Predictors of Severity of Influenza-Related Hospitalizations: Results From the Global Influenza Hospital Surveillance Network (GIHSN)

doi:10.1093/infdis/jiad303

. 2024 Apr 12;229(4):999-1009.

doi: 10.1093/infdis/jiad303.

Predictors of Severity of Influenza-Related Hospitalizations: Results From the Global Influenza Hospital Surveillance Network (GIHSN)

Lily E Cohen^{1

2}, Chelsea L Hansen^{3

4

5}, Melissa K Andrew⁶, Shelly A McNeil⁶, Philippe Vanhems⁷, Jan Kyncl^{8

9}, Javier Díez Domingo¹⁰, Tao Zhang¹¹, Ghassan Dbaibo¹², Victor Alberto Laguna-Torres¹³, Anca Draganescu¹⁴, Elsa Baumeister¹⁵, Doris Gomez¹⁶, Sonia M Raboni¹⁷, Heloisa I G Giamberardino¹⁷, Marta C Nunes^{18

19}, Elena Burtseva²⁰, Anna Sominina²¹, Snežana Medić^{22

23}, Daouda Coulibaly²⁴, Afif Ben Salah^{25

26}, Nancy A Otieno²⁷, Parvaiz A Koul²⁸, Serhat Unal^{29

30}, Mine Durusu Tanriover^{30

31}, Marie Mazur¹, Joseph Bresee¹, Cecile Viboud³, Sandra S Chaves³²

Affiliations

¹ Ready2Respond p/o The Task Force for Global Health, Decatur, Georgia, USA.
² Department of Medical Education, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
³ Division of International Epidemiology and Population Studies, Fogarty International Center, National Institutes of Health, Bethesda, Maryland, USA.
⁴ Brotman Baty Institute, University of Washington, Seattle, Washington, USA.
⁵ PandemiX Center, Department of Science & Environment, Roskilde University, Denmark.
⁶ Canadian Center for Vaccinology, IWK Health Centre and Nova Scotia Health, Dalhousie University, Halifax, Nova Scotia, Canada.
⁷ Hôpital Edouard Herriot, Lyon, France.
⁸ Department of Infectious Diseases Epidemiology, National Institute of Public Health, Prague, Czech Republic.
⁹ Department of Epidemiology and Biostatistics, Third Faculty of Medicine, Charles University, Prague, Czech Republic.
¹⁰ Fundación Para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO-Public Health), Valencia, Spain.
¹¹ School of Public Health, Fudan University, Shanghai, China.
¹² Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon.
¹³ Clínica Internacional, Instituto de Medicina Tropical Universidad Nacional Mayor de San Marcos, Lima, Peru.
¹⁴ National Institute for Infectious Diseases "Prof Dr Matei Bals", Bucharest, Romania.
¹⁵ Respiratory Virus Laboratory, Virology Department, INEI-ANLIS, Buenos Aires, Argentina.
¹⁶ Grupo de Investigación UNIMOL, Facultad de Medicina, Universidad de Cartagena, Cartagena de Indias, Colombia.
¹⁷ Virology Laboratory, Infectious Diseases Division, Universidade Federal do Paraná, Hospital Pequeno Principe, Curitiba, Paraná, Brazil.
¹⁸ South African Medical Research Council, Vaccines and Infectious Diseases Analytics Research Unit, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
¹⁹ Department of Science and Technology/National Research Foundation, South African Research Chair Initiative in Vaccine Preventable Diseases, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
²⁰ Gamaleya Federal Research Center for Epidemiology and Microbiology, Ministry of Health of Russian Federation, Moscow, Russia.
²¹ Smorodintsev Research Institute of Influenza, St Petersburg, Russia.
²² Institute for Public Health of Vojvodina, Novi Sad, Serbia.
²³ Faculty of Medicine, University of Novi Sad, Novi Sad, Serbia.
²⁴ National Institute of Public Hygiene, Abidjan, Côte d'Ivoire.
²⁵ Institut Pasteur de Tunis, Tunis, Tunisia.
²⁶ Arabian Gulf University, Manama, Bahrain.
²⁷ Kenya Medical Research Institute (KEMRI), Nairobi, Kenya.
²⁸ Sheri Kashmir Institute of Medical Sciences, Srinagar, India.
²⁹ Department of Infectious Diseases and Clinical Microbiology, Hacettepe University School of Medicine, Ankara, Turkey.
³⁰ Turkish Society of Internal Medicine, Ankara, Turkey.
³¹ Department of Internal Medicine, Hacettepe University School of Medicine, Ankara, Turkey.
³² Foundation for Influenza Epidemiology, Fondation de France, Paris, France.

PMID: 37527470
PMCID: PMC11011157
DOI: 10.1093/infdis/jiad303

Predictors of Severity of Influenza-Related Hospitalizations: Results From the Global Influenza Hospital Surveillance Network (GIHSN)

Lily E Cohen et al. J Infect Dis. 2024.

. 2024 Apr 12;229(4):999-1009.

doi: 10.1093/infdis/jiad303.

Authors

Affiliations

¹ Ready2Respond p/o The Task Force for Global Health, Decatur, Georgia, USA.
² Department of Medical Education, Icahn School of Medicine at Mount Sinai, New York, New York, USA.
³ Division of International Epidemiology and Population Studies, Fogarty International Center, National Institutes of Health, Bethesda, Maryland, USA.
⁴ Brotman Baty Institute, University of Washington, Seattle, Washington, USA.
⁵ PandemiX Center, Department of Science & Environment, Roskilde University, Denmark.
⁶ Canadian Center for Vaccinology, IWK Health Centre and Nova Scotia Health, Dalhousie University, Halifax, Nova Scotia, Canada.
⁷ Hôpital Edouard Herriot, Lyon, France.
⁸ Department of Infectious Diseases Epidemiology, National Institute of Public Health, Prague, Czech Republic.
⁹ Department of Epidemiology and Biostatistics, Third Faculty of Medicine, Charles University, Prague, Czech Republic.
¹⁰ Fundación Para el Fomento de la Investigación Sanitaria y Biomédica de la Comunitat Valenciana (FISABIO-Public Health), Valencia, Spain.
¹¹ School of Public Health, Fudan University, Shanghai, China.
¹² Center for Infectious Diseases Research, American University of Beirut, Beirut, Lebanon.
¹³ Clínica Internacional, Instituto de Medicina Tropical Universidad Nacional Mayor de San Marcos, Lima, Peru.
¹⁴ National Institute for Infectious Diseases "Prof Dr Matei Bals", Bucharest, Romania.
¹⁵ Respiratory Virus Laboratory, Virology Department, INEI-ANLIS, Buenos Aires, Argentina.
¹⁶ Grupo de Investigación UNIMOL, Facultad de Medicina, Universidad de Cartagena, Cartagena de Indias, Colombia.
¹⁷ Virology Laboratory, Infectious Diseases Division, Universidade Federal do Paraná, Hospital Pequeno Principe, Curitiba, Paraná, Brazil.
¹⁸ South African Medical Research Council, Vaccines and Infectious Diseases Analytics Research Unit, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
¹⁹ Department of Science and Technology/National Research Foundation, South African Research Chair Initiative in Vaccine Preventable Diseases, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa.
²⁰ Gamaleya Federal Research Center for Epidemiology and Microbiology, Ministry of Health of Russian Federation, Moscow, Russia.
²¹ Smorodintsev Research Institute of Influenza, St Petersburg, Russia.
²² Institute for Public Health of Vojvodina, Novi Sad, Serbia.
²³ Faculty of Medicine, University of Novi Sad, Novi Sad, Serbia.
²⁴ National Institute of Public Hygiene, Abidjan, Côte d'Ivoire.
²⁵ Institut Pasteur de Tunis, Tunis, Tunisia.
²⁶ Arabian Gulf University, Manama, Bahrain.
²⁷ Kenya Medical Research Institute (KEMRI), Nairobi, Kenya.
²⁸ Sheri Kashmir Institute of Medical Sciences, Srinagar, India.
²⁹ Department of Infectious Diseases and Clinical Microbiology, Hacettepe University School of Medicine, Ankara, Turkey.
³⁰ Turkish Society of Internal Medicine, Ankara, Turkey.
³¹ Department of Internal Medicine, Hacettepe University School of Medicine, Ankara, Turkey.
³² Foundation for Influenza Epidemiology, Fondation de France, Paris, France.

PMID: 37527470
PMCID: PMC11011157
DOI: 10.1093/infdis/jiad303

Abstract

Background: The Global Influenza Hospital Surveillance Network (GIHSN) has since 2012 provided patient-level data on severe influenza-like-illnesses from >100 participating clinical sites worldwide based on a core protocol and consistent case definitions.

Methods: We used multivariable logistic regression to assess the risk of intensive care unit admission, mechanical ventilation, and in-hospital death among hospitalized patients with influenza and explored the role of patient-level covariates and country income level.

Results: The data set included 73 121 patients hospitalized with respiratory illness in 22 countries, including 15 660 with laboratory-confirmed influenza. After adjusting for patient-level covariates we found a 7-fold increase in the risk of influenza-related intensive care unit admission in lower middle-income countries (LMICs), compared with high-income countries (P = .01). The risk of mechanical ventilation and in-hospital death also increased by 4-fold in LMICs, though these differences were not statistically significant. We also find that influenza mortality increased significantly with older age and number of comorbid conditions. Across all severity outcomes studied and after controlling for patient characteristics, infection with influenza A/H1N1pdm09 was more severe than with A/H3N2.

Conclusions: Our study provides new information on influenza severity in underresourced populations, particularly those in LMICs.

Keywords: disease severity; global health; influenza epidemiology; lower middle-income countries; surveillance.

PubMed Disclaimer

Conflict of interest statement

Potential conflicts of interest . All authors: No reported conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

Figures

**Figure 1.**
Geographic distribution of sites collaborating in the Global Influenza Hospital Surveillance Network (GIHSN), 2012–2019 influenza seasons.

**Figure 2.**
A, Median proportion (*dots*) and range (*bars*) of the percent positivity for influenza by season (A) or month (B) and country income level. Data from the Global Influenza Hospital Surveillance Network (GIHSN), 2012–2019.

**Figure 3.**
A, Distribution of influenza-positive hospitalizations by coordinating site and country income level, along with influenza type (A), number of patient comorbid conditions (B), and age group (C). Data from the Global Influenza Hospital Surveillance Network (GIHSN), 2012–2019.

**Figure 4.**
Severity outcomes among patients hospitalized with laboratory-confirmed influenza, by age group, influenza type, and country income level, Global Influenza Hospital Surveillance Network (GIHSN), 2012–2019. The y-axis depicts the percentage of patients with severe clinical outcomes.

**Figure 5.**
Risk factors for intensive care unit (ICU) admission (A), mechanical ventilation (including extracorporeal membrane oxygenation) (B), and in-hospital death (C) among patients hospitalized with laboratory-confirmed influenza. Abbreviations: CI, confidence interval; OR, odds ratio.

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References

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[1] Iuliano AD, Roguski KM, Chang HH, et al. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet 2018; 391:1285–300. - PMC - PubMed

[2] Iuliano AD, Roguski KM, Chang HH, et al. Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet 2018; 391:1285–300. - PMC - PubMed

[3] World Health Organization. Influenza (seasonal). https://www.who.int/news-room/fact-sheets/detail/influenza-(seasonal). Accessed 13 June 2022.

[4] World Health Organization. Influenza (seasonal). https://www.who.int/news-room/fact-sheets/detail/influenza-(seasonal). Accessed 13 June 2022.

[5] Neuzil KM, Wright PF, Jr ME, Griffin MR. The burden of influenza illness in children with asthma and other chronic medical conditions. J Pediatr 2000; 137:856–64. - PubMed

[6] Neuzil KM, Wright PF, Jr ME, Griffin MR. The burden of influenza illness in children with asthma and other chronic medical conditions. J Pediatr 2000; 137:856–64. - PubMed

[7] Chow EJ, Rolfes MA, O’Halloran A, et al. Respiratory and nonrespiratory diagnoses associated with influenza in hospitalized adults. JAMA Netw Open 2020; 3:e201323. - PMC - PubMed

[8] Chow EJ, Rolfes MA, O’Halloran A, et al. Respiratory and nonrespiratory diagnoses associated with influenza in hospitalized adults. JAMA Netw Open 2020; 3:e201323. - PMC - PubMed

[9] Derqui N, Nealon J, Mira-Iglesias A, Díez-Domingo J, Mahé C, Chaves SS. Predictors of influenza severity among hospitalized adults with laboratory confirmed influenza: analysis of nine influenza seasons from the Valencia region, Spain. Influenza Other Respi Viruses 2022; 16:862–72. - PMC - PubMed

[10] Derqui N, Nealon J, Mira-Iglesias A, Díez-Domingo J, Mahé C, Chaves SS. Predictors of influenza severity among hospitalized adults with laboratory confirmed influenza: analysis of nine influenza seasons from the Valencia region, Spain. Influenza Other Respi Viruses 2022; 16:862–72. - PMC - PubMed

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Predictors of Severity of Influenza-Related Hospitalizations: Results From the Global Influenza Hospital Surveillance Network (GIHSN)

Affiliations

Predictors of Severity of Influenza-Related Hospitalizations: Results From the Global Influenza Hospital Surveillance Network (GIHSN)

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