World Health Organization, 2015. Global Tuberculosis Report 2015. Available at: http://apps.who.int/iris/bitstream/10665/191102/1/9789241565059_eng.pdf?ua=1. Accessed November 2, 2015.
Getahun H, Matteelli A, Chaisson RE, Raviglione M, 2015. Latent Mycobacterium tuberculosis infection. N Engl J Med 372: 2127–2135.
Corbett EL, Watt CJ, Walker N, Maher D, Williams BG, Raviglione MC, Dye C, 2003. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 163: 1009–1021.
Houben RM, Dodd PJ, 2016. The global burden of latent tuberculosis infection: a re-estimation using mathematical modelling. PLoS Med 13: e1002152.
van Zyl Smit RN, Pai M, Yew WW, Leung CC, Zumla A, Bateman ED, Dheda K, 2010. Global lung health: the colliding epidemics of tuberculosis, tobacco smoking, HIV and COPD. Eur Respir J 35: 27–33.
den Boon S, et al., 2007. Association between passive smoking and infection with Mycobacterium tuberculosis in children. Pediatrics 119: 734–739.
du Preez K, Mandalakas AM, Kirchner HL, Grewal HM, Schaaf HS, van Wyk SS, Hesseling AC, 2011. Environmental tobacco smoke exposure increases Mycobacterium tuberculosis infection risk in children. Int J Tuberc Lung Dis 15: 1490–1496 i.
Huang CC, et al., 2014. Cigarette smoking among tuberculosis patients increases risk of transmission to child contacts. Int J Tuberc Lung Dis 18: 1285–1291.
Singh M, Mynak ML, Kumar L, Mathew JL, Jindal SK, 2005. Prevalence and risk factors for transmission of infection among children in household contact with adults having pulmonary tuberculosis. Arch Dis Child 90: 624–628.
Sridhar S, Karnani N, Connell DW, Millington KA, Dosanjh D, Bakir M, Soysal A, Deeks J, Lalvani A, 2014. Increased risk of Mycobacterium tuberculosis infection in household child contacts exposed to passive tobacco smoke. Pediatr Infect Dis J 33: 1303–1306.
Hill PC, et al., 2006. Comparison of enzyme-linked immunospot assay and tuberculin skin test in healthy children exposed to Mycobacterium tuberculosis. Pediatrics 117: 1542–1548.
Adetifa IM, et al., 2013. Interferon-gamma ELISPOT as a biomarker of treatment efficacy in latent tuberculosis infection: a clinical trial. Am J Respir Crit Care Med 187: 439–445.
de Jong BC, Adetifa I, Walther B, Hill PC, Antonio M, Ota M, Adegbola RA, 2010. Differences between tuberculosis cases infected with Mycobacterium africanum, West African type 2, relative to Euro-American Mycobacterium tuberculosis: an update. FEMS Immunol Med Microbiol 58: 102–105.
Hill PC, et al., 2008. Incidence of tuberculosis and the predictive value of ELISPOT and Mantoux tests in Gambian case contacts. PLoS One 3: e1379.
Adetifa IM, Muhammad AK, Jeffries D, Donkor S, Borgdorff MW, Corrah T, D’Alessandro U, 2015. A tuberculin skin test survey and the annual risk of Mycobacterium tuberculosis infection in Gambian school children. PLoS One 10: e0139354.
Davies PD, Yew WW, Ganguly D, Davidow AL, Reichman LB, Dheda K, Rook GA, 2006. Smoking and tuberculosis: the epidemiological association and immunopathogenesis. Trans R Soc Trop Med Hyg 100: 291–298.
Shang S, et al., 2011. Cigarette smoke increases susceptibility to tuberculosis–evidence from in vivo and in vitro models. J Infect Dis 203: 1240–1248.
Hodge S, Hodge G, Ahern J, Jersmann H, Holmes M, Reynolds PN, 2007. Smoking alters alveolar macrophage recognition and phagocytic ability: implications in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 37: 748–755.
Patra J, Bhatia M, Suraweera W, Morris SK, Patra C, Gupta PC, Jha P, 2015. Exposure to second-hand smoke and the risk of tuberculosis in children and adults: a systematic review and meta-analysis of 18 observational studies. PLoS Med 12: e1001835.
Walraven GE, Nyan OA, Van Der Sande MA, Banya WA, Ceesay SM, Milligan PJ, McAdam KP, 2001. Asthma, smoking and chronic cough in rural and urban adult communities in The Gambia. Clin Exp Allergy 31: 1679–1685.
Maassen IT, Kremers SP, Mudde AN, Joof BM, 2004. Smoking initiation among Gambian adolescents: social cognitive influences and the effect of cigarette sampling. Health Educ Res 19: 551–560.
Adetifa IM, Lugos MD, Hammond A, Jeffries D, Donkor S, Adegbola RA, Hill PC, 2007. Comparison of two interferon gamma release assays in the diagnosis of Mycobacterium tuberculosis infection and disease in The Gambia. BMC Infect Dis 7: 122.
Adetifa IM, et al., 2016. A tuberculosis nationwide prevalence survey in Gambia, 2012. Bull World Health Organ 94: 433–441.
Oberg M, Jaakkola MS, Woodward A, Peruga A, Pruss-Ustun A, 2011. Worldwide burden of disease from exposure to second-hand smoke: a retrospective analysis of data from 192 countries. Lancet 377: 139–146.
World Health Organization, 2011. Second-Hand Tobacco Smoke. Available at: http://www.who.int/tobacco/research/secondhand_smoke/faq/en/. Accessed April 26, 2016.
Kassem NO, et al., 2014. Children’s exposure to secondhand and thirdhand smoke carcinogens and toxicants in homes of hookah smokers. Nicotine Tob Res 16: 961–975.
Thomas JL, Hecht SS, Luo X, Ming X, Ahluwalia JS, Carmella SG, 2014. Thirdhand tobacco smoke: a tobacco-specific lung carcinogen on surfaces in smokers’ homes. Nicotine Tob Res 16: 26–32.
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Tobacco use is a major risk factor for tuberculosis (TB). Secondhand smoke (SHS) is also a risk factor for TB and to a lesser extent, Mycobacterium tuberculosis infection without disease. We investigated the added risk of M. tuberculosis infection due to SHS exposure in childhood contacts of TB cases in The Gambia. Participants were childhood household contacts aged ≤ 14 years of newly diagnosed pulmonary TB (PTB) cases. The intensity of exposure to the case was categorized according to whether contacts slept in the same room, same house, or a different house as the case. Contacts were tested with an enzyme-linked immunospot interferon gamma release assay. In multivariate regression models, M. tuberculosis infection was associated with increasing exposure to a case (odds ratios [OR]: 3.9, 95% confidence interval [CI]: 2.11–71.4, P < 0.001]) and with male gender (OR: 1.5 [95% CI: 1.12–2.11], P = 0.008). Tobacco use caused a 3-fold increase in the odds of M. tuberculosis infection in children who slept closest to a case who smoked within the same home compared with a nonsmoking case (OR: 8.0 [95% CI: 2.74–23.29] versus 2.4 [95% CI: 1.17–4.92], P < 0.001). SHS exposure as an effect modifier appears to greatly increase the risk of M. tuberculosis infection in children exposed to PTB cases. Smoking cessation campaigns may be important for reducing transmission of M. tuberculosis to children within households.
Financial support: The United Kingdom’s Medical Research Council funded this study through the Medical Research Council Unit, The Gambia.
Authors’ addresses: Ifedayo M. O. Adetifa, Department of Infectious Diseases Epidemiology, London School of Hygiene and Tropical Medicine, London, United Kingdom, Medical Education and Development Unit, College of Medicine, University of Lagos, Nigeria, and Disease Control and Elimination Theme, Medical Research Council Unit, The Gambia, Fajara, The Gambia, E-mail: Ifedayo.Adetifa@lshtm.ac.uk. Lindsay Kendall, Simon Donkor, Moses D. Lugos, Abdulrahman S. Hammond, and Patrick K. Owiafe, Disease Control and Elimination Theme, Medical Research Council Laboratories The Gambia, Fajara, The Gambia, E-mails: lindsay_kendall@hotmail.com, sdonkor@mrc.gm, mlugos2003@yahoo.com, abdulhammond@hotmail.com, and pkowiafe@uhas.edu.gh. Martin O. C. Ota, World Health Organization-Regional Office for Africa, Research, Publication and Library Services, Brazzaville, Congo, E-mail: otama@who.int. Roger H. Brookes, Sanofi Pasteur Ltd., Bioprocess Research and Development, Toronto, ON, Canada, E-mail: roger.brookes@sanofipasteur.com. Philip C. Hill, Department of Preventive and Social Medicine, University of Otago School of Medicine, Dunedin, Otago, New Zealand, E-mail: philip.hill@otago.ac.nz.
World Health Organization, 2015. Global Tuberculosis Report 2015. Available at: http://apps.who.int/iris/bitstream/10665/191102/1/9789241565059_eng.pdf?ua=1. Accessed November 2, 2015.
Getahun H, Matteelli A, Chaisson RE, Raviglione M, 2015. Latent Mycobacterium tuberculosis infection. N Engl J Med 372: 2127–2135.
Corbett EL, Watt CJ, Walker N, Maher D, Williams BG, Raviglione MC, Dye C, 2003. The growing burden of tuberculosis: global trends and interactions with the HIV epidemic. Arch Intern Med 163: 1009–1021.
Houben RM, Dodd PJ, 2016. The global burden of latent tuberculosis infection: a re-estimation using mathematical modelling. PLoS Med 13: e1002152.
van Zyl Smit RN, Pai M, Yew WW, Leung CC, Zumla A, Bateman ED, Dheda K, 2010. Global lung health: the colliding epidemics of tuberculosis, tobacco smoking, HIV and COPD. Eur Respir J 35: 27–33.
den Boon S, et al., 2007. Association between passive smoking and infection with Mycobacterium tuberculosis in children. Pediatrics 119: 734–739.
du Preez K, Mandalakas AM, Kirchner HL, Grewal HM, Schaaf HS, van Wyk SS, Hesseling AC, 2011. Environmental tobacco smoke exposure increases Mycobacterium tuberculosis infection risk in children. Int J Tuberc Lung Dis 15: 1490–1496 i.
Huang CC, et al., 2014. Cigarette smoking among tuberculosis patients increases risk of transmission to child contacts. Int J Tuberc Lung Dis 18: 1285–1291.
Singh M, Mynak ML, Kumar L, Mathew JL, Jindal SK, 2005. Prevalence and risk factors for transmission of infection among children in household contact with adults having pulmonary tuberculosis. Arch Dis Child 90: 624–628.
Sridhar S, Karnani N, Connell DW, Millington KA, Dosanjh D, Bakir M, Soysal A, Deeks J, Lalvani A, 2014. Increased risk of Mycobacterium tuberculosis infection in household child contacts exposed to passive tobacco smoke. Pediatr Infect Dis J 33: 1303–1306.
Hill PC, et al., 2006. Comparison of enzyme-linked immunospot assay and tuberculin skin test in healthy children exposed to Mycobacterium tuberculosis. Pediatrics 117: 1542–1548.
Adetifa IM, et al., 2013. Interferon-gamma ELISPOT as a biomarker of treatment efficacy in latent tuberculosis infection: a clinical trial. Am J Respir Crit Care Med 187: 439–445.
de Jong BC, Adetifa I, Walther B, Hill PC, Antonio M, Ota M, Adegbola RA, 2010. Differences between tuberculosis cases infected with Mycobacterium africanum, West African type 2, relative to Euro-American Mycobacterium tuberculosis: an update. FEMS Immunol Med Microbiol 58: 102–105.
Hill PC, et al., 2008. Incidence of tuberculosis and the predictive value of ELISPOT and Mantoux tests in Gambian case contacts. PLoS One 3: e1379.
Adetifa IM, Muhammad AK, Jeffries D, Donkor S, Borgdorff MW, Corrah T, D’Alessandro U, 2015. A tuberculin skin test survey and the annual risk of Mycobacterium tuberculosis infection in Gambian school children. PLoS One 10: e0139354.
Davies PD, Yew WW, Ganguly D, Davidow AL, Reichman LB, Dheda K, Rook GA, 2006. Smoking and tuberculosis: the epidemiological association and immunopathogenesis. Trans R Soc Trop Med Hyg 100: 291–298.
Shang S, et al., 2011. Cigarette smoke increases susceptibility to tuberculosis–evidence from in vivo and in vitro models. J Infect Dis 203: 1240–1248.
Hodge S, Hodge G, Ahern J, Jersmann H, Holmes M, Reynolds PN, 2007. Smoking alters alveolar macrophage recognition and phagocytic ability: implications in chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 37: 748–755.
Patra J, Bhatia M, Suraweera W, Morris SK, Patra C, Gupta PC, Jha P, 2015. Exposure to second-hand smoke and the risk of tuberculosis in children and adults: a systematic review and meta-analysis of 18 observational studies. PLoS Med 12: e1001835.
Walraven GE, Nyan OA, Van Der Sande MA, Banya WA, Ceesay SM, Milligan PJ, McAdam KP, 2001. Asthma, smoking and chronic cough in rural and urban adult communities in The Gambia. Clin Exp Allergy 31: 1679–1685.
Maassen IT, Kremers SP, Mudde AN, Joof BM, 2004. Smoking initiation among Gambian adolescents: social cognitive influences and the effect of cigarette sampling. Health Educ Res 19: 551–560.
Adetifa IM, Lugos MD, Hammond A, Jeffries D, Donkor S, Adegbola RA, Hill PC, 2007. Comparison of two interferon gamma release assays in the diagnosis of Mycobacterium tuberculosis infection and disease in The Gambia. BMC Infect Dis 7: 122.
Adetifa IM, et al., 2016. A tuberculosis nationwide prevalence survey in Gambia, 2012. Bull World Health Organ 94: 433–441.
Oberg M, Jaakkola MS, Woodward A, Peruga A, Pruss-Ustun A, 2011. Worldwide burden of disease from exposure to second-hand smoke: a retrospective analysis of data from 192 countries. Lancet 377: 139–146.
World Health Organization, 2011. Second-Hand Tobacco Smoke. Available at: http://www.who.int/tobacco/research/secondhand_smoke/faq/en/. Accessed April 26, 2016.
Kassem NO, et al., 2014. Children’s exposure to secondhand and thirdhand smoke carcinogens and toxicants in homes of hookah smokers. Nicotine Tob Res 16: 961–975.
Thomas JL, Hecht SS, Luo X, Ming X, Ahluwalia JS, Carmella SG, 2014. Thirdhand tobacco smoke: a tobacco-specific lung carcinogen on surfaces in smokers’ homes. Nicotine Tob Res 16: 26–32.
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