids. 1992;6(8):809–14.
Chintu C, Bhat G, Luo C, et al. Seroprevalence of human immunodeficiency virus type 1 infection in Zambian children with tuberculosis. Pediatr Infect Dis J. 1993;12(6):499–504.
Nunn P, Gathua S, Kibuga D, et al. The impact of HIV on resource utilization by patients with tuberculosis in a tertiary referral hospital, Nairobi, Kenya. Tuber Lung Dis. 1993;74(4):273–9.
Van den Broek J, Borgdorff M, Pakker N, et al. HIV-1 infection as a risk factor for the development of tuberculosis: a case–control study in Tanzania. Int J Epidemiol. 1993;22(6):1159–65.
Houston S, Ray S, Mahari M, et al. The association of tuberculosis and HIV infection in Harare, Zimbabwe. Tuber Lung Dis. 1994;75(3):220–6.
Luo C, Chintu C, Bhat G, et al. Human immunodeficiency virus type-1 infection in zambian children with tuberculosis: changing seroprevalance and evaluation of a thioacetazone-free regimen. Tuber Lung Dis. 1994;75(2):110–5.
Sassan-Morokro M, De Cock KM, Ackah A, et al. Tuberculosis and HIV infection in children in Abidjan, Cote d’Ivoire. Trans R Soc Trop Med Hyg. 1994;88(2):178–81.
Richards SB, St Louis ME, Nieburg P, et al. Impact of the HIV epidemic on trends in tuberculosis in Abidjan, Cote d’Ivoire. Tuber Lung Dis. 1995;76(1):11–6.
van Cleeff MR, Chum HJ. The proportion of tuberculosis cases in Tanzania attributable to human immunodeficiency virus. Int J Epidemiol. 1995;24(3):637–42.
Chum HJ, O’brien RJ, Chonde TM, Graf P, Rieder HL. An epidemiological study of tuberculosis and HIV infection in Tanzania, 1991–1993. AIDS. 1996;10(3):299–310.
Malkin JE, Prazuck T, Simonnet F, et al. Tuberculosis and human immunodeficiency virus infection in west Burkina Faso: clinical presentation and clinical evolution. Int J Tuberc Lung Dis. 1997;1(1):68–74.
Colvin M, Karim Abdool SS. HIV infection among patients with tuberculosis in KwaZulu/Natal, South Africa. Int J Tuberc Lung Dis. 1998;2(2):172.
Karstaedt AS, Jones N, Khoosal M, Crewe-Brown HH. The bacteriology of pulmonary tuberculosis in a population with high human immunodeficiency virus seroprevalence. Int J Tuberc Lung Dis. 1998;2(4):312–6.
Churchyard GJ, Kleinschmidt I, Corbett EL, Mulder D, De Cock KM. Mycobacterial disease in South African gold miners in the era of HIV infection. Int J Tuberc Lung Dis. 1999;3(9):791–8.
Onipede A, Idigbe O, Ako-Nai A, et al. Sero-prevalence of HIV antibodies in tuberculosis patients in Ile-Ife, Nigeria. East Afr Med J. 1999;76(3):127–32.
Demissie M, Lindtjørn B, Tegbaru B. Human Immunodeficiency virus (HIV) infection in tuberculosis patients in Addis Ababa. Ethiop J Health Dev. 2000;14(3):277–82.
Madhi SA, Huebner RE, Doedens L, Aduc T, Wesley D, Cooper PA. HIV-1 co-infection in children hospitalised with tuberculosis in South Africa. Int J Tuberc Lung Dis. 2000;4(5):448–54.
Kiwanuka J, Graham SM, Coulter JB, et al. Diagnosis of pulmonary tuberculosis in children in an HIV-endemic area, Malawi. Ann Trop Paediatr. 2001;21(1):5–14.
Range N, Ipuge YA, O’Brien RJ, et al. Trend in HIV prevalence among tuberculosis patients in Tanzania, 1991–1998. Int J Tuberc Lung Dis. 2001;5(5):405–12.
Bruchfeld J, Aderaye G, Palme IB, et al. Evaluation of outpatients with suspected pulmonary tuberculosis in a high HIV prevalence setting in Ethiopia: clinical, diagnostic and epidemiological characteristics. Scand J Infect Dis. 2002;34(5):331–7.
Moses A, Adelowo K, Ajayi B. Prevalence of HIV-1 infection among patients with leprosy and pulmonary tuberculosis in a semi-arid region, Nigeria. J R Soc Promot Health. 2003;123(2):117–9.
Odaibo GN, Gboun MF, Ekanem EE, et al. HIV infection among patients with pulmonary tuberculosis in Nigeria. Afr J Med Med Sci. 2006;35(Suppl):93–8.
Gellete A, Kebede D, Berhane Y. Tuberculosis and HIV infection in southern Ethiopia. Ethiop J Health Dev. 2017;11(1):51–9.
Daniel O, Salako A, Oluwole F, Alausa O, Oladapo O. HIV sero-prevalence among newly diagnosed adult pulmonary tuberculosis patients in Sagamu. Niger J Med. 2004;13(4):393.
Yassin MA, Takele L, Gebresenbet S, et al. HIV and tuberculosis coinfection in the southern region of Ethiopia: a prospective epidemiological study. Scand J Infect Dis. 2004;36(9):670–3.
Daniel O, Ogunfowora O, Oladapo O. HIV and tuberculosis co-infection in children: presentation and treatment outcome. Niger J Paediatr. 2005;32(4):83–7.
Ige OM, Sogaolu OM, Ogunlade OA. Pattern of presentation of tuberculosis and the hospital prevalence of tuberculosis and HIVco-infection in University College Hospital, Ibadan: a review of five years (1998–2002). Afr J Med Med Sci. 2005;34(4):329–33.
Adjei AA, Adiku TK, Ayeh-Kumi PF, Hesse IF. Prevalence of human immunodeficiency virus infection among tuberculosis suspect patients in Accra, Ghana. West Afr J Med. 2006;25(1):38–41.
Salami AK, Katibi IA. Human immunodeficiency virus-associated tuberculosis: pattern and trend in the University of Ilorin Teaching Hospital. Afr J Med Med Sci. 2006;35(4):457–60.
Daniel OJ, Ogunfowora OB, Oladapo OT. HIV sero-prevalence among children diagnosed with TB in Nigeria. Trop Doct. 2007;37(4):268–9.
Kassu A, Mengistu G, Ayele B, et al. HIV and intestinal parasites in adult TB patients in a teaching hospital in Northwest Ethiopia. Trop Doct. 2007;37(4):222–4.
Range N, Magnussen P, Mugomela A, et al. HIV and parasitic co-infections in tuberculosis patients: a cross-sectional study in Mwanza, Tanzania. Ann Trop Med Parasitol. 2007;101(4):343–51.
van der Werf MJ, Sebhatu M, Weldegergis T, Tesfazion A, Borgdorff MW. TB-HIV co-infection in Eritrea. Int J Tuberc Lung Dis. 2007;11(7):823–6.
Chakaya J, Uplekar M, Mansoer J, et al. Public-private mix for control of tuberculosis and TB-HIV in Nairobi, Kenya: outcomes, opportunities and obstacles. Int J Tuberc Lung Dis. 2008;12(11):1274–8.
Datiko DG, Yassin MA, Chekol LT, Kabeto LE, Lindtjorn B. The rate of TB-HIV co-infection depends on the prevalence of HIV infection in a community. BMC Public Health. 2008;8:266.
Mwinga A, Mwananyambe N, Kanene C, et al. Provider-initiated HIV testing and counseling of TB patients—Livingstone District, Zambia, September 2004–December 2006. MMWR Morb Mortal Wkly Rep. 2008;57(11):285–9.
Odhiambo J, Kizito W, Njoroge A, et al. Provider-initiated HIV testing and counselling for TB patients and suspects in Nairobi, Kenya. Int J Tuberc Lung Dis. 2008;12(3 Suppl 1):63–8.
Sume GE, Etogo D, Kabore S, Gnigninanjouena O, Epome SS, Metchendje JN. Seroprevalence of human immunodeficiency virus infection among tuberculosis patients in the Nylon district hospital tuberculosis treatment centre. East Afr Med J. 2008;85(11):529–36.
Ayenew A, Leykun A, Colebunders R, Deribew A. Predictors of HIV testing among patients with tuberculosis in North West Ethiopia: a case–control study. PLoS ONE. 2010;5(3):e9702.
Erhabor O, Jeremiah Z, Adias T, Okere C. The prevalence of human immunodeficiency virus infection among TB patients in Port Harcourt Nigeria. HIV/AIDS (Auckland, NZ). 2010;2:1.
Pennap G, Makpa S, Ogbu S. Sero-prevalence of HIV infection among tuberculosis patients in a rural tuberculosis referral clinic in northern nigeria. Pan Afr Med J. 2010;5:22.
Dagnra A, Adjoh K, Tchaptchet HS, et al. Prevalence of HIV-TB co-infection and impact of HIV infection on pulmonary tuberculosis outcome in Togo. Bull Soc Pathol Exot. 2011;104(5):342–6.
Kamenju P, Aboud S. Tuberculosis-HIV co-infection among patients admitted at Muhimbili National hospital in Dar es salaam, Tanzania. J Health Res. 2011;13(1):25–31.
Ligidi T, Gebre-Selassie S, Tsegaye A. The immunological status of newly diagnosed tuberculosis patients co-infected with human immunodeficiency virus-1 in Adama Hospital, Ethiopia. Ethiop Med J. 2011;49(2):75–83.
van’t Hoog AH, Laserson KF, Githui WA, et al. High prevalence of pulmonary tuberculosis and inadequate case finding in rural western Kenya. Am J Respir Crit Care Med. 2011;183(9):1245–53.
Nyamogoba HDN, Mbuthia G, Mining S, et al. HIV co-infection with tuberculous and non-tuberculous mycobacteria in western Kenya: challenges in the diagnosis and management. Afr Health Sci. 2012;12(3):305–11.
Teklu T, Belyhun Y, Tesfaye S, Medhin G. Trends of tuberculosis and HIV infections between 2004 and 2008 in Wolaita Sodo, southern Ethiopia. Ethiop Med J. 2012;50(1):1–11.
Valadas E, Gomes A, Sutre A, et al. Tuberculosis with malaria or HIV co-infection in a large hospital in Luanda, Angola. J Infect Dev Ctries. 2013;7(3):269–72.
Kebede W, Keno F, Ewunetu T, Mamo G. Acceptance of provider initiated HIV testing and counseling among tuberculosis patients in East Wollega administrative zone, Oromia regional state, western Ethiopia. Tuberc Res Treat. 2014. https://doi.org/10.1155/2014/935713.
Keflie TS, Ameni G. Microscopic examination and smear negative pulmonary tuberculosis in Ethiopia. Pan Afr Med J. 2014;19:162.
Kishimba RS, Mghamba J, Mmbaga VM. Trend of HIV infection among pediatric tuberculosis patients in Tanzania, 2006-2010. Int J Infect Dis. 2014;21:125.
Mihret A, Bekele Y, Aytenew M, et al. Human immunodeficiency virus infection among new smear positive pulmonary tuberculosis patients in Addis Ababa, Ethiopia. Ethiop Med J. 2014;2014(Suppl 1):1–6.
Belay M, Bjune G, Abebe F. Prevalence of tuberculosis, HIV, and TB-HIV co-infection among pulmonary tuberculosis suspects in a predominantly pastoralist area, northeast Ethiopia. Global Health Action. 2015;8:27949.
Namme LH, Marie-Solange D, Bertrand MNH, Elvis T, Achu JH, Christopher K. Extrapulmonary tuberculosis and HIV coinfection in patients treated for tuberculosis at the Douala General Hospital in Cameroon. Ann Trop Med Public Health. 2013;6(1):100.
Yadeta D, Alemseged F, Biadgilign S. Provider-initiated HIV testing and counseling among tuberculosis patients in a hospital in the Oromia region of Ethiopia. J Infect Public Health. 2013;6(3):222–9.
Denegetu AW, Dolamo BL. HIV screening among TB patients and co-trimoxazole preventive therapy for TB/HIV patients in Addis Ababa: facility based descriptive study. PLoS ONE. 2014;9(2):e86614.
Linguissi LS, Mayengue PI, Sidibe A, et al. Prevalence of national treatment algorithm defined smear positive pulmonary tuberculosis in HIV positive patients in Brazzaville, Republic of Congo. BMC Res Notes. 2014;7:578.
Gomerep SS, Eze UA, Chiegboka LO, et al. Sputum smear pattern among patients diagnosed with pulmonary tuberculosis in Makurdi, North Central Nigeria. Niger J Med. 2015;24(3):201–6.
Ojiezeh TI, Ogundipe OO, Adefosoye VA. A retrospective study on incidence of pulmonary tuberculosis and human immunodeficiency virus co-infection among patients attending National Tuberculosis and Leprosy Control Programme, Owo centre. Pan Afr Med J. 2015;20:345.
Gebrecherkos T, Gelaw B, Tessema B. Smear positive pulmonary tuberculosis and HIV co-infection in prison settings of North Gondar Zone, Northwest Ethiopia. BMC Public Health. 2016;16(1):1091.
Ranti KO, Glory AO, Victoria BT, Isaac KO. Prevalence of HIV infection among tuberculosis patients in a teaching hospital in south-west Nigeria: a four-year retrospective study. HIV Rev. 2016;15(4):136–40.
Tarekegne D, Jemal M, Atanaw T, et al. Prevalence of human immunodeficiency virus infection in a cohort of tuberculosis patients at Metema Hospital, Northwest Ethiopia: a 3 years retrospective study. BMC Res Notes. 2016;9(1):192.
Chanda-Kapata P, Kapata N, Klinkenberg E, Grobusch MP, Cobelens F. The prevalence of HIV among adults with pulmonary TB at a population level in Zambia. BMC Infect Dis. 2017;17(1):236.
Chinedu K, Takim AE, Obeagu EI, Chinazor UD, Eloghosa O, Ojong OE. HIV and TB co-infection among patients who used Directly Observed Treatment Short-course centres in Yenagoa, Nigeria. IOSR J Pharm Biol Sci. 2017;12(4):70–5.
Osei E, Der J, Owusu R, Kofie P, Axame WK. The burden of HIV on tuberculosis patients in the Volta region of Ghana from 2012 to 2015: implication for tuberculosis control. BMC Infect Dis. 2017;17(1):504.
World Health Organization. Strategic framework to decrease the burden of TB/HIV. Geneva: World Health Organization; 2002.
MSF. Out of focus: how millions of people in West and Central Africa are being left out of the global HIV response; 2016.
World Health Organization. Global tuberculosis report 2016; 2016.
Uplekar M, Weil D, Lonnroth K, et al. WHO’s new end TB strategy. Lancet. 2015;385(9979):1799–801.
UNAIDS, Fast-track. Ending the AIDS epidemic by 2030. UNAIDS, Geneva. 2014.
Medecins Sans Frontires. How millions of people in west and central Africa are being left out of the global HIV response: MSF; 2016.
Harries AD, Boxshall M, Phiri S, Kwanjana J. Managing HIV and tuberculosis in sub-Saharan Africa. Lancet. 2006;367(9525):1817–8.
Acknowledgements
YG is supported by University of Queensland International Scholarship (UQI). We thank Mr. Scott Macintyre for his professional support during electronic database search.
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YAG, YA, GW and RSM conceived the research question and study design. YAG performed the electronic database search, data abstraction, analysis and wrote the first draft of the article. YAG supervised and reviewed the database search, data analysis and interpretation. GW, CG, RSM and HG supervised the research process and provided comments. All authors reviewed subsequent versions and approved the final version of the manuscript.
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Gelaw, Y.A., Williams, G., Soares Magalhães, R.J. et al. HIV Prevalence Among Tuberculosis Patients in Sub-Saharan Africa: A Systematic Review and Meta-analysis. AIDS Behav 23, 1561–1575 (2019). https://doi.org/10.1007/s10461-018-02386-4
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DOI: https://doi.org/10.1007/s10461-018-02386-4