Prevalence and Predictors of Tuberculosis Infection in Children and Adolescents in Rural Uganda: A Cross-sectional Study.


Journal

The Pediatric infectious disease journal
ISSN: 1532-0987
Titre abrégé: Pediatr Infect Dis J
Pays: United States
ID NLM: 8701858

Informations de publication

Date de publication:
15 Jul 2024
Historique:
medline: 17 7 2024
pubmed: 17 7 2024
entrez: 17 7 2024
Statut: aheadofprint

Résumé

Much of the latent tuberculosis (TB) reservoir is established in childhood and adolescence. Yet, age-specific data on prevalence and predictors of infection in this population are sparse and needed to guide prevention and case finding. From December 2021 to June 2023, we measured TB infection in children 1-17 years in 25 villages in rural Southwestern Uganda. We defined TB infection as a positive QuantiFERON Gold Plus Test (QFT). We estimated overall and age-stratified population-level prevalence and adjusted risk ratios (aRR) of TB infection for individual, household, and community-based predictors, accounting for age, TB contact, and clustering by household. Estimated TB infection prevalence was 9.6% [95% confidence interval (CI): 8.7-10.5%] among the 5789 participants, and prevalence varied slightly with age. Household-level risk factors included crowding (aRR: 1.25, 95% CI: 1.03-1.53), indoor cooking (aRR: 1.62, 95% CI: 1.14-2.30), living with ≥2 persons who drink alcohol (aRR: 1.47, 95% CI: 1.04-2.07). The predominant community-based risk factor was child mobility (aRR: 1.67, 95% CI: 1.24-2.26). In age-stratified analyses, household predictors were important in early childhood but not adolescence, where mobility was predominant (aRR: 1.66, 95% CI: 1.13-2.44). We detected a high prevalence of TB infection in children and adolescents in rural Uganda. On a population level, TB risk factors change throughout the early life course, with child mobility a key risk factor in adolescence. Age-specific TB case finding and prevention strategies that address both household and extra-household risk factors are needed to address TB transmission.

Sections du résumé

BACKGROUND BACKGROUND
Much of the latent tuberculosis (TB) reservoir is established in childhood and adolescence. Yet, age-specific data on prevalence and predictors of infection in this population are sparse and needed to guide prevention and case finding.
METHODS METHODS
From December 2021 to June 2023, we measured TB infection in children 1-17 years in 25 villages in rural Southwestern Uganda. We defined TB infection as a positive QuantiFERON Gold Plus Test (QFT). We estimated overall and age-stratified population-level prevalence and adjusted risk ratios (aRR) of TB infection for individual, household, and community-based predictors, accounting for age, TB contact, and clustering by household.
RESULTS RESULTS
Estimated TB infection prevalence was 9.6% [95% confidence interval (CI): 8.7-10.5%] among the 5789 participants, and prevalence varied slightly with age. Household-level risk factors included crowding (aRR: 1.25, 95% CI: 1.03-1.53), indoor cooking (aRR: 1.62, 95% CI: 1.14-2.30), living with ≥2 persons who drink alcohol (aRR: 1.47, 95% CI: 1.04-2.07). The predominant community-based risk factor was child mobility (aRR: 1.67, 95% CI: 1.24-2.26). In age-stratified analyses, household predictors were important in early childhood but not adolescence, where mobility was predominant (aRR: 1.66, 95% CI: 1.13-2.44).
CONCLUSION CONCLUSIONS
We detected a high prevalence of TB infection in children and adolescents in rural Uganda. On a population level, TB risk factors change throughout the early life course, with child mobility a key risk factor in adolescence. Age-specific TB case finding and prevention strategies that address both household and extra-household risk factors are needed to address TB transmission.

Identifiants

pubmed: 39018476
doi: 10.1097/INF.0000000000004475
pii: 00006454-990000000-00946
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Institutes of Allergy and Infectious Diseases of the National Institute of Health
ID : R01AI151209

Informations de copyright

Copyright © 2024 Wolters Kluwer Health, Inc. All rights reserved.

Déclaration de conflit d'intérêts

The authors have no conflicts of interest to disclose.

Références

Global Tuberculosis Report 2022. Available at: https://www.who.int/teams/global-tuberculosis-programme/tb-reports/global-tuberculosis-report-2022. Accessed December 16, 2022.
Snow KJ, Cruz AT, Seddon JA, et al. The incidence of tuberculosis among adolescents and young adults: a global estimate. Lancet Child Adolesc Health. 2020;4:68–79.
Dodd PJ, Gardiner E, Coghlan R, et al. Burden of childhood tuberculosis in 22 high-burden countries: a mathematical modelling study. Lancet Glob Health. 2014;2:e453–e459.
Andrews JR, Morrow C, Walensky RP, et al. Integrating social contact and environmental data in evaluating tuberculosis transmission in a South African township. J Infect Dis. 2014;210:597–603.
Johnstone-Robertson SP, Mark D, Morrow C, et al. Social mixing patterns within a South African township community: implications for respiratory disease transmission and control. Am J Epidemiol. 2011;174:1246–1255.
Martinez L, Shen Y, Mupere E, et al. Transmission of mycobacterium tuberculosis in households and the community: a systematic review and meta-analysis. Am J Epidemiol. 2017;185:1327–1339.
Martinez L, Lo NC, Cords O, et al. Paediatric tuberculosis transmission outside the household: challenging historical paradigms to inform future public health strategies. Lancet Respir Med. 2019;7:544–552.
WHO consolidated guidelines on tuberculosis Module 2: Screening – Systematic screening for tuberculosis disease. 2022. Available at: https://www.who.int/publications-detail-redirect/9789240022676. Accessed July 22, 2022.
Balen J, McManus DP, Li Y-S, et al. Comparison of two approaches for measuring household wealth via an asset-based index in rural and peri-urban settings of Hunan province, China. Emerg Themes Epidemiol. 2010;7:7.
Vyas S, Kumaranayake L. Constructing socio-economic status indices: how to use principal components analysis. Health Policy Plan. 2006;21:459–468.
Marquez C, Chamie G, Achan J, et al. Tuberculosis infection in early childhood and the association with HIV-exposure in HIV-uninfected children in rural Uganda. Pediatr Infect Dis J. 2016;35:524–529.
Cranmer LM, Kanyugo M, Jonnalagadda SR, et al. High prevalence of tuberculosis infection in HIV-1 exposed Kenyan infants. Pediatr Infect Dis J. 2014;33:401–406.
Mecha J, Escudero JN, Richardson BA, et al. Maternal HIV status and risk of infant mycobacterium tuberculosis infection as measured by tuberculin skin test. Pediatr Infect Dis J. 2023;43:250–256.
Qiagen. QuantiFERON-TB Gold Plus (QFT-Plus) Package Insert. Germantown, Maryland, USA; 2018.
Wikell A, Jonsson J, Dyrdak R, et al. The impact of borderline Quantiferon-TB gold plus results for latent tuberculosis screening under routine conditions in a low-endemicity setting. J Clin Microbiol. 2021;59:e0137021.
Jonsson J, Westman A, Bruchfeld J, et al. A borderline range for quantiferon gold in-tube results. PLoS One. 2017;12:e0187313.
Metcalfe JZ, Cattamanchi A, McCulloch CE, et al. Test variability of the QuantiFERON-TB gold in-tube assay in clinical practice. Am J Respir Crit Care Med. 2013;187:206–211.
Ringshausen FC, Nienhaus A, Schablon A, et al. Predictors of persistently positive Mycobacterium-tuberculosis-specific interferon-gamma responses in the serial testing of health care workers. BMC Infect Dis. 2010;10:220.
Andrews JR, Nemes E, Tameris M, et al. Serial QuantiFERON testing and tuberculosis disease risk among young children: an observational cohort study. Lancet Respir Med. 2017;5:282–290.
Ledesma JR, Ma J, Zheng P, et al. Interferon-gamma release assay levels and risk of progression to active tuberculosis: a systematic review and dose-response meta-regression analysis. BMC Infect Dis. 2021;21:467.
Balzer LB, van der Laan M, Ayieko J, et al. Two-Stage TMLE to reduce bias and improve efficiency in cluster randomized trials. Biostatistics. 2021;24:502–517.
van der Laan MJ, Polley EC, Hubbard AE. Super learner. Stat Appl Genet Mol Biol. 2007;6:Article25.
Marquez C, Atukunda M, Balzer LB, et al. The age-specific burden and household and school-based predictors of child and adolescent tuberculosis infection in rural Uganda. PLoS One. 2020;15:e0228102.
Jeremiah K, Lyimo E, Ritz C, et al. Prevalence of mycobacterium tuberculosis infection as measured by the QuantiFERON-TB Gold assay and ESAT-6 free IGRA among adolescents in Mwanza, Tanzania. PLoS One. 2021;16:e0252808.
Zanetti C, Peracchi M, Zorzi D, et al. Outbreak of transient conversions of the QuantiFERON-TB Gold In-Tube test in laboratory health care worker screenings. Clin Vaccine Immunol. 2012;19:954–960.
Andrews JR, Hatherill M, Mahomed H, et al. The dynamics of QuantiFERON-TB gold in-tube conversion and reversion in a cohort of South African adolescents. Am J Respir Crit Care Med. 2015;191:584–591.
Nygaard U, Poulsen A, Yde Nielsen A, et al. Borderline-positive quantiferon in children. Pediatr Infect Dis J. 2019;38:e307–e309.
World Health Organization. Global Tuberculosis Report, 2023. Available at: https://www.who.int/teams/global-tuberculosis-programme/tb-reports. Accessed March 29, 2024.
Puryear SB, Fatch R, Beesiga B, et al. Higher levels of alcohol use are associated with latent tuberculosis infection in adults living with human immunodeficiency virus. Clin Infect Dis. 2021;72:865–868.
Abbott R, Landseidel K, Atukunda M. Incident Tuberculosis Infection is Associated with Alcohol use in Adults in Rural Uganda [published online ahead of print June 2, 2024]. Clin Infect Dis. doi:10.1093/cid/ciae304.
Huang C-C, Tchetgen ET, Becerra MC, et al. Cigarette smoking among tuberculosis patients increases risk of transmission to child contacts. Int J Tuberc Lung Dis. 2014;18:1285–1291.
Blount RJ, Phan H, Trinh T, et al. Indoor air pollution and susceptibility to tuberculosis infection in urban Vietnamese children. Am J Respir Crit Care Med. 2021;204:1211–1221.
Martinez L, le Roux DM, Barnett W, et al. Tuberculin skin test conversion and primary progressive tuberculosis disease in the first 5 years of life: a birth cohort study from Cape Town, South Africa. Lancet Child Adolesc Health. 2018;2:46–55.
Nalugoda F, Nabukalu D, Ssekasanvu J, et al. Smoker characteristics and trends in tobacco smoking in Rakai, Uganda, 2010–2018. Tob Induc Dis. 2022;20:23.
Jafta N, Jeena PM, Barregard L, et al. Childhood tuberculosis and exposure to indoor air pollution: a systematic review and meta-analysis. Int J Tuberc Lung Dis. 2015;19:596–602.
Jafta N, Jeena PM, Barregard L, et al. Association of childhood pulmonary tuberculosis with exposure to indoor air pollution: a case control study. BMC Public Health. 2019;19:275.
Havlir DV, Balzer LB, Charlebois ED, et al. HIV testing and treatment with the use of a community health approach in rural Africa. N Engl J Med. 2019;381:219–229.
Marquez C, Atukunda M, Nugent J, et al. Community-Wide universal human immunodeficiency virus (HIV) test and treat intervention reduces tuberculosis transmission in rural Uganda: a cluster-randomized trial. Clin Infect Dis. 2024;78:1601–1607.
Dodd PJ, Looker C, Plumb ID, et al. Age- and sex-specific social contact patterns and incidence of mycobacterium tuberculosis infection. Am J Epidemiol. 2016;183:156–166.
Laycock KM, Enane LA, Steenhoff AP. Tuberculosis in adolescents and young adults: emerging data on TB transmission and prevention among vulnerable young people. Trop Med Infect Dis. 2021;6:148.
Musaazi J, Sekaggya-Wiltshire C, Okoboi S, et al. Increased uptake of tuberculosis preventive therapy (TPT) among people living with HIV following the 100-days accelerated campaign: a retrospective review of routinely collected data at six urban public health facilities in Uganda. PLoS One. 2023;18:e0268935.

Auteurs

Elijah Kakande (E)

From the Infectious Diseases Research Collaboration, Kampala, Uganda.

Bob Ssekyanzi (B)

From the Infectious Diseases Research Collaboration, Kampala, Uganda.

Rachel Abbott (R)

Department of Medicine, Division of HIV, ID and Global Medicine, University of California, San Francisco, California.

Willington Ariho (W)

From the Infectious Diseases Research Collaboration, Kampala, Uganda.

Gloria Nattabi (G)

From the Infectious Diseases Research Collaboration, Kampala, Uganda.

Kirsten Landsiedel (K)

Division of Biostatistics, University of California, Berkeley, Berkeley, California.

Jennifer Temple (J)

Department of Medicine, Division of HIV, ID and Global Medicine, University of California, San Francisco, California.

Gabriel Chamie (G)

Department of Medicine, Division of HIV, ID and Global Medicine, University of California, San Francisco, California.

Diane V Havlir (DV)

Department of Medicine, Division of HIV, ID and Global Medicine, University of California, San Francisco, California.

Moses R Kamya (MR)

From the Infectious Diseases Research Collaboration, Kampala, Uganda.
Department of Medicine, School of Medicine, Makerere University, Kampala, Uganda.

Edwin D Charlebois (ED)

Department of Medicine, Center for AIDS Prevention Studies, Division of Prevention Science, University of California, San Francisco, San Francisco, California.

Laura B Balzer (LB)

Division of Biostatistics, University of California, Berkeley, Berkeley, California.

Carina Marquez (C)

Department of Medicine, Division of HIV, ID and Global Medicine, University of California, San Francisco, California.

Classifications MeSH