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

GBD Tuberculosis Collaborators, Hmwe Hmwe Kyu, Emilie R Maddison, Nathaniel J Henry, Jorge R Ledesma, Kirsten E Wiens, Robert Reiner Jr, Molly H Biehl, Chloe Shields, Aaron Osgood-Zimmerman, Jennifer M Ross, Austin Carter, Tahvi D Frank, Haidong Wang, Vinay Srinivasan, 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, GBD Tuberculosis Collaborators, Hmwe Hmwe Kyu, Emilie R Maddison, Nathaniel J Henry, Jorge R Ledesma, Kirsten E Wiens, Robert Reiner Jr, Molly H Biehl, Chloe Shields, Aaron Osgood-Zimmerman, Jennifer M Ross, Austin Carter, Tahvi D Frank, Haidong Wang, Vinay Srinivasan, 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

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 age-standardised 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.

Copyright © 2018 The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. Published by Elsevier Ltd.. All rights reserved.

Figures

Figure 1
Figure 1
Global tuberculosis incidence (A) and mortality (B) by drug-resistance type and HIV status, 1990–2016 Dark lines are estimates and shaded areas are 95% uncertainty intervals. HIV-tuberculosis=tuberculosis in individuals with HIV/AIDS. Multidrug-resistant tuberculosis=multidrug-resistant tuberculosis without extensive drug resistance.
Figure 2
Figure 2
Global age-sex distribution of incident cases of tuberculosis (A) and deaths due to tuberculosis (B) among HIV-negative individuals in 2016 Error bars are 95% uncertainty intervals.
Figure 3
Figure 3
Age-standardised tuberculosis incidence (A) and mortality (B) in HIV-negative individuals, 2016 ATG=Antigua and Barbuda. VCT=Saint Vincent and the Grenadines. LCA=Saint Lucia. TTO=Trinidad and Tobago. Isl=Islands. FSM=Federated States of Micronesia. TLS=Timor-Leste.
Figure 4
Figure 4
Ratio of observed to expected age-standardised incidence and mortality on the basis of SDI by GBD region and country in 2016, for drug-susceptible tuberculosis and multidrug-resistant tuberculosis, by HIV status Ratio of observed age-standardised incidence or mortality to that expected on the basis of a country's SDI for a given year. A ratio of one means that observed and expected values are equal. A ratio higher than one means the observed rate is greater than expected, and a ratio of less than one means the observed rate is lower than expected. GBD=Global Burden of Disease. Multidrug-resistant tuberculosis=multidrug-resistant tuberculosis without extensive drug resistance. SDI=Socio-demographic Index.
Figure 4
Figure 4
Ratio of observed to expected age-standardised incidence and mortality on the basis of SDI by GBD region and country in 2016, for drug-susceptible tuberculosis and multidrug-resistant tuberculosis, by HIV status Ratio of observed age-standardised incidence or mortality to that expected on the basis of a country's SDI for a given year. A ratio of one means that observed and expected values are equal. A ratio higher than one means the observed rate is greater than expected, and a ratio of less than one means the observed rate is lower than expected. GBD=Global Burden of Disease. Multidrug-resistant tuberculosis=multidrug-resistant tuberculosis without extensive drug resistance. SDI=Socio-demographic Index.
Figure 4
Figure 4
Ratio of observed to expected age-standardised incidence and mortality on the basis of SDI by GBD region and country in 2016, for drug-susceptible tuberculosis and multidrug-resistant tuberculosis, by HIV status Ratio of observed age-standardised incidence or mortality to that expected on the basis of a country's SDI for a given year. A ratio of one means that observed and expected values are equal. A ratio higher than one means the observed rate is greater than expected, and a ratio of less than one means the observed rate is lower than expected. GBD=Global Burden of Disease. Multidrug-resistant tuberculosis=multidrug-resistant tuberculosis without extensive drug resistance. SDI=Socio-demographic Index.
Figure 4
Figure 4
Ratio of observed to expected age-standardised incidence and mortality on the basis of SDI by GBD region and country in 2016, for drug-susceptible tuberculosis and multidrug-resistant tuberculosis, by HIV status Ratio of observed age-standardised incidence or mortality to that expected on the basis of a country's SDI for a given year. A ratio of one means that observed and expected values are equal. A ratio higher than one means the observed rate is greater than expected, and a ratio of less than one means the observed rate is lower than expected. GBD=Global Burden of Disease. Multidrug-resistant tuberculosis=multidrug-resistant tuberculosis without extensive drug resistance. SDI=Socio-demographic Index.

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