The global burden of viral hepatitis from 1990 to 2013: findings from the Global Burden of Disease Study 2013

doi:10.1016/S0140-6736(16)30579-7

Comment

. 2016 Sep 10;388(10049):1081-1088.

doi: 10.1016/S0140-6736(16)30579-7. Epub 2016 Jul 7.

The global burden of viral hepatitis from 1990 to 2013: findings from the Global Burden of Disease Study 2013

Jeffrey D Stanaway¹, Abraham D Flaxman², Mohsen Naghavi², Christina Fitzmaurice³, Theo Vos², Ibrahim Abubakar⁴, Laith J Abu-Raddad⁵, Reza Assadi⁶, Neeraj Bhala⁷, Benjamin Cowie⁸, Mohammad H Forouzanfour², Justina Groeger⁹, Khayriyyah Mohd Hanafiah¹⁰, Kathryn H Jacobsen¹¹, Spencer L James¹², Jennifer MacLachlan⁸, Reza Malekzadeh¹³, Natasha K Martin¹⁴, Ali A Mokdad¹⁵, Ali H Mokdad², Christopher J L Murray², Dietrich Plass¹⁶, Saleem Rana¹⁷, David B Rein¹⁸, Jan Hendrik Richardus¹⁹, Juan Sanabria²⁰, Mete Saylan²¹, Saeid Shahraz²², Samuel So²³, Vasiliy V Vlassov²⁴, Elisabete Weiderpass²⁵, Steven T Wiersma²⁶, Mustafa Younis²⁷, Chuanhua Yu²⁸, Maysaa El Sayed Zaki²⁹, Graham S Cooke³⁰

Affiliations

¹ Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA. Electronic address: stanaway@uw.edu.
² Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA.
³ Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA; Division of Hematology, Department of Medicine, University of Washington, Seattle, WA, USA.
⁴ Institute for Global Health, University College London, London, UK.
⁵ Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Qatar Foundation, Doha, Qatar.
⁶ Mashhad University of Medical Sciences, Mashhad, Iran.
⁷ Queen Elizabeth Hospital Birmingham, Birmingham, UK; University of Otago Medical School, Wellington, New Zealand.
⁸ WHO Collaborating Centre for Viral Hepatitis, Victorian Infectious Diseases Reference Laboratory, Melbourne, VIC, Australia; Doherty Institute, University of Melbourne, Melbourne, VIC, Australia.
⁹ Johns Hopkins Bayview Medical Center, Baltimore, MD, USA.
¹⁰ Centre for Biomedical Research, Burnet Institute, Melbourne, VIC, Australia; School of Biological Sciences, Universiti Sains Malaysia, Penang, Malaysia.
¹¹ Department of Global and Community Health, George Mason University, Fairfax, VA, USA.
¹² Geisel School of Medicine at Dartmouth, Dartmouth College, Hanover, NH, USA.
¹³ Digestive Disease Research Institute, Tehran University of Medical Sciences, Tehran, Iran.
¹⁴ Division of Global Public Health, University of California San Diego, San Diego, CA, USA; School of Social and Community Medicine, University of Bristol, Bristol, UK.
¹⁵ Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.
¹⁶ Section Exposure Assessment and Environmental Health Indicators, Federal Environmental Agency, Berlin, Germany.
¹⁷ Contech School of Public Health, Lahore, Pakistan; Contech International Health Consultants, Lahore, Pakistan.
¹⁸ NORC at the University of Chicago, Chicago, IL, USA.
¹⁹ Department of Public Health, Erasmus MC, University Medical Center Rotterdam, Rotterdam, Netherlands.
²⁰ Case Western Reserve University, Cleveland, OH, USA; Cancer Treatment Centers of America, Rosalind Franklin University Chicago Medical School, North Chicago, IL, USA.
²¹ Bayer AG Turkey, Fatih Sultan Mehmet Mah Balkan Cad, Istanbul, Turkey.
²² Tufts Medical Center, Boston, MA, USA.
²³ Asian Liver Center, Stanford University School of Medicine, Palo Alto, CA, USA.
²⁴ National Research University Higher School of Economics, Moscow, Russia.
²⁵ Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden; Department of Research, Cancer Registry of Norway, Oslo, Norway; Department of Community Medicine, Faculty of Health Sciences, University of Tromsø-The Arctic University of Norway, Tromsø, Norway; Genetic Epidemiology Group, Folkhälsan Research Center, University of Helsinki, Helsinki, Finland.
²⁶ US Centers for Disease Control and Prevention, Kampala, Uganda.
²⁷ Jackson State University, Jackson, MS, USA.
²⁸ Department of Epidemiology and Biostatistics, School of Public Health, and Global Health Institute, Wuhan University, Wuhan, Hubei, China.
²⁹ Faculty of Medicine, Mansoura University, Mansoura, Egypt.
³⁰ Division of Infectious Diseases, Imperial College, London, UK. Electronic address: g.cooke@imperial.ac.uk.

PMID: 27394647
PMCID: PMC5100695
DOI: 10.1016/S0140-6736(16)30579-7

Comment

The global burden of viral hepatitis from 1990 to 2013: findings from the Global Burden of Disease Study 2013

Jeffrey D Stanaway et al. Lancet. 2016.

. 2016 Sep 10;388(10049):1081-1088.

doi: 10.1016/S0140-6736(16)30579-7. Epub 2016 Jul 7.

Authors

Affiliations

¹ Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA. Electronic address: stanaway@uw.edu.
² Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA.
³ Institute for Health Metrics and Evaluation, University of Washington, Seattle, WA, USA; Division of Hematology, Department of Medicine, University of Washington, Seattle, WA, USA.
⁴ Institute for Global Health, University College London, London, UK.
⁵ Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, Qatar Foundation, Doha, Qatar.
⁶ Mashhad University of Medical Sciences, Mashhad, Iran.
⁷ Queen Elizabeth Hospital Birmingham, Birmingham, UK; University of Otago Medical School, Wellington, New Zealand.
⁸ WHO Collaborating Centre for Viral Hepatitis, Victorian Infectious Diseases Reference Laboratory, Melbourne, VIC, Australia; Doherty Institute, University of Melbourne, Melbourne, VIC, Australia.
⁹ Johns Hopkins Bayview Medical Center, Baltimore, MD, USA.
¹⁰ Centre for Biomedical Research, Burnet Institute, Melbourne, VIC, Australia; School of Biological Sciences, Universiti Sains Malaysia, Penang, Malaysia.
¹¹ Department of Global and Community Health, George Mason University, Fairfax, VA, USA.
¹² Geisel School of Medicine at Dartmouth, Dartmouth College, Hanover, NH, USA.
¹³ Digestive Disease Research Institute, Tehran University of Medical Sciences, Tehran, Iran.
¹⁴ Division of Global Public Health, University of California San Diego, San Diego, CA, USA; School of Social and Community Medicine, University of Bristol, Bristol, UK.
¹⁵ Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.
¹⁶ Section Exposure Assessment and Environmental Health Indicators, Federal Environmental Agency, Berlin, Germany.
¹⁷ Contech School of Public Health, Lahore, Pakistan; Contech International Health Consultants, Lahore, Pakistan.
¹⁸ NORC at the University of Chicago, Chicago, IL, USA.
¹⁹ Department of Public Health, Erasmus MC, University Medical Center Rotterdam, Rotterdam, Netherlands.
²⁰ Case Western Reserve University, Cleveland, OH, USA; Cancer Treatment Centers of America, Rosalind Franklin University Chicago Medical School, North Chicago, IL, USA.
²¹ Bayer AG Turkey, Fatih Sultan Mehmet Mah Balkan Cad, Istanbul, Turkey.
²² Tufts Medical Center, Boston, MA, USA.
²³ Asian Liver Center, Stanford University School of Medicine, Palo Alto, CA, USA.
²⁴ National Research University Higher School of Economics, Moscow, Russia.
²⁵ Department of Medical Epidemiology and Biostatistics, Karolinska Institute, Stockholm, Sweden; Department of Research, Cancer Registry of Norway, Oslo, Norway; Department of Community Medicine, Faculty of Health Sciences, University of Tromsø-The Arctic University of Norway, Tromsø, Norway; Genetic Epidemiology Group, Folkhälsan Research Center, University of Helsinki, Helsinki, Finland.
²⁶ US Centers for Disease Control and Prevention, Kampala, Uganda.
²⁷ Jackson State University, Jackson, MS, USA.
²⁸ Department of Epidemiology and Biostatistics, School of Public Health, and Global Health Institute, Wuhan University, Wuhan, Hubei, China.
²⁹ Faculty of Medicine, Mansoura University, Mansoura, Egypt.
³⁰ Division of Infectious Diseases, Imperial College, London, UK. Electronic address: g.cooke@imperial.ac.uk.

PMID: 27394647
PMCID: PMC5100695
DOI: 10.1016/S0140-6736(16)30579-7

Abstract

Background: With recent improvements in vaccines and treatments against viral hepatitis, an improved understanding of the burden of viral hepatitis is needed to inform global intervention strategies. We used data from the Global Burden of Disease (GBD) Study to estimate morbidity and mortality for acute viral hepatitis, and for cirrhosis and liver cancer caused by viral hepatitis, by age, sex, and country from 1990 to 2013.

Methods: We estimated mortality using natural history models for acute hepatitis infections and GBD's cause-of-death ensemble model for cirrhosis and liver cancer. We used meta-regression to estimate total cirrhosis and total liver cancer prevalence, as well as the proportion of cirrhosis and liver cancer attributable to each cause. We then estimated cause-specific prevalence as the product of the total prevalence and the proportion attributable to a specific cause. Disability-adjusted life-years (DALYs) were calculated as the sum of years of life lost (YLLs) and years lived with disability (YLDs).

Findings: Between 1990 and 2013, global viral hepatitis deaths increased from 0·89 million (95% uncertainty interval [UI] 0·86-0·94) to 1·45 million (1·38-1·54); YLLs from 31·0 million (29·6-32·6) to 41·6 million (39·1-44·7); YLDs from 0·65 million (0·45-0·89) to 0·87 million (0·61-1·18); and DALYs from 31·7 million (30·2-33·3) to 42·5 million (39·9-45·6). In 2013, viral hepatitis was the seventh (95% UI seventh to eighth) leading cause of death worldwide, compared with tenth (tenth to 12th) in 1990.

Interpretation: Viral hepatitis is a leading cause of death and disability worldwide. Unlike most communicable diseases, the absolute burden and relative rank of viral hepatitis increased between 1990 and 2013. The enormous health loss attributable to viral hepatitis, and the availability of effective vaccines and treatments, suggests an important opportunity to improve public health.

Funding: Bill & Melinda Gates Foundation.

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Figures

**Figure 1. Decomposed drivers of global changes in DALYs attributable to viral hepatitis between 1990 and 2013, by virus and for all hepatitis viruses combined**
Error bars represent 95% uncertainty intervals. DALYs=disability-adjusted life-years.

**Figure 2. Leading causes of mortality and trends, 1990–2013**
COPD=chronic obstructive pulmonary disease.

**Figure 3. Map of viral hepatitis-related, age-standardised mortality rate, by GBD region**
Overlaid pie charts indicate each virus type’s contribution to the total hepatitis-related mortality; the size of the pie charts are proportional to the region’s hepatitis-attributable mortality rate. GBD=Global Burden of Disease.

**Figure 4**
Age-standardised disability-adjusted life-year rates (per 100 000 per year) attributable to hepatitis A, B, C, and E viruses in 2013, by country

**Figure 5. Burden of viral hepatitis, stratified by economic status**
(A) Annual deaths and (B) DALYs of viral hepatitis. Error bars indicate 95% uncertainty intervals. DALYs=disability-adjusted life-years.

See this image and copyright information in PMC

Comment in

The global burden of viral hepatitis: better estimates to guide hepatitis elimination efforts.
Wiktor SZ, Hutin YJ. Wiktor SZ, et al. Lancet. 2016 Sep 10;388(10049):1030-1031. doi: 10.1016/S0140-6736(16)31018-2. Epub 2016 Jul 7. Lancet. 2016. PMID: 27394646 No abstract available.
Viral hepatitis: The global burden of viral hepatitis is increasing.
Ray K. Ray K. Nat Rev Gastroenterol Hepatol. 2016 Sep;13(9):499. doi: 10.1038/nrgastro.2016.121. Epub 2016 Jul 27. Nat Rev Gastroenterol Hepatol. 2016. PMID: 27485784 No abstract available.
Hepatitis C: the path towards effective universal therapy.
Piroth L, Rabaud C, Rey D, Schmit JL, Chirouze C, Beck-Wirth G, Robineau O, Bani-Sadr F; ICONE Study Group. Piroth L, et al. Lancet. 2016 Sep 10;388(10049):1051-1052. doi: 10.1016/S0140-6736(16)31540-9. Lancet. 2016. PMID: 27628513 No abstract available.
Estimating the burden of hepatitis.
Livinec B. Livinec B. Lancet. 2016 Dec 3;388(10061):2738-2739. doi: 10.1016/S0140-6736(16)31649-X. Epub 2016 Dec 2. Lancet. 2016. PMID: 27924771 No abstract available.
Addressing the increasing global burden of viral hepatitis.
Brown CR, MacLachlan JH, Cowie BC. Brown CR, et al. Hepatobiliary Surg Nutr. 2017 Aug;6(4):274-276. doi: 10.21037/hbsn.2017.05.02. Hepatobiliary Surg Nutr. 2017. PMID: 28848753 Free PMC article. No abstract available.
The evolution of the burden of viral hepatitis from 1990 to 2013: still an open challenge to global public health policy.
Franco E, Pettinicchio V, Zorzoli E. Franco E, et al. Hepatobiliary Surg Nutr. 2017 Aug;6(4):277-279. doi: 10.21037/hbsn.2017.05.01. Hepatobiliary Surg Nutr. 2017. PMID: 28848754 Free PMC article. No abstract available.

Comment on

The global burden of viral hepatitis: better estimates to guide hepatitis elimination efforts.
Wiktor SZ, Hutin YJ. Wiktor SZ, et al. Lancet. 2016 Sep 10;388(10049):1030-1031. doi: 10.1016/S0140-6736(16)31018-2. Epub 2016 Jul 7. Lancet. 2016. PMID: 27394646 No abstract available.

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References

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[1] Rein DB, Stevens GA, Theaker J, Wittenborn JS, Wiersma ST. The global burden of hepatitis E virus genotypes 1 and 2 in 2005. Hepatology. 2012;55:988–97. - PubMed

[2] Rein DB, Stevens GA, Theaker J, Wittenborn JS, Wiersma ST. The global burden of hepatitis E virus genotypes 1 and 2 in 2005. Hepatology. 2012;55:988–97. - PubMed

[3] Jacobsen KH, Wiersma ST. Hepatitis A virus seroprevalence by age and world region, 1990 and 2005. Vaccine. 2010;28:6653–57. - PubMed

[4] Jacobsen KH, Wiersma ST. Hepatitis A virus seroprevalence by age and world region, 1990 and 2005. Vaccine. 2010;28:6653–57. - PubMed

[5] Ott JJ, Stevens GA, Groeger J, Wiersma ST. Global epidemiology of hepatitis B virus infection: new estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine. 2012;30:2212–19. - PubMed

[6] Ott JJ, Stevens GA, Groeger J, Wiersma ST. Global epidemiology of hepatitis B virus infection: new estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine. 2012;30:2212–19. - PubMed

[7] Mohd Hanafiah K, Groeger J, Flaxman AD, Wiersma ST. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology. 2013;57:1333–42. - PubMed

[8] Mohd Hanafiah K, Groeger J, Flaxman AD, Wiersma ST. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology. 2013;57:1333–42. - PubMed

[9] Schweitzer A, Horn J, Mikolajczyk RT, Krause G, Ott JJ. Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet. 2015;386:1546–55. - PubMed

[10] Schweitzer A, Horn J, Mikolajczyk RT, Krause G, Ott JJ. Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet. 2015;386:1546–55. - PubMed

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The global burden of viral hepatitis from 1990 to 2013: findings from the Global Burden of Disease Study 2013

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The global burden of viral hepatitis from 1990 to 2013: findings from the Global Burden of Disease Study 2013

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