Sustained high fatality during TB therapy amid rapid decline in TB mortality at population level: A retrospective cohort and ecological analysis from Shiselweni, Eswatini.

HIV TB-related deaths population-level trends

Journal

Tropical medicine & international health : TM & IH
ISSN: 1365-3156
Titre abrégé: Trop Med Int Health
Pays: England
ID NLM: 9610576

Informations de publication

Date de publication:
15 Dec 2023
Historique:
medline: 15 12 2023
pubmed: 15 12 2023
entrez: 15 12 2023
Statut: aheadofprint

Résumé

Despite declining TB notifications in Southern Africa, TB-related deaths remain high. We describe patient- and population-level trends in TB-related deaths in Eswatini over a period of 11 years. Patient-level (retrospective cohort, from 2009 to 2019) and population-level (ecological analysis, 2009-2017) predictors and rates of TB-related deaths were analysed in HIV-negative and HIV-coinfected first-line TB treatment cases and the population of the Shiselweni region. Patient-level TB treatment data, and population and HIV prevalence estimates were combined to obtain stratified annual mortality rates. Multivariable Poisson regressions models were fitted to identify patient-level and population-level predictors of deaths. Of 11,883 TB treatment cases, 1302 (11.0%) patients died during treatment: 210/2798 (7.5%) HIV-negative patients, 984/8443 (11.7%) people living with HIV (PLHIV), and 108/642 (16.8%) patients with unknown HIV-status. The treatment case fatality ratio remained above 10% in most years. At patient-level, fatality risk was higher in PLHIV (aRR 1.74, 1.51-2.02), and for older age and extra-pulmonary TB irrespective of HIV-status. For PLHIV, fatality risk was higher for TB retreatment cases (aRR 1.38, 1.18-1.61) and patients without antiretroviral therapy (aRR 1.70, 1.47-1.97). It decreases with increasing higher CD4 strata and the programmatic availability of TB-LAM testing (aRR 0.65, 0.35-0.90). At population-level, mortality rates decreased 6.4-fold (-147/100,000 population) between 2009 (174/100,000) and 2017 (27/100,000), coinciding with a decline in TB treatment cases (2785 in 2009 to 497 in 2017). Although the absolute decline in mortality rates was most pronounced in PLHIV (-826/100,000 vs. HIV-negative: -23/100,000), the relative population-level mortality risk remained higher in PLHIV (aRR 4.68, 3.25-6.72) compared to the HIV-negative population. TB-related mortality rapidly decreased at population-level and most pronounced in PLHIV. However, case fatality among TB treatment cases remained high. Further strategies to reduce active TB disease and introduce improved TB therapies are warranted.

Identifiants

pubmed: 38100203
doi: 10.1111/tmi.13961
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023 The Authors Tropical Medicine & International Health Published by John Wiley & Sons Ltd.

Références

WHO. Global tuberculosis report. Geneva, Switzerland: World Health Organization; 2020. p. 2020.
Corbett EL, Marston B, Churchyard GJ, Cock KMD. Tuberculosis in sub-Saharan Africa: opportunities, challenges, and change in the era of antiretroviral treatment. Lancet. 2006;367(9514):926-937.
Lawn SD, Wood R, De Cock KM, Kranzer K, Lewis JJ, Churchyard GJ. Antiretrovirals and isoniazid preventive therapy in the prevention of HIV-associated tuberculosis in settings with limited health-care resources. Lancet Infect Dis. 2010;10(7):489-498.
Gupta A, Wood R, Kaplan R, Bekker LG, Lawn SD. Tuberculosis incidence rates during 8 years of follow-up of an antiretroviral treatment cohort in South Africa: comparison with rates in the community. PLoS One. 2012;7(3):e34156. https://doi.org/10.1371/journal.pone.0034156
Bruchfeld J, Correia-Neves M, Källenius G. Tuberculosis and HIV coinfection. Cold Spring Harb Perspect Med. 2015;5(7):a017871. https://doi.org/10.1101/cshperspect.a017871
Lawn SD, Harries AD, Meintjes G, Getahun H, Havlir DV, Wood R. Reducing deaths from tuberculosis in antiretroviral treatment programmes in sub-Saharan Africa. AIDS Lond Engl. 2012;26(17):2121-2133.
García-Basteiro AL, DiNardo A, Saavedra B, Silva DR, Palmero D, Gegia M, et al. Point of care diagnostics for tuberculosis. Pulmonology. 2018;24(2):73-85.
Bulterys MA, Wagner B, Redard-Jacot M, Suresh A, Pollock NR, Moreau E, et al. Point-of-care urine LAM tests for tuberculosis diagnosis: a status update. J Clin Med. 2020;9(1):111.
Cox HS, Mbhele S, Mohess N, Whitelaw A, Muller O, Zemanay W, et al. Impact of Xpert MTB/RIF for TB diagnosis in a primary care clinic with high TB and HIV prevalence in South Africa: a pragmatic randomised trial. PLoS Med. 2014;11(11):e1001760. https://doi.org/10.1371/journal.pmed.1001760
Suthar AB, Rutherford GW, Horvath T, Doherty MC, Negussie EK. Improving antiretroviral therapy scale-up and effectiveness through service integration and decentralization. AIDS. 2014;28(Suppl 2):S175-S185.
Manosuthi W, Wiboonchutikul S, Sungkanuparph S. Integrated therapy for HIV and tuberculosis. AIDS Res Ther. 2016;13:22. https://doi.org/10.1186/s12981-016-0106-y
Gilbert JA, Long EF, Brooks RP, Friedland GH, Moll AP, Townsend JP, et al. Integrating community-based interventions to reverse the convergent TB/HIV epidemics in rural South Africa. PLoS One. 2015;10(5):e0126267. https://doi.org/10.1371/journal.pone.0126267
Haumba S, Dlamini T, Calnan M, Ghazaryan V, Smith-Arthur AE, Preko P, et al. Declining tuberculosis notification trend associated with strengthened TB and expanded HIV care in Swaziland. Public Health Action. 2015;5(2):103-105.
Kerschberger B, Schomaker M, Telnov A, Vambe D, Kisyeri N, Sikhondze W, et al. Decreased risk of HIV-associated TB during antiretroviral therapy expansion in rural Eswatini from 2009 to 2016: a cohort and population-based analysis. Trop Med Int Health. 2019;24(9):1114-1127.
Mchunu G, van Griensven J, Hinderaker SG, Kizito W, Sikhondze W, Manzi M, et al. High mortality in tuberculosis patients despite HIV interventions in Swaziland. Public Health Action. 2016;6(2):105-110.
WHO. The end TB strategy. Geneva, Switzerland: World Health Organization; 2015.
Ministry of Health. TB program annual report. Mbabane: Ministry of Health; 2012. p. 2013.
Ministry of Health of Swaziland. 2017 annual TB program report. Mbabane: Ministry of Health of Swaziland; 2018.
World Health Organization. Global tuberculosis report 2013. Geneva, Switzerland: World Health Organization; 2013.
Central Statistical Office of Eswatini. The 2017 population and housing census preliminary results. Mbabane, Eswatini: Central Statistical Office of Eswatini; 2017.
Ministry of Health of Eswatini. Swaziland HIV incidence measurement survey 2 (SHIMS2) 2016-2017. Final Report. Mbabane, Eswatini: Ministry of Health of Eswatini; 2019.
Kerschberger B, Schomaker M, Ciglenecki I, Pasipamire L, Mabhena E, Telnov A, et al. Programmatic outcomes and impact of rapid public sector antiretroviral therapy expansion in adults prior to introduction of the WHO treat-all approach in rural Eswatini. Trop Med Int Health. 2019;24(6):701-714.
Kerschberger B, Jobanputra K, Schomaker M, Kabore SM, Teck R, Mabhena E, et al. Feasibility of antiretroviral therapy initiation under the treat-all policy under routine conditions: a prospective cohort study from Eswatini. J Int AIDS Soc. 2019;22(10):e25401.
World Health Organization. Definitions and reporting framework for tuberculosis-2013 revision: updated December 2014 and January 2020 [Internet]. Définitions et cadre de notification pour la tuberculose-révision 2013. Geneva: World Health Organization; 2013.
Central Statistical Office (CSO). 2007 Swaziland population census. Mbabane: Central Statistical Office (CSO); 2009.
Central Statistical Office (CSO). The 2017 population and housing census - Prelimiary results. Mbabane, Eswatini: Central Statistical Office (CSO); 2017.
Central Statistical Office (CSO). Swaziland demographic and health survey 2006-2007. Mbabane, Swaziland: Central Statistical Office; 2007.
Swaziland Ministry of Health. Swaziland HIV Incidence Measurement Survey (SHIMS). First findings report. Mbabane, Swaziland: Swaziland Ministry of Health; 2012.
Blaizot S, Riche B, Ecochard R. Potential impact of multiple interventions on HIV incidence in a hyperendemic region in Western Kenya: a modelling study. Lyon, France: Epicentre, Médecins Sans Frontières; 2016.
Heunis JC, Kigozi NG, Chikobvu P, Botha S, van Rensburg HD. Risk factors for mortality in TB patients: a 10-year electronic record review in a South African province. BMC Public Health. 2017;17(1):38.
de Albuquerque Mde F, Ximenes RA, Lucena-Silva N, de Souza WV, Dantas AT, Dantas OM, et al. Factors associated with treatment failure, dropout, and death in a cohort of tuberculosis patients in Recife, Pernambuco state, Brazil. Cad Saude Publica. 2007;23(7):1573-1582.
Vree M, Huong NT, Duong BD, Sy DN, Van LN, Co NV, et al. Mortality and failure among tuberculosis patients who did not complete treatment in Vietnam: a cohort study. BMC Public Health. 2007;7(1):134.
Low S, Ang LW, Cutter J, James L, Chee CB, Wang YT, et al. Mortality among tuberculosis patients on treatment in Singapore. Int J Tuberc Lung Dis. 2009;13(3):328-334.
Lefebvre N, Falzon D. Risk factors for death among tuberculosis cases: analysis of European surveillance data. Eur Respir J. 2008;31(6):1256-1260.
Cj W, Sb S. A systematic review of risk factors for death in adults during and after tuberculosis treatment. Int J Tuberc Lung Dis. 2011;15(7):871-885.
Sanchez-Padilla E, Dlamini T, Ascorra A, Rusch-Gerdes S, Tefera ZD, Calain P, et al. High prevalence of multidrug-resistant tuberculosis, Swaziland, 2009-2010. Emerg Infect Dis. 2012;18(1):29-37.
Sanchez-Padilla E, Merker M, Beckert P, Jochims F, Dlamini T, Kahn P, et al. Detection of drug-resistant tuberculosis by Xpert MTB/RIF in Swaziland. N Engl J Med. 2015;372(12):1181-1182.
Beckert P, Sanchez-Padilla E, Merker M, Dreyer V, Kohl TA, Utpatel C, et al. Tuberculosis outbreak clone in Eswatini missed by Xpert has elevated bedaquiline resistance dated to the pre-treatment era. Genome Med. 2020;12(1):104.
Steingart KR, Schiller I, Horne DJ, Pai M, Boehme CC, Dendukuri N. Xpert® Mtb/Rif assay for pulmonary tuberculosis and rifampicin resistance in adults. Cochrane Database Syst Rev. 2014;1:1-166.
Horne DJ, Kohli M, Zifodya JS, Schiller I, Dendukuri N, Tollefson D, et al. Xpert MTB/RIF and Xpert MTB/RIF ultra for pulmonary tuberculosis and rifampicin resistance in adults. Cochrane Database Syst Rev. 2019;6:CD009593.
Mathabire Rucker SC, Cossa L, Harrison RE, Mpunga J, Lobo S, Kisaka Kimupelenge P, et al. Feasibility of using Determine TB-LAM to diagnose tuberculosis in HIV-positive patients in programmatic conditions: a multisite study. Glob Health Action. 2019;12:1672366. https://doi.org/10.1080/16549716.2019.1672366
Yoon C, Semitala FC, Asege L, Katende J, Mwebe S, Andama AO, et al. Yield and efficiency of novel intensified tuberculosis case-finding algorithms for people living with HIV. Am J Respir Crit Care Med. 2019;199(5):643-650.
Theron G, Zijenah L, Chanda D, Clowes P, Rachow A, Lesosky M, et al. Feasibility, accuracy, and clinical effect of point-of-care Xpert MTB/RIF testing for tuberculosis in primary-care settings in Africa: a multicentre, randomised, controlled trial. Lancet Lond Engl. 2014;383(9915):424-435.
Di Tanna GL, Khaki AR, Theron G, McCarthy K, Cox H, Mupfumi L, et al. Effect of Xpert MTB/RIF on clinical outcomes in routine care settings: individual patient data meta-analysis. Lancet Glob Health. 2019;7(2):e191-e199.
Bjerrum S, Schiller I, Dendukuri N, Kohli M, Nathavitharana RR, Zwerling AA, et al. Lateral flow urine lipoarabinomannan assay for detecting active tuberculosis in people living with HIV. Cochrane Database Syst Rev. 2019;10(10):CD011420. https://doi.org/10.1002/14651858.CD011420.pub3
Ricks S, Denkinger CM, Schumacher SG, Hallett TB, Arinaminpathy N. The potential impact of urine-LAM diagnostics on tuberculosis incidence and mortality: a modelling analysis. PLoS Med. 2020;17(12):e0230808. https://doi.org/10.1371/journal.pone.0230808
Kanyerere H, Mganga A, Harries AD, Tayler-Smith K, Jahn A, Chimbwandira FM, et al. Decline in national tuberculosis notifications with national scale-up of antiretroviral therapy in Malawi. Public Health Action. 2014;4(2):113-115.
Zachariah R, Bemelmans M, Akesson A, Gomani P, Phiri K, Isake B, et al. Reduced tuberculosis case notification associated with scaling up antiretroviral treatment in rural Malawi. Int J Tuberc Lung Dis. 2011;15(7):933-937.
Hermans S, Boulle A, Caldwell J, Pienaar D, Wood R. Temporal trends in TB notification rates during ART scale-up in Cape Town: an ecological analysis. J Int AIDS Soc. 2015;18(1):20240. https://doi.org/10.7448/IAS.18.1.20240
Neyrolles O, Quintana-Murci L. Sexual inequality in tuberculosis. PLoS Med. 2009;6(12):e1000199. https://doi.org/10.1371/journal.pmed.1000199
Horton KC, MacPherson P, Houben RMGJ, White RG, Corbett EL. Sex differences in tuberculosis burden and notifications in low- and middle-income countries: a systematic review and meta-analysis. PLoS Med. 2016;13(9):e1002119.
Hermans S, Horsburgh CR Jr, Wood R. A century of tuberculosis epidemiology in the northern and southern hemisphere: the differential impact of control interventions. PLoS One. 2015;10(8):e0135179. https://doi.org/10.1371/journal.pone.0135179
MacPherson P, Houben RM, Glynn JR, Corbett EL, Kranzer K. Pre-treatment loss to follow-up in tuberculosis patients in low- and lower-middle-income countries and high-burden countries: a systematic review and meta-analysis. Bull World Health Organ. 2014;92(2):126-138.
Hermans S, Cornell M, Middelkoop K, Wood R. The differential impact of HIV and antiretroviral therapy on gender-specific tuberculosis rates. Trop Med Int Health. 2019;24(4):454-462.
WHO. Global tuberculosis report 2018. Geneva, Switzerland: World Health Organization; 2018.
Sterne JAC, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, et al. Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ. 2009;338:b2393.
WHO. Improving the diagnosis and treatment of smear-negative pulmonary and extrapulmonary tuberculosis among adults and adolescents: recommendations for HIV-prevalent and resource-constrained settings. Geneva, Switzerland: World Health Organization; 2006.
Engelbrecht M, Heunis C, Kigozi G. The views of primary health care nurses on HIV counselling and testing for tuberculosis patients in two districts of the Free State Province in South Africa. Afr J Nurs Midwifery. 2008;10(2):70-83.
Ramírez S, Mejía F, Rojas M, Seas C, van der Stuyft P, Gotuzzo E, et al. HIV screening among newly diagnosed TB patients: a cross sectional study in Lima, Peru. BMC Infect Dis. 2018;18(1):136.
Ngari MM, Rashid MA, Sanga D, Mathenge H, Agoro O, Mberia JK, et al. Burden of HIV and treatment outcomes among TB patients in rural Kenya: a 9-year longitudinal study. BMC Infect Dis. 2023;23(1):362.
Gebremariam G, Asmamaw G, Hussen M, Hailemariam MZ, Asegu D, Astatkie A, et al. Impact of HIV status on treatment outcome of tuberculosis patients registered at Arsi Negele health center, Southern Ethiopia: a six year retrospective study. PloS One. 2016;11(4):e0153239.

Auteurs

Bernhard Kerschberger (B)

Médecins sans Frontières, Mbabane, Eswatini.
Médecins sans Frontières/Ärzte ohne Grenzen, Vienna Evaluation Unit, Vienna, Austria.

Debrah Vambe (D)

National TB Control Programme (NTCP), Manzini, Eswatini.

Michael Schomaker (M)

Centre for Infectious Disease Epidemiology and Research, School of Public Health and Family Medicine, University of Cape Town, Cape Town, South Africa.
Department of Statistics, Ludwig-Maximilians University Munich, Munich, Germany.

Edwin Mabhena (E)

Médecins sans Frontières, Mbabane, Eswatini.

Michelle Daka (M)

Médecins sans Frontières, Mbabane, Eswatini.

Themba Dlamini (T)

National TB Control Programme (NTCP), Manzini, Eswatini.

Siphiwe Ngwenya (S)

National TB Control Programme (NTCP), Manzini, Eswatini.

Bheki Mamba (B)

National TB Control Programme (NTCP), Manzini, Eswatini.

Bongekile Nxumalo (B)

National TB Control Programme (NTCP), Manzini, Eswatini.

Joyce Sibanda (J)

National TB Control Programme (NTCP), Manzini, Eswatini.

Sisi Dube (S)

National TB Control Programme (NTCP), Manzini, Eswatini.

Lindiwe Mdluli Dlamini (LM)

National TB Control Programme (NTCP), Manzini, Eswatini.

Esther Mukooza (E)

Médecins sans Frontières, Mbabane, Eswatini.

Tom Ellman (T)

Médecins sans Frontières, Cape Town, South Africa.

Iza Ciglenecki (I)

Médecins sans Frontières, Geneva, Switzerland.

Classifications MeSH