World Health Organization, 2016. Global Tuberculosis Report 2016. Geneva, Switzerland. November 16, 2016. Available at: http://apps.who.int/iris/bitstream/10665/250441/1/9789241565394-eng.pdf?ua=1. Accessed January 16, 2017.
Zumla A et al. 2016. Tuberculosis and mass gatherings-opportunities for defining burden, transmission risk, and the optimal surveillance, prevention, and control measures at the annual Hajj pilgrimage. Int J Infect Dis 47: 86–91.
Al-Orainey IO, 2013. Tuberculosis infection during Hajj pilgrimage. The risk to pilgrims and their communities. Saudi Med J 34: 676–680.
Gautret P, Benkouiten S, Griffiths K, Sridhar S, 2015. The inevitable Hajj cough: surveillance data in French pilgrims, 2012–2014. Travel Med Infect Dis 13: 485–489.
Alzeer A, Mashlah A, Fakim N, Al-Sugair N, Al-Hedaithy M, Al-Majed S, Jamjoom G, 1998. Tuberculosis is the commonest cause of pneumonia requiring hospitalization during Hajj (pilgrimage to Makkah). J Infect 36: 303–306.
Helb D et al. 2010. Rapid detection of Mycobacterium tuberculosis and rifampin resistance by use of on-demand, near-patient technology. J Clin Microbiol 48: 229–237.
Wilder-Smith A, Foo W, Earnest A, Paton NI, 2005. High risk of Mycobacterium tuberculosis infection during the Hajj pilgrimage. Trop Med Int Health 10: 336–339.
Aldridge RW, Yates TA, Zenner D, White PJ, Abubakar I, Hayward AC, 2014. Pre-entry screening programmes for tuberculosis in migrants to low-incidence countries: a systematic review and meta-analysis. Lancet Infect Dis 14: 1240–1249.
Ayles H, Schaap A, Nota A, Sismanidis C, Tembwe R, de Haas P, Muyoyeta M, Beyers N, Peter Godfrey-Faussett for the ZAMSTAR Study Team, 2009. Prevalence of tuberculosis, HIV and respiratory symptoms in two Zambian communities: implications for tuberculosis control in the era of HIV. PLoS One 4: e5602.
Hoa NB, Sy DN, Nhung NV, Tiemersma EW, Borgdorff MW, Cobelens FG, 2010. National survey of tuberculosis prevalence in Viet Nam. Bull World Health Organ 88: 273–280.
Onozaki I, Law I, Sismanidis C, Zignol M, Glaziou P, Floyd K, 2015. National tuberculosis prevalence surveys in Asia, 1990–2012: an overview of results and lessons learned. Trop Med Int Health 20: 1128–1145.
Golub JE, Bur S, Cronin WA, Gange S, Baruch N, Comstock GW, Chaisson RE, 2006. Delayed tuberculosis diagnosis and tuberculosis transmission. Int J Tuberc Lung Dis 10: 24–30.
Nanoo A, Izu A, Ismail NA, Ihekweazu C, Abubakar I, Mametja D, Madhi SA, 2015. Nationwide and regional incidence of microbiologically confirmed pulmonary tuberculosis in South Africa, 2004–2012: a time series analysis. Lancet Infect Dis 15: 1066–1076.
Shisana O et al. 2014. South African National HIV Prevalence, Incidence and Behaviour Survey, 2012. HSRC Press. Available at: http://www.hsrc.ac.za/en/research-data/view/6871. Accessed January 16, 2017.
Muntingh L, 2013. Race, Gender and Socioeconomic Status in Law Enforcement in South Africa—Are There Worrying Signs? Available at: http://cspri.org.za/publications/research-reports/Inequality%20paper.pdf. Accessed January 16, 2017.
Sanchez-Barriga JJ, 2015. Mortality trends and risk of dying from pulmonary tuberculosis in the 7 socioeconomic regions and the 32 States of Mexico, 2000–2009. Arch Bronconeumol 51: 16–23.
Needham DM, Foster SD, Tomlinson G, Godfrey-Faussett P, 2001. Socio-economic, gender and health services factors affecting diagnostic delay for tuberculosis patients in urban Zambia. Trop Med Int Health 6: 256–259.
Gelaw SM, 2016. Socioeconomic factors associated with knowledge on tuberculosis among adults in Ethiopia. Tuberc Res Treat 2016: 6207457.
Dogar OF, Shah SK, Chughtai AA, Qadeer E, 2012. Gender disparity in tuberculosis cases in eastern and western provinces of Pakistan. BMC Infect Dis 12: 244.
Memish ZA et al. 2014. Prevalence of MERS-CoV nasal carriage and compliance with the Saudi health recommendations among pilgrims attending the 2013 Hajj. J Infect Dis 210: 1067–1072.
Marais BJ et al. 2013. Tuberculosis comorbidity with communicable and non-communicable diseases: integrating health services and control efforts. Lancet Infect Dis 13: 436–448.
Bates M et al. 2012. Evaluation of the burden of unsuspected pulmonary tuberculosis and co-morbidity with non-communicable diseases in sputum producing adult inpatients. PLoS One 7: e40774.
Pan SC, Ku CC, Kao D, Ezzati M, Fang CT, Lin HH, 2015. Effect of diabetes on tuberculosis control in 13 countries with high tuberculosis: a modelling study. Lancet Diabetes Endocrinol 3: 323–330.
The Lancet DE, 2014. Diabetes and tuberculosis—a wake-up call. Lancet Diabetes Endocrinol 2: 677.
Ebrahim SH, Memish ZA, Uyeki TM, Khoja TA, Marano N, McNabb SJ, 2009. Public health. Pandemic H1N1 and the 2009 Hajj. Science 326: 938–940.
Lin HH, Ezzati M, Murray M, 2007. Tobacco smoke, indoor air pollution and tuberculosis: a systematic review and meta-analysis. PLoS Med 4: e20.
Leung CC et al. 2015. Smoking adversely affects treatment response, outcome and relapse in tuberculosis. Eur Respir J 45: 738–745.
World Health Organization, 2007. Tuberculosis Care and Control in Refugee and Displaced Populations. An Interagency Field Manual. Geneva, Switzerland: WHO. Available at: http://apps.who.int/iris/bitstream/10665/43661/1/9789241595421_eng.pdf. Accessed May 30, 2017.
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Mass gatherings pose a risk for tuberculosis (TB) transmission and reactivation of latent TB infection. The annual Hajj pilgrimage attracts 2 million pilgrims many from high TB-endemic countries. We evaluated the burden of undiagnosed active pulmonary TB in pilgrims attending the 2015 Hajj mass gathering. We conducted a prospective cross-sectional study in Mecca, Kingdom of Saudi Arabia, for nonhospitalized adult pilgrims from five high TB-endemic countries. Enrollment criteria were the presence of a cough and the ability to produce a sputum sample. Sputum samples were processed using the Xpert MTB-RIF assay. Data were analyzed for drug-resistant TB, risk factors, and comorbidities by the country of origin. Of 1,164 consenting pilgrims enrolled from five countries: Afghanistan (316), Bangladesh (222), Nigeria (176), Pakistan (302), and South Africa (148), laboratory results were available for 1,063 (91.3%). The mean age of pilgrims was 54.5 (range = 18–94 years) with a male to female ratio of 2.6:1; 27.7% had an underlying comorbidity, with hypertension and diabetes being the most common, 20% were smokers, and 2.8% gave a history of previous TB treatment. Fifteen pilgrims (1.4%) had active previously undiagnosed drug-sensitive pulmonary TB (Afghanistan [12; 80%], Pakistan [2; 13.3%], and Nigeria [1; 6.7%]). No multidrug-resistant TB cases were detected. Pilgrims from high TB-endemic Asian and African countries with undiagnosed active pulmonary TB pose a risk to other pilgrims from over 180 countries. Further studies are required to define the scale of the TB problem during the Hajj mass gathering and the development of proactive screening, treatment and prevention guidelines.
Authors’ addresses: Saber Yezli, Yara Yassin, and Badriah Alotaibi, The Global Centre for Mass Gatherings Medicine, Ministry of Health, Riyadh, Saudi Arabia, E-mails: saber.yezli@gmail.com, yyassin@moh.gov.sa, and otaibi_b1@yahoo.com. Alimuddin Zumla, Center for Clinical Microbiology, Division of Infection and Immunity, University College London and NIHR Biomedical Research Centre at UCL Hospitals, London, United Kingdom, E-mail: a.i.zumla@gmail.com. Ali M. Al-Shangiti, National Health Laboratory, Ministry of Health, Riyadh, Saudi Arabia, E-mail: Aalshangiti@moh.gov.sa. Gamal Mohamed, Liverpool School of Tropical Medicine, Liverpool, United Kingdom, E-mail: olagamal99@gmail.com. Abdulhafiz M. Turkistani, Makkah Regional Health Affairs, Ministry of Health, Jeddah, Saudi Arabia, E-mail: aturkistani@moh.gov.sa.
World Health Organization, 2016. Global Tuberculosis Report 2016. Geneva, Switzerland. November 16, 2016. Available at: http://apps.who.int/iris/bitstream/10665/250441/1/9789241565394-eng.pdf?ua=1. Accessed January 16, 2017.
Zumla A et al. 2016. Tuberculosis and mass gatherings-opportunities for defining burden, transmission risk, and the optimal surveillance, prevention, and control measures at the annual Hajj pilgrimage. Int J Infect Dis 47: 86–91.
Al-Orainey IO, 2013. Tuberculosis infection during Hajj pilgrimage. The risk to pilgrims and their communities. Saudi Med J 34: 676–680.
Gautret P, Benkouiten S, Griffiths K, Sridhar S, 2015. The inevitable Hajj cough: surveillance data in French pilgrims, 2012–2014. Travel Med Infect Dis 13: 485–489.
Alzeer A, Mashlah A, Fakim N, Al-Sugair N, Al-Hedaithy M, Al-Majed S, Jamjoom G, 1998. Tuberculosis is the commonest cause of pneumonia requiring hospitalization during Hajj (pilgrimage to Makkah). J Infect 36: 303–306.
Helb D et al. 2010. Rapid detection of Mycobacterium tuberculosis and rifampin resistance by use of on-demand, near-patient technology. J Clin Microbiol 48: 229–237.
Wilder-Smith A, Foo W, Earnest A, Paton NI, 2005. High risk of Mycobacterium tuberculosis infection during the Hajj pilgrimage. Trop Med Int Health 10: 336–339.
Aldridge RW, Yates TA, Zenner D, White PJ, Abubakar I, Hayward AC, 2014. Pre-entry screening programmes for tuberculosis in migrants to low-incidence countries: a systematic review and meta-analysis. Lancet Infect Dis 14: 1240–1249.
Ayles H, Schaap A, Nota A, Sismanidis C, Tembwe R, de Haas P, Muyoyeta M, Beyers N, Peter Godfrey-Faussett for the ZAMSTAR Study Team, 2009. Prevalence of tuberculosis, HIV and respiratory symptoms in two Zambian communities: implications for tuberculosis control in the era of HIV. PLoS One 4: e5602.
Hoa NB, Sy DN, Nhung NV, Tiemersma EW, Borgdorff MW, Cobelens FG, 2010. National survey of tuberculosis prevalence in Viet Nam. Bull World Health Organ 88: 273–280.
Onozaki I, Law I, Sismanidis C, Zignol M, Glaziou P, Floyd K, 2015. National tuberculosis prevalence surveys in Asia, 1990–2012: an overview of results and lessons learned. Trop Med Int Health 20: 1128–1145.
Golub JE, Bur S, Cronin WA, Gange S, Baruch N, Comstock GW, Chaisson RE, 2006. Delayed tuberculosis diagnosis and tuberculosis transmission. Int J Tuberc Lung Dis 10: 24–30.
Nanoo A, Izu A, Ismail NA, Ihekweazu C, Abubakar I, Mametja D, Madhi SA, 2015. Nationwide and regional incidence of microbiologically confirmed pulmonary tuberculosis in South Africa, 2004–2012: a time series analysis. Lancet Infect Dis 15: 1066–1076.
Shisana O et al. 2014. South African National HIV Prevalence, Incidence and Behaviour Survey, 2012. HSRC Press. Available at: http://www.hsrc.ac.za/en/research-data/view/6871. Accessed January 16, 2017.
Muntingh L, 2013. Race, Gender and Socioeconomic Status in Law Enforcement in South Africa—Are There Worrying Signs? Available at: http://cspri.org.za/publications/research-reports/Inequality%20paper.pdf. Accessed January 16, 2017.
Sanchez-Barriga JJ, 2015. Mortality trends and risk of dying from pulmonary tuberculosis in the 7 socioeconomic regions and the 32 States of Mexico, 2000–2009. Arch Bronconeumol 51: 16–23.
Needham DM, Foster SD, Tomlinson G, Godfrey-Faussett P, 2001. Socio-economic, gender and health services factors affecting diagnostic delay for tuberculosis patients in urban Zambia. Trop Med Int Health 6: 256–259.
Gelaw SM, 2016. Socioeconomic factors associated with knowledge on tuberculosis among adults in Ethiopia. Tuberc Res Treat 2016: 6207457.
Dogar OF, Shah SK, Chughtai AA, Qadeer E, 2012. Gender disparity in tuberculosis cases in eastern and western provinces of Pakistan. BMC Infect Dis 12: 244.
Memish ZA et al. 2014. Prevalence of MERS-CoV nasal carriage and compliance with the Saudi health recommendations among pilgrims attending the 2013 Hajj. J Infect Dis 210: 1067–1072.
Marais BJ et al. 2013. Tuberculosis comorbidity with communicable and non-communicable diseases: integrating health services and control efforts. Lancet Infect Dis 13: 436–448.
Bates M et al. 2012. Evaluation of the burden of unsuspected pulmonary tuberculosis and co-morbidity with non-communicable diseases in sputum producing adult inpatients. PLoS One 7: e40774.
Pan SC, Ku CC, Kao D, Ezzati M, Fang CT, Lin HH, 2015. Effect of diabetes on tuberculosis control in 13 countries with high tuberculosis: a modelling study. Lancet Diabetes Endocrinol 3: 323–330.
The Lancet DE, 2014. Diabetes and tuberculosis—a wake-up call. Lancet Diabetes Endocrinol 2: 677.
Ebrahim SH, Memish ZA, Uyeki TM, Khoja TA, Marano N, McNabb SJ, 2009. Public health. Pandemic H1N1 and the 2009 Hajj. Science 326: 938–940.
Lin HH, Ezzati M, Murray M, 2007. Tobacco smoke, indoor air pollution and tuberculosis: a systematic review and meta-analysis. PLoS Med 4: e20.
Leung CC et al. 2015. Smoking adversely affects treatment response, outcome and relapse in tuberculosis. Eur Respir J 45: 738–745.
World Health Organization, 2007. Tuberculosis Care and Control in Refugee and Displaced Populations. An Interagency Field Manual. Geneva, Switzerland: WHO. Available at: http://apps.who.int/iris/bitstream/10665/43661/1/9789241595421_eng.pdf. Accessed May 30, 2017.
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