Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Epidemiology and population health

Association between body mass index and laboratory-confirmed influenza in middle aged and older adults: a prospective cohort study

International Journal of Obesity volume 42, pages 1480–1488 (2018)Cite this article

Subjects

Abstract

Background

Studies conducted during the 2009 influenza A (H1N1) pandemic found that obesity increases the risk of severe influenza including hospitalization and death. In this study, we examined the relationship of BMI with having laboratory-confirmed seasonal influenza and influenza-related respiratory hospitalization.

Methods

We linked a cohort of 246,494 adults aged ≥45 years with data on BMI to subsequent laboratory-confirmed influenza notifications and cause-specific hospitalizations from 2006 to 2015. Cox-proportional hazard models were used to estimate the risk of incident laboratory-confirmed influenza and influenza-related respiratory hospitalizations according to BMI, adjusting for age, sex and other covariates.

Results

After 1,840,408 person-years of follow-up, 1891 participants had laboratory-confirmed influenza notifications (crude rate 10.3/10,000 person-years) of whom 623 were hospitalized for a respiratory illness. Compared to those with healthy BMI (22.5 to <25.0 kg/m2), influenza incidence was respectively 27% (adjusted HR [aHR]: 1.27, 95% CI: 1.10–1.46) and 69% (aHR: 1.69, 1.24–2.29) greater among obese (BMI: 30 to <40 kg/m2) and very obese adults (40 to <50 kg/m2). The equivalent aHRs for hospitalization were 1.57 (95% CI: 1.22–2.01) and 4.81 (95% CI: 3.23–7.17). For every 5-unit BMI increase above 22.5 kg/m2, there was a 15% (aHR: 1.15, 95% CI: 1.09–1.22) increase in risk of having a diagnosis of influenza and 42% increase in hospitalization (aHR: 1.42, 95% CI: 1.30–1.60). These trends did not differ between the pandemic year (2009) and other years.

Conclusions

Our results suggest that obese adults have a similar risk of hospitalization for seasonal influenza as adults with cardiovascular disease and diabetes, and should therefore  be equally prioritized for funded interventions such as targeted immunization programs.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

USD 39.95

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. World Health Organization. Influenza (seasonal), Fact sheet. 2016. http://www.who.int/mediacentre/factsheets/fs211/en/. Accessed 15 May 2017.

  2. Nicholson KG, Wood JM, Zambon M. Influenza. Lancet. 2003;362:1733–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Dyda A, Karki S, Hayen A, MacIntyre CR, Menzies R, Banks E, et al. Influenza and pneumococcal vaccination in Australian adults: a systematic review of coverage and factors associated with uptake. BMC Infect Dis. 2016;16:515.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Blank PR, Szucs TD. Increasing influenza vaccination coverage in recommended population groups in Europe. Expert Rev Vaccin. 2009;8:425–33.

    Article  Google Scholar 

  5. World Health Organization. Obesity and Overweight, Fact sheet. 2016. http://www.who.int/mediacentre/factsheets/fs311/en/. Accessed 15 May 2017.

  6. Australian Bureau of Statistics. National Health Survey, First Results, Australia 2014-2015. http://www.abs.gov.au/AUSSTATS/abs@.nsf/DetailsPage/4364.0.55.0012014-15?OpenDocument. Accessed 15 May 2017.

  7. Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among us adults, 1999-2010. JAMA. 2012;307:491–7.

    Article  PubMed  Google Scholar 

  8. Australian Government, Department of Health. The Australian Immunisation Handbook, 10th Edition. http://www.immunise.health.gov.au/internet/immunise/publishing.nsf/Content/7B28E87511E08905CA257D4D001DB1F8/$File/Aus-Imm-Handbook.pdf. Accessed 15 May 2017.

  9. Martin V, Castilla J, Godoy P, Delgado-Rodriguez M, Soldevila N, Fernandez-Villa T, et al. High body mass index as a risk factor for hospitalization due to influenza: a case-control study. Arch Bronconeumol. 2016;52:299–307.

    Article  PubMed  Google Scholar 

  10. Centers for Disease C, Prevention. Intensive-care patients with severe novel influenza A (H1N1) virus infection - Michigan, June 2009. MMWR Morb Mortal Wkly Rep. 2009;58:749–52.

    Google Scholar 

  11. Sun Y, Wang Q, Yang G, Lin C, Zhang Y, Yang P. Weight and prognosis for influenza A(H1N1)pdm09 infection during the pandemic period between 2009 and 2011: a systematic review of observational studies with meta-analysis. Infect Dis. 2016;48:813–22.

    Article  Google Scholar 

  12. Fezeu L, Julia C, Henegar A, Bitu J, Hu FB, Grobbee DE, et al. Obesity is associated with higher risk of intensive care unit admission and death in influenza A (H1N1) patients: a systematic review and meta-analysis. Obes Rev. 2011;12:653–9.

    Article  CAS  PubMed  Google Scholar 

  13. Louie JK, Acosta M, Samuel MC, Schechter R, Vugia DJ, Harriman K, et al. A novel risk factor for a novel virus: obesity and 2009 pandemic influenza A (H1N1). Clin Infect Dis. 2011;52:301–12.

    Article  PubMed  Google Scholar 

  14. Mertz D, Kim TH, Johnstone J, Lam PP, Science M, Kuster SP, et al. Populations at risk for severe or complicated influenza illness: systematic review and meta-analysis. BMJ. 2013;347:f5061.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Tempia S, Walaza S, Moyes J, Cohen AL, von Mollendorf C, Treurnicht FK, et al. Risk factors for influenza-associated severe acute respiratory illness hospitalization in South Africa, 2012-2015. Open Forum Infect Dis. 2017;4:ofw262.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Charland KM, Buckeridge DL, Hoen AG, Berry JG, Elixhauser A, Melton F, et al. Relationship between community prevalence of obesity and associated behavioral factors and community rates of influenza-related hospitalizations in the United States. Influenza Other Respir Virus. 2013;7:718–28.

    Article  Google Scholar 

  17. Kwong JC, Campitelli MA, Rosella LC. Obesity and respiratory hospitalizations during influenza seasons in Ontario, Canada: a cohort study. Clin Infect Dis. 2011;53:413–21.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Dimitrijevic D, Ilic D, Rakic Adrovic S, Suljagic V, Pelemis M, Stevanovic G, et al. Predictors of hospitalization and admission to intensive care units of influenza patients in serbia through four influenza seasons from 2010/2011 to 2013/2014. Jpn J Infect Dis. 2017;70:275–83.

    Article  PubMed  Google Scholar 

  19. Zhou Y, Cowling BJ, Wu P, Chan WM, Lee SY, Lau EH, et al. Adiposity and influenza-associated respiratory mortality: a cohort study. Clin Infect Dis. 2015;60:e49–57.

    Article  PubMed  Google Scholar 

  20. Braun ES, Crawford FW, Desai MM, Meek J, Kirley PD, Miller L, et al. Obesity not associated with severity among hospitalized adults with seasonal influenza virus infection. Infection. 2015;43:569–75.

    Article  PubMed  Google Scholar 

  21. Blumentals WA, Nevitt A, Peng MM, Toovey S. Body mass index and the incidence of influenza-associated pneumonia in a UK primary care cohort. Influenza Other Respir Virus. 2012;6:28–36.

    Article  Google Scholar 

  22. Cocoros NM, Lash TL, DeMaria A Jr, Klompas M. Obesity as a risk factor for severe influenza-like illness. Influenza Other Respir Virus. 2014;8:25–32.

    Article  Google Scholar 

  23. Coleman LA, Waring SC, Irving SA, Vandermause M, Shay DK, Belongia EA. Evaluation of obesity as an independent risk factor for medically attended laboratory-confirmed influenza. Influenza Other Respir Virus. 2013;7:160–7.

    Article  Google Scholar 

  24. Neidich SD, Green WD, Rebeles J, Karlsson EA, Schultz-Cherry S, Noah TL, et al. Increased risk of influenza among vaccinated adults who are obese. Int J Obes. 2017;41:1324–30.

    Article  CAS  Google Scholar 

  25. 45 and Up Study Collaborators, Banks E, Redman S, Jorm L, Armstrong B, Bauman A, et al. Cohort profile: the 45 up study. Int J Epidemiol. 2008;37:941–7.

  26. Centre for Health Record Linkage (CHeReL): Quality assurance. http://www.cherel.org.au/media/24160/qa_report_2012.pdf. Accessed 14 May 2017.

  27. Center for Health Record Linkage. Data dictionaries- Notifiable Conditions Information Management System (NCIMS). http://www.cherel.org.au/media/29612/ncims_data_dictionary_feb_2014-a.docx. Accessed 17 May 2017.

  28. Center for Health Record Linkage. Data dictionaries- NSW Admitted Patient Data Collection (APDC). http://www.cherel.org.au/data-dictionaries#section1. Accessed 17 May 2017.

  29. World Health Organization. Body Mass Index—BMI. 2017. http://www.euro.who.int/en/health-topics/disease-prevention/nutrition/a-healthy-lifestyle/body-mass-index-bmi. Accessed 18 May 2017.

  30. Australian Institute of Health and Welfare. Rural, Regional and Remote Health: A Guide to Remoteness Classifications. Rural Health Series No. 4. AIHW Cat. No. PHE 53. AIHW, Canberra. 2004. http://www.aihw.gov.au/WorkArea/DownloadAsset.aspx?id=6442459567. Accessed 7 Aug 2017.

  31. Green WD, Beck MA. Obesity impairs the adaptive immune response to influenza virus. Ann Am Thorac Soc. 2017;14:S406–S409.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Paich HA, Sheridan PA, Handy J, Karlsson EA, Schultz-Cherry S, Hudgens MG, et al. Overweight and obese adult humans have a defective cellular immune response to pandemic H1N1 influenza A virus. Obesity. 2013;21:2377–86.

    Article  CAS  PubMed  Google Scholar 

  33. Karlsson EA, Sheridan PA, Beck MA. Diet-induced obesity in mice reduces the maintenance of influenza-specific CD8+ memory T cells. J Nutr. 2010;140:1691–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Smith AG, Sheridan PA, Harp JB, Beck MA. Diet-induced obese mice have increased mortality and altered immune responses when infected with influenza virus. J Nutr. 2007;137:1236–43.

    Article  CAS  PubMed  Google Scholar 

  35. Painter SD, Ovsyannikova IG, Poland GA. The weight of obesity on the human immune response to vaccination. Vaccine. 2015;33:4422–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Peiris JS, Hui KP, Yen HL. Host response to influenza virus: protection versus immunopathology. Curr Opin Immunol. 2010;22:475–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Morgan OW, Bramley A, Fowlkes A, Freedman DS, Taylor TH, Gargiullo P, et al. Morbid obesity as a risk factor for hospitalization and death due to 2009 pandemic influenza A(H1N1) disease. PLoS ONE. 2010;5:e9694.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Van Kerkhove MD, Vandemaele KA, Shinde V, Jaramillo-Gutierrez G, Koukounari A, Donnelly CA, et al. Risk factors for severe outcomes following 2009 influenza A (H1N1) infection: a global pooled analysis. PLoS Med. 2011;8:e1001053.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Campitelli MA, Rosella LC, Kwong JC. The association between obesity and outpatient visits for acute respiratory infections in Ontario, Canada. Int J Obes. 2014;38:113–9.

    Article  CAS  Google Scholar 

  40. Phung DT, Wang Z, Rutherford S, Huang C, Chu C. Body mass index and risk of pneumonia: a systematic review and meta-analysis. Obes Rev. 2013;14:839–57.

    Article  CAS  PubMed  Google Scholar 

  41. Flahault A, de Lamballerie X, Hanslik T. Symptomatic infections less frequent with H1N1pdm than with seasonal strains: Antoine Flahault, Xavier de Lamballerie, Camille Pelat, Nicolas Salez, Thomas Hanslik. PLoS Curr. 2009;1:RRN1140.

    PubMed  PubMed Central  Google Scholar 

  42. Leung NH, Xu C, Ip DK, Cowling BJ. Review article: the fraction of influenza virus infections that are asymptomatic: a systematic review and meta-analysis. Epidemiology. 2015;26:862–72.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Dyda A, MacIntyre CR, McIntyre P, Newall AT, Banks E, Kaldor J, et al. Factors associated with influenza vaccination in middle and older aged Australian adults according to eligibility for the national vaccination program. Vaccine. 2015;33:3299–305.

    Article  PubMed  Google Scholar 

  44. Ng SP, Korda R, Clements M, Latz I, Bauman A, Bambrick H, et al. Validity of self-reported height and weight and derived body mass index in middle-aged and elderly individuals in Australia. Aust N Z J Public Health. 2011;35:557–63.

    Article  PubMed  Google Scholar 

  45. Prospective Studies Collaboration. Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies. Lancet. 2009;373:1083–96.

    Article  PubMed Central  Google Scholar 

  46. World Health Organization, 2017. Influenza, FluNet. http://apps.who.int/flumart/Default?ReportNo=12. Accessed 24 Jul 2017.

  47. Lau D, Eurich DT, Majumdar SR, Katz A, Johnson JA. Working-age adults with diabetes experience greater susceptibility to seasonal influenza: a population-based cohort study. Diabetologia. 2014;57:690–8.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This research was completed using data collected through the 45 and Up Study (www.saxinstitute.org.au). The 45 and Up Study is managed by the Sax Institute in collaboration with major partner Cancer Council NSW; and partners: the National Heart Foundation of Australia (NSW Division); NSW Ministry of Health; NSW Government Family & Community Services—Ageing, Carers and the Disability Council NSW; and the Australian Red Cross Blood Service. We thank the many thousands of people participating in the 45 and Up Study.

Funding

This work was supported by National Health and Medical Research Council (NHMRC) grant (Grant number: 1048180). EB, AN, and BL are supported by NHMRC Fellowships.

Author information

Authors and Affiliations

  1. School of Public Health and Community Medicine, University of New South Wales (UNSW), Sydney, NSW, Australia

    S. Karki, D. J. Muscatello, C. R. MacIntyre & B. Liu

  2. National Centre for Epidemiology and Population Health, Australian National University, Canberra, ACT, Australia

    E. Banks

  3. The Sax Institute, Sydney, NSW, Australia

    E. Banks

  4. College of Health Solutions, Arizona State University, Tempe, AZ, USA

    C. R. MacIntyre

  5. National Centre for Immunization Research and Surveillance, Kids Research Institute, Children’s Hospital at Westmead, Sydney, NSW, Australia

    P. McIntyre

Authors
  1. S. Karki
    View author publications

    Search author on:PubMed Google Scholar

  2. D. J. Muscatello
    View author publications

    Search author on:PubMed Google Scholar

  3. E. Banks
    View author publications

    Search author on:PubMed Google Scholar

  4. C. R. MacIntyre
    View author publications

    Search author on:PubMed Google Scholar

  5. P. McIntyre
    View author publications

    Search author on:PubMed Google Scholar

  6. B. Liu
    View author publications

    Search author on:PubMed Google Scholar

Corresponding authors

Correspondence to S. Karki or B. Liu.

Ethics declarations

Conflict of interest

PM sits on the Australian Government expert advisory committee for immunization. EB chairs the Australian Government Advisory Committee on the Safety of Vaccines. CRM had received funding and/or laboratory testing support for investigator driven research from CSL Biotherapies, Pfizer and Merck but not related to this research. She has participated in advisory boards for Pfizer, Merck and GSK. All other authors declare no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karki, S., Muscatello, D.J., Banks, E. et al. Association between body mass index and laboratory-confirmed influenza in middle aged and older adults: a prospective cohort study. Int J Obes 42, 1480–1488 (2018). https://doi.org/10.1038/s41366-018-0029-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Version of record:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41366-018-0029-x

This article is cited by

Search

Advanced search

Quick links