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Global, regional, and national sex differences in the global burden of tuberculosis by HIV status, 1990–2019: results from the Global Burden of Disease Study 2019

journal contribution
submitted on 2024-04-17, 07:31 and posted on 2024-04-17, 07:32 authored by Jorge R Ledesma, Jianing Ma, Avina Vongpradith, Emilie R Maddison, Amanda Novotney, Molly H Biehl, Kate E LeGrand, Jennifer M Ross, Deepa Jahagirdar, Dana Bryazka, Rachel Feldman, Hassan Abolhassani, Akine Eshete Abosetugn, Eman Abu-Gharbieh, Oladimeji M Adebayo, Qorinah Estiningtyas Sakilah Adnani, Saira Afzal, Bright Opoku Ahinkorah, Sajjad Ahmad Ahmad, Sepideh Ahmadi, Tarik Ahmed Rashid, Yusra Ahmed Salih, Addis Aklilu, Chisom Joyqueenet Akunna, Hanadi Al Hamad, Fares Alahdab, Yosef Alemayehu, Kefyalew Addis Alene, Beriwan Abdulqadir Ali, Liaqat Ali, Vahid Alipour, Hesam Alizade, Rajaa M Al-Raddadi, Nelson Alvis-Guzman, Saeed Amini, Arianna Maever L Amit, Jason A Anderson, Sofia Androudi, Carl Abelardo T Antonio, Catherine M Antony, Razique Anwer, Jalal Arabloo, Asrat Arja, Mulusew A Asemahagn, Sachin R Atre, Gulrez Shah Azhar, Darshan B B, Zaheer-Ud-Din Babar, Atif Amin Baig, Maciej Banach, Hiba Jawdat Barqawi, Fabio Barra, Amadou Barrow, Sanjay Basu, Uzma Iqbal Belgaumi, Akshaya Srikanth Bhagavathula, Nikha Bhardwaj, Pankaj Bhardwaj, Natalia V Bhattacharjee, Krittika Bhattacharyya, Ali Bijani, Boris Bikbov, Archith Boloor, Nikolay Ivanovich Briko, Danilo Buonsenso, Sharath Burugina Nagaraja, Zahid A Butt, Austin Carter, Felix Carvalho, Jaykaran Charan, Souranshu Chatterjee, Soosanna Kumary Chattu, Vijay Kumar Chattu, Devasahayam J Christopher, Dinh-Toi Chu, Mareli M Claassens, Omid Dadras, Amare Belachew Dagnew, Xiaochen Dai, Lalit Dandona, Rakhi Dandona, Parnaz Daneshpajouhnejad, Aso Mohammad Darwesh, Deepak Dhamnetiya, Mostafa Dianatinasab, Daniel Diaz, Linh Phuong Doan, Sahar Eftekharzadeh, Muhammed Elhadi, Amir Emami, Shymaa Enany, Emerito Jose A Faraon, Farshad Farzadfar, Eduarda Fernandes, Lorenzo Ferro Desideri, Irina Filip, Florian Fischer, Masoud Foroutan, Tahvi D Frank, Alberto L Garcia-Basteiro, Christian Garcia-Calavaro, Tushar Garg, Biniyam Sahiledengle Geberemariyam, Keyghobad Ghadiri, Ahmad Ghashghaee, Mahaveer Golechha, Amador Goodridge, Bhawna Gupta, Sapna Gupta, Veer Bala Gupta, Vivek Kumar Gupta, Mohammad Rifat Haider, Samer Hamidi, Asif Hanif, Shafiul Haque, Harapan Harapan, Arief Hargono, Ahmed I Hasaballah, Abdiwahab Hashi, Shoaib Hassan, Hadi Hassankhani, Khezar Hayat, Kamal Hezam, Ramesh Holla, Mehdi Hosseinzadeh, Mihaela Hostiuc, Mowafa Househ, Rabia Hussain, Segun Emmanuel Ibitoye, Irena M Ilic, Milena D Ilic, Seyed Sina Naghibi Irvani, Nahlah Elkudssiah Ismail, Ramaiah Itumalla, Jalil Jaafari, Kathryn H Jacobsen, Vardhmaan Jain, Fatemeh Javanmardi, Sathish Kumar Jayapal, Shubha Jayaram, Ravi Prakash Jha, Jost B Jonas, Nitin Joseph, Farahnaz Joukar, Zubair Kabir, Ashwin Kamath, Tanuj Kanchan, Himal Kandel, Patrick DMC Katoto, Gbenga A Kayode, Parkes J Kendrick, Amene Abebe Kerbo, Himanshu Khajuria, Rovshan Khalilov, Khaled Khatab, Abdullah T Khoja, Jagdish Khubchandani, Min Seo Kim, Yun Jin Kim, Adnan Kisa, Sezer Kisa, Soewarta Kosen, Parvaiz A Koul, Sindhura Lakshmi Koulmane Laxminarayana, Ai Koyanagi, Kewal Krishan, Burcu Kucuk Bicer, Avinash Kumar, G Anil Kumar, Narinder Kumar, Nithin Kumar, Alexander Kwarteng, Hassan Mehmood Lak, Dharmesh Kumar Lal, Iván Landires, Savita Lasrado, Shaun Wen Huey Lee, Wei-Chen Lee, Christine Lin, Xuefeng Liu, Platon D Lopukhov, Rafael Lozano, Daiane Borges Machado, Shilpashree Madhava Kunjathur, Deepak Madi, Preetam Bhalchandra Mahajan, Azeem Majeed, Ahmad Azam Malik, Francisco Rogerlândio Martins-Melo, Saurabh Mehta, Ziad A Memish, Walter Mendoza, Ritesh G Menezes, Hayimro Edemealem Merie, Amanual Getnet Mersha, Mohamed Kamal Mesregah, Tomislav Mestrovic, Nour Mheidly Mheidly, Sanjeev Misra, Prasanna Mithra, Masoud Moghadaszadeh, Mokhtar Mohammadi, Abdollah Mohammadian-Hafshejani, Shafiu Mohammed, Mariam Molokhia, Mohammad Ali Moni, Ahmed Al Montasir, Catrin E Moore, Ahamarshan Jayaraman Nagarajan, Sanjeev Nair, Suma Nair, Atta Abbas Naqvi, Sreenivas Narasimha Swamy, Biswa Prakash Nayak, Javad Nazari, Sandhya Neupane Kandel, Trang Huyen Nguyen, Molly R Nixon, Chukwudi A Nnaji, Mpiko Ntsekhe, Virginia Nuñez-Samudio, Bogdan Oancea, Oluwakemi Ololade Odukoya, Andrew T Olagunju, Eyal Oren, Mahesh P A, Ramakrishnan Parthasarathi, Fatemeh Pashazadeh Kan, Sanjay M Pattanshetty, Rajan Paudel, Pintu Paul, Shrikant Pawar, Veincent Christian Filipino Pepito, Norberto Perico, Majid Pirestani, Roman V Polibin, Maarten J Postma, Akram Pourshams, Akila Prashant, Dimas Ria Angga Pribadi, Amir Radfar, Alireza Rafiei, Fakher Rahim, Vafa Rahimi-Movaghar, Mahfuzar Rahman, Mosiur Rahman, Amir Masoud Rahmani, Priyanga Ranasinghe, Chythra R Rao, David Laith Rawaf, Salman Rawaf, Marissa B Reitsma, Giuseppe Remuzzi, Andre M N Renzaho, Melese Abate Reta, Nima Rezaei, Omid Rezahosseini, Mohammad sadegh Rezai, Aziz Rezapour, Gholamreza Roshandel, Denis O Roshchin, Siamak Sabour, KM Saif-Ur-Rahman, Nasir Salam, Hossein Samadi Kafil, Mehrnoosh Samaei, Abdallah M Samy, Satish Saroshe, Benn Sartorius, Brijesh Sathian, Susan M Sawyer, Subramanian Senthilkumaran, Allen Seylani, Omid Shafaat, Masood Ali Shaikh, Kiomars Sharafi, Ranjitha S Shetty, Mika Shigematsu, Jae Il Shin, João Pedro Silva, Jitendra Kumar Singh, Smriti Sinha, Valentin Yurievich Skryabin, Anna Aleksandrovna Skryabina, Emma Elizabeth Spurlock, Chandrashekhar T Sreeramareddy, Paschalis Steiropoulos, Mu'awiyyah Babale Sufiyan, Takahiro Tabuchi, Eyayou Girma Tadesse, Zemenu Tamir, Elvis Enowbeyang Tarkang, Yohannes Tekalegn, Fisaha Haile Tesfay, Belay Tessema, Rekha Thapar, Imad I Tleyjeh, Ruoyan Tobe-Gai, Bach Xuan Tran, Berhan Tsegaye, Gebiyaw Wudie Tsegaye, Anayat Ullah, Chukwuma David Umeokonkwo, Sahel Valadan Tahbaz, Bay Vo, Giang Thu Vu, Yasir Waheed, Magdalene K Walters, Joanna L Whisnant, Mesfin Agachew Woldekidan, Befikadu Legesse Wubishet, Seyed Hossein Yahyazadeh Jabbari, Taklo Simeneh Yazie Yazie, Yigizie Yeshaw, Siyan Yi, Vahit Yiğit, Naohiro Yonemoto, Chuanhua Yu, Ismaeel Yunusa, Mikhail Sergeevich Zastrozhin, Anasthasia Zastrozhina, Zhi-Jiang Zhang, Alimuddin Zumla, Ali H Mokdad, Joshua A Salomon, Robert C Reiner Jr, Stephen S Lim, Mohsen Naghavi, Theo Vos, Simon I Hay, Christopher J L Murray, Hmwe Hmwe Kyu

Background

Tuberculosis is a major contributor to the global burden of disease, causing more than a million deaths annually. Given an emphasis on equity in access to diagnosis and treatment of tuberculosis in global health targets, evaluations of differences in tuberculosis burden by sex are crucial. We aimed to assess the levels and trends of the global burden of tuberculosis, with an emphasis on investigating differences in sex by HIV status for 204 countries and territories from 1990 to 2019.

Methods

We used a Bayesian hierarchical Cause of Death Ensemble model (CODEm) platform to analyse 21 505 site-years of vital registration data, 705 site-years of verbal autopsy data, 825 site-years of sample-based vital registration data, and 680 site-years of mortality surveillance data to estimate mortality due to tuberculosis among HIV-negative individuals. We used a population attributable fraction approach to estimate mortality related to HIV and tuberculosis coinfection. A compartmental meta-regression tool (DisMod-MR 2.1) was then used to synthesise all available data sources, including prevalence surveys, annual case notifications, population-based tuberculin surveys, and tuberculosis cause-specific mortality, to produce estimates of incidence, prevalence, and mortality that were internally consistent. We further estimated the fraction of tuberculosis mortality that is attributable to independent effects of risk factors, including smoking, alcohol use, and diabetes, for HIV-negative individuals. For individuals with HIV and tuberculosis coinfection, we assessed mortality attributable to HIV risk factors including unsafe sex, intimate partner violence (only estimated among females), and injection drug use. We present 95% uncertainty intervals for all estimates.

Findings

Globally, in 2019, among HIV-negative individuals, there were 1·18 million (95% uncertainty interval 1·08–1·29) deaths due to tuberculosis and 8·50 million (7·45–9·73) incident cases of tuberculosis. Among HIV-positive individuals, there were 217 000 (153 000–279 000) deaths due to tuberculosis and 1·15 million (1·01–1·32) incident cases in 2019. More deaths and incident cases occurred in males than in females among HIV-negative individuals globally in 2019, with 342 000 (234 000–425 000) more deaths and 1·01 million (0·82–1·23) more incident cases in males than in females. Among HIV-positive individuals, 6250 (1820–11 400) more deaths and 81 100 (63 300–100 000) more incident cases occurred among females than among males in 2019. Age-standardised mortality rates among HIV-negative males were more than two times greater in 105 countries and age-standardised incidence rates were more than 1·5 times greater in 74 countries than among HIV-negative females in 2019. The fraction of global tuberculosis deaths among HIV-negative individuals attributable to alcohol use, smoking, and diabetes was 4·27 (3·69–5·02), 6·17 (5·48–7·02), and 1·17 (1·07–1·28) times higher, respectively, among males than among females in 2019. Among individuals with HIV and tuberculosis coinfection, the fraction of mortality attributable to injection drug use was 2·23 (2·03–2·44) times greater among males than females, whereas the fraction due to unsafe sex was 1·06 (1·05–1·08) times greater among females than males.

Interpretation

As countries refine national tuberculosis programmes and strategies to end the tuberculosis epidemic, the excess burden experienced by males is important. Interventions are needed to actively communicate, especially to men, the importance of early diagnosis and treatment. These interventions should occur in parallel with efforts to minimise excess HIV burden among women in the highest HIV burden countries that are contributing to excess HIV and tuberculosis coinfection burden for females. Placing a focus on tuberculosis burden among HIV-negative males and HIV and tuberculosis coinfection among females might help to diminish the overall burden of tuberculosis. This strategy will be crucial in reaching both equity and burden targets outlined by global health milestones.

Funding

Bill & Melinda Gates Foundation.

Other Information

Published in: The Lancet Infectious Diseases
License: http://creativecommons.org/licenses/by/4.0/
See article on publisher's website: https://dx.doi.org/10.1016/s1473-3099(21)00449-7

History

Language

  • English

Publisher

Elsevier

Publication Year

  • 2022

License statement

This Item is licensed under the Creative Commons Attribution 4.0 International License.

Institution affiliated with

  • Hamad Medical Corporation
  • Rumailah Hospital - HMC
  • Hamad Bin Khalifa University
  • College of Science and Engineering - HBKU

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