Global, regional, and national burden of tuberculosis, 1990-2016: Results from the Global Burden of Diseases, Injuries, and Risk Factors 2016 Study

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Hmwe Hmwe Kyu, Emilie R. Maddison, Nathaniel J. Henry, Jorge R. Ledesma, Kirsten E. Wiens, Robert Reiner, Molly H. Biehl, Chloe Shields, Aaron Osgood-Zimmerman, Jennifer M. Ross, Austin Carter, Tahvi D. Frank, Haidong Wang, Vinay Srinivasan, Zegeye Abebe, Sanjay Kumar Agarwal, Fares Alahdab, Kefyalew Addis Alene, Beriwan Abdulqadir Ali, Nelson Alvis-Guzman, Jason R. Andrews, Carl Abelardo T. Antonio, Suleman Atique, Sachin R. Atre, Ashish Awasthi, Henok Tadesse Ayele, Hamid Badali, Alaa Badawi, Aleksandra Barac, Neeraj Bedi, Masoud Behzadifar, Meysam Behzadifar, Bayu Begashaw Bekele, Saba Abraham Belay, Isabela M. Bensenor, Zahid A. Butt, Félix Carvalho, Kelly Cercy, Devasahayam J. Christopher, Alemneh Kabeta Daba, Lalit Dandona, Rakhi Dandona, Ahmad Daryani, Feleke Mekonnen Demeke, Kebede Deribe, Samath Dhamminda Dharmaratne, David Teye Doku, Manisha Dubey, Dumessa Edessa, Ziad El-Khatib, Shymaa Enany, Eduarda Fernandes, Florian Fischer, Alberto L. Garcia-Basteiro, Abadi Kahsu Gebre, Gebremedhin Berhe Gebregergs, Teklu Gebrehiwo Gebremichael, Tilayie Feto Gelano, Demeke Geremew, Philimon N. Gona, Amador Goodridge, Rahul Gupta, Hassan Haghparast Bidgoli, Gessessew Bugssa Hailu, Hamid Yimam Hassen, Mohammad T. Tadesse Hedayati, Andualem Henok, Sorin Hostiuc, Mamusha Aman Hussen, Olayinka Stephen Ilesanmi, Seyed Sina Naghibi Irvani, Kathryn H. Jacobsen, Sarah C. Johnson, Jost B. Jonas, Amaha Kahsay, Surya Kant, Amir Kasaeian, Tesfaye Dessale Kassa, Yousef Saleh Khader, Morteza Abdullatif Khafaie, Ibrahim Khalil, Ejaz Ahmad Khan, Young-Ho Khang, Yun Jin Kim, Sonali Kochhar, Ai Koyanagi, Kristopher J. Krohn, G. Anil Kumar, Ayenew Molla Lakew, Cheru Tesema Leshargie, Rakesh Lodha, Erlyn Rachelle King MacArayan, Reza Majdzadeh, Francisco Rogerlândio Martins-Melo, Addisu Melese, Ziad A. Memish, Walter Mendoza, Desalegn Tadese Mengistu, Getnet Mengistu, Tomislav Mestrovic, Babak Moazen, Karzan Abdulmuhsin Mohammad, Shafiu Mohammed, Ali H. Mokdad, Mahmood Moosazadeh, Seyyed Meysam Mousavi, Ghulam Mustafa, Jean B. Nachega, Long Hoang Nguyen, Son Hoang Nguyen, Trang Huyen Nguyen, Dina Nur Anggraini Ningrum, Yirga Legesse Nirayo, Vuong Minh Nong, Richard Ofori-Asenso, Felix Akpojene Ogbo, In-Hwan Oh, Olanrewaju Oladimeji, Andrew T. Olagunju, Eyal Oren, David M. Pereira, Swayam Prakash, Mostafa Qorbani, Anwar Rafay, Rajesh Kumar Rai, Usha Ram, Salvatore Rubino, Saeid Safiri, Joshua A. Salomon, Abdallah M. Samy, Benn Sartorius, Maheswar Satpathy, Seyedmojtaba Seyedmousavi, Mehdi Sharif, João Pedro Silva, Dayane Gabriele Alves Silveira, Jasvinder A. Singh, Chandrashekhar T. Sreeramareddy, Bach Xuan Tran, Afewerki Gebremeskel Tsadik, Kingsley Nnanna Ukwaja, Irfan Ullah, Olalekan A. Uthman, Vasily Vlassov, Stein Emil Vollset, Giang Vu, Fitsum Weldegebreal, Andrea Werdecker, Ebrahim M. Yimer, Naohiro Yonemoto, Marcel Yotebieng, Mohsen Naghavi, Theo Vos, Simon I. Hay, Christopher J.L. Murray

2018 The Lancet Infectious Diseases Vol. 18 Issue 12 Article Cited by 181 Quartile

Abstract

Background Although a preventable and treatable disease, tuberculosis causes more than a million deaths each year. As countries work towards achieving the Sustainable Development Goal (SDG) target to end the tuberculosis epidemic by 2030, robust assessments of the levels and trends of the burden of tuberculosis are crucial to inform policy and programme decision making. We assessed the levels and trends in the fatal and non-fatal burden of tuberculosis by drug resistance and HIV status for 195 countries and territories from 1990 to 2016. Methods We analysed 15 943 site-years of vital registration data, 1710 site-years of verbal autopsy data, 764 site-years of sample-based vital registration data, and 361 site-years of mortality surveillance data to estimate mortality due to tuberculosis using the Cause of Death Ensemble model. We analysed all available data sources, including annual case notifications, prevalence surveys, population-based tuberculin surveys, and estimated tuberculosis cause-specific mortality to generate internally consistent estimates of incidence, prevalence, and mortality using DisMod-MR 2.1, a Bayesian meta-regression tool. We assessed how the burden of tuberculosis differed from the burden predicted by the Socio-demographic Index (SDI), a composite indicator of income per capita, average years of schooling, and total fertility rate. Findings Globally in 2016, among HIV-negative individuals, the number of incident cases of tuberculosis was 9·02 million (95% uncertainty interval [UI] 8·05-10·16) and the number of tuberculosis deaths was 1·21 million (1·16-1·27). Among HIV-positive individuals, the number of incident cases was 1·40 million (1·01-1·89) and the number of tuberculosis deaths was 0·24 million (0·16-0·31). Globally, among HIV-negative individuals the agestandardised incidence of tuberculosis decreased annually at a slower rate (-1·3% [-1·5 to -1·2]) than mortality did (-4·5% [-5·0 to -4·1]) from 2006 to 2016. Among HIV-positive individuals during the same period, the rate of change in annualised age-standardised incidence was -4·0% (-4·5 to -3·7) and mortality was -8·9% (-9·5 to -8·4). Several regions had higher rates of age-standardised incidence and mortality than expected on the basis of their SDI levels in 2016. For drug-susceptible tuberculosis, the highest observed-to-expected ratios were in southern sub-Saharan Africa (13·7 for incidence and 14·9 for mortality), and the lowest ratios were in high-income North America (0·4 for incidence) and Oceania (0·3 for mortality). For multidrug-resistant tuberculosis, eastern Europe had the highest observed-to-expected ratios (67·3 for incidence and 73·0 for mortality), and high-income North America had the lowest ratios (0·4 for incidence and 0·5 for mortality). Interpretation If current trends in tuberculosis incidence continue, few countries are likely to meet the SDG target to end the tuberculosis epidemic by 2030. Progress needs to be accelerated by improving the quality of and access to tuberculosis diagnosis and care, by developing new tools, scaling up interventions to prevent risk factors for tuberculosis, and integrating control programmes for tuberculosis and HIV. Funding Bill & Melinda Gates Foundation. © 2018 The Author(s).

Affiliations

Department of Health Metrics Sciences, United States; Institute for Health Metrics and Evaluation, Seattle, 98121, WA, United States; Department of Global Health and Infection, Brighton and Sussex Medical School, Brighton, United Kingdom; University of Washington, Seattle, WA, United States; Department of Nephrology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India; Department of Paediatrics, United States; All India Institute of Medical Sciences, New Delhi, India; Evidence Based Practice Center, Mayo Clinic Foundation for Medical Education and Research, Rochester, MN, United States; University Institute of Public Health, University of Lahore, Lahore, Pakistan; Department of Medical Microbiology, United States; Epidemiology and Biostatistics Department, Health Services Academy, Islamabad, Pakistan; Human Nutrition Department, United States; University of Gondar, Gondar, Ethiopia; Research School of Population Health, Australian National University, Canberra, ACT, Australia; Medical Technical Institute, Erbil Polytechnic University, Erbil, Iraq; Faculty of Pharmacy, United States; Ishik University, Erbil, Iraq; Research Group on Health Economics, University of Cartagena, Cartagena, Colombia; Research Group in Hospital Management and Health Policies, University of the Coast, Barranquilla, Colombia; Division of Infectious Disease and Geographic Medicine, United States; Center for Health Policy, Center for Primary Care and Outcomes Research, United States; Stanford University, Stanford, CA, United States; Department of Health Policy and Administration, United States; Development and Communication Studies, United States; University of the Philippines Manila, Manila, Philippines; University of Hail, Hail, Saudi Arabia; Center for Clinical Global Health Education, United States; Department of Epidemiology, University of Pittsburgh, Pittsburgh, PA, United States; Johns Hopkins University, Baltimore, MD, United States; Dr. D.y. Patil Medical College, Dr. D.y. Patil Vidyapeeth, Pune, India; Indian Institute of Public Health, Gandhinagar, India; Public Health Foundation of India, Gurugram, India; Department of Epidemiology, Biostatistics, and Occupational Health, McGill University, Montreal, QC, Canada; Public Health Department, Dilla University, Dilla, Ethiopia; Department of Medical Mycology, United States; Toxoplasmosis Research Center, United States; Health Sciences Research Center, United States; Invasive Fungi Research Center, United States; Mazandaran University of Medical Sciences, Sari, Iran; Public Health Risk Sciences Division, Public Health Agency of Canada, Toronto, ON, Canada; Department of Nutritional Sciences, University of Toronto, Toronto, ON, Canada; Clinic for Infectious and Tropical Diseases, Clinical Center of Serbia, Belgrade, Serbia; Faculty of Medicine, University of Belgrade, Belgrade, Serbia; Department of Community Medicine, Gandhi Medical College Bhopal, Bhopal, India; Jazan University, Jazan, Saudi Arabia; Health Management and Economics Research Center, Iran University of Medical Sciences, Tehran, Iran; Social Determinants of Health Research Center, United States; Lorestan University of Medical Sciences, Khorramabad, Iran; Mizan-Tepi University, Teppi, Ethiopia; Dr. Tewelde Legesse Health Sciences College, Mekelle, Ethiopia; Department of Internal Medicine, University of São Paulo, São Paulo, Brazil; School of Population and Public Health, University of British Columbia, Vancouver, BC, Canada; Al Shifa School of Public Health, Al Shifa Trust Eye Hospital, Rawalpindi, Pakistan; REQUIMTE/LAQV, United States; Ucibio, United States; Applied Molecular Biosciences Unit, United States; University of Porto, Porto, Portugal; Department of Pulmonary Medicine, Christian Medical College and Hospital (CMC), Vellore, India; College of Medicine and Health Sciences, Hawassa University, Hawassa, Ethiopia; School of Public Health, Addis Ababa University, Addis Ababa, Ethiopia; Department of Community Medicine, University of Peradeniya, Peradeniya, Sri Lanka; Department of Population and Health, University of Cape Coast, Cape Coast, Ghana; Faculty of Social Sciences, Health Sciences, University of Tampere, Tampere, Finland; United Nations World Food Programme, New Delhi, India; School of Pharmacy, United States; Department of Medical Laboratory Science, United States; Haramaya University, Harar, Ethiopia; Department of Public Health Sciences, Karolinska Institutet, Stockholm, Sweden; Department of Microbiology and Immunology, Suez Canal University, Ismailia, Egypt; Department of Public Health Medicine, Bielefeld University, Bielefeld, Germany; Tuberculosis, Manhiça Health Research Center, Manhiça, Mozambique; Tuberculosis Department, Barcelona Institute for Global Health, Barcelona, Spain; Biomedical Sciences Division, United States; Department of Nutrition and Dietetics, United States; Clinical Pharmacy Unit, United States; School of Medicine, Xiamen University Malaysia, Sepang, Malaysia; Mekelle University, Mekelle, Ethiopia; Nursing and Health Sciences Department, University of Massachusetts Boston, Boston, MA, United States; Tuberculosis Biomarker Research Unit, Institute for Scientific Research and High Technology Services, City Of Knowledge, Panama; Commissioner of Public Health, West Virginia Bureau for Public Health, Charleston, WV, United States; Department of Health Policy, Management and Leadership, West Virginia University School of Public Health, Morgantown, WV, United States; Institute for Global Health, University College London, London, United Kingdom; Unit of Epidemiology and Social Medicine, University Hospital Antwerp, Wilrijk, Belgium; Faculty of Dentistry, Dept of Legal Medicine and Bioethics, Carol Davila University of Medicine and Pharmacy, Bucharest, Romania; Department of Health Education and Behavioral Sciences, Jimma University, Jimma, Ethiopia; Department of Public Health and Community Medicine, University of Liberia, Monrovia, Liberia; Research Institute for Endocrine Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran; Non-communicable Diseases Research Center, Alborz University of Medical Sciences, Karaj, Iran; Hematology-Oncology and Stem Cell Transplantation Research Center, United States; Community-Based Participatory-Research Center CBPR, United States; Department of Health Management and Economics, United States; Center of Expertise in Microbiology, United States; Hematologic Malignancies Research Center, United States; Knowledge Utilization Research Center, United States; Tehran University of Medical Sciences, Tehran, Iran; Department of Global and Community Health, George Mason University, Fairfax, VA, United States; Department of Ophthalmology, United States; Heidelberg University, Mannheim, Germany; Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Beijing, China; Department of Respiratory Medicine, King George's Medical University, Lucknow, India; Department of Public Health and Community Medicine, Jordan University of Science and Technology, Ramtha, Jordan; Department of Public Health, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran; Institute of Health Policy and Management, United States; Seoul National University, Seoul, South Korea; Department of Public Health, Erasmus University Medical Center, Rotterham, Netherlands; Research and Development Unit, San Juan de Dios Sanitary Park, Sant Boi De Llobregat, Spain; Department of Public Health, Debre Markos University, Debre Markos, Ethiopia; Ariadne Labs, Harvard University, Boston, MA, United States; Campus Caucaia, Federal Institute of Education, Science and Technology of Ceará, Caucaia, Brazil; College of Health Sciences, Debre Tabor University, Debre Tabor, Ethiopia; Research Department Prince Mohammed Bin Abdulaziz Hospital, Ministry of Health, Riyadh, Saudi Arabia; College of Medicine, Alfaisal University, Riyadh, Saudi Arabia; Peru Country Office, United Nations Population Fund, UNFPA, Lima, Peru; Department of Pharmacy, Wollo University, Dessie, Ethiopia; Clinical Microbiology and Parasitology Unit, Dr. Zora Profozic Polyclinic, Zagreb, Croatia; University Centre Varazdin, University North, Varazdin, Croatia; Institute of Addiction Research, Frankfurt University of Applied Sciences, Frankfurt, Germany; Department of Biology, Salahaddin University, Erbil, Iraq; Health Systems and Policy Research Unit, Ahmadu Bello University, Zaria, Nigeria; Pediatrics Department, Nishtar Medical University, Multan, Pakistan; Pediatrics and Pediatric Pulmonology, Institute of Mother and Child Care, Multan, Pakistan; Center for Excellence in Behavioral Health, United States; Center of Excellence in Behavioral Medicine, United States; Nguyen Tat Thanh University, Ho Chi Minh City, Viet Nam; Public Health Science Department, State University of Semarang, Kota Semarang, Indonesia; Graduate Institute of Biomedical Informatics, Taipei Medical University, Taipei City, Taiwan; Institute for Global Health Innovations, Duy Tan University, Hanoi, Viet Nam; Centre of Cardiovascular Research and Education in Therapeutics, Monash University, Melbourne, VIC, Australia; Independent Consultant, Accra, Ghana; Western Sydney University, Penrith, NSW, Australia; Department of Preventive Medicine, Kyung Hee University, Dongdaemun-gu, South Korea; Human Sciences Research Council, Durban, South Africa; School of Public Health, Faculty of Health Sciences, University of Namibia, Osakhati, Namibia; University of Adelaide, Adelaide, SA, Australia; Department of Psychiatry, University of Lagos, Lagos, Nigeria; Graduate School of Public Health, San Diego State University, San Diego, CA, United States; Cartagena University, Cartagena, Colombia; Department of Epidemiology and Biostatistics, Contech School of Public Health, Lahore, Pakistan; Society for Health and Demographic Surveillance, Suri, India; Department of Economics, University of Goettingen, Göttingen, Germany; Department of Public Health and Mortality Studies, International Institute for Population Sciences, Mumbai, India; Department of Biomedical Science, University of Sassari, Sassari, Italy; Managerial Epidemiology Research Center, Maragheh University of Medical Sciences, Maragheh, Iran; Department of Entomology, Ain Shams University, Cairo, Egypt; Department of Public Health Medicine, University of Kwazulu-natal, Durban, South Africa; Ugc Centre of Advanced Study in Psychology, Utkal University, Bhubaneswar, India; Udyam-global Association for Sustainable Development, Bhubaneswar, India; Department of Basic Sciences, Islamic Azad University, Sari, Iran; Brasília University, Brasília, Brazil; Department of the Health Industrial Complex and Innovation in Health, Federal Ministry of Health, Brasília, Brazil; Department of Medicine, United States; University of Alabama at Birmingham, Birmingham, AL, United States; Division of Community Medicine, International Medical University, Kuala Lumpur, Malaysia; Department of Health Economics, Hanoi Medical University, Hanoi, Viet Nam; Department of Internal Medicine, Federal Teaching Hospital, Abakaliki, Nigeria; Gomal University, Dera Ismail Khan, Pakistan; Tb Culture Laboratory, Mufti Mehmood Memorial Teaching Hospital, Dera Ismail Khan, Pakistan; Division of Health Sciences, University of Warwick, Coventry, United Kingdom; Department of Health Care Administration and Economy, National Research University Higher School of Economics, Moscow, Russian Federation; Demographic Change and Ageing Research Area, Federal Institute for Population Research, Wiesbaden, Germany; Department of Psychopharmacology, National Center of Neurology and Psychiatry, Tokyo, Japan; College of Public Health, Ohio State University, Columbus, OH, United States; School of Public Health, University of Kinshasa, Kinshasa, Congo