Burden of Influenza in Less Than 5-Year-Old Children Admitted to Hospital with Pneumonia in Developing and Emerging Countries: A Descriptive, Multicenter Study

Cédric Dananché Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France;
Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France;

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Valentina Sánchez Picot Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France;

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Thomas Bénet Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France;
Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France;

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Mélina Messaoudi Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France;

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Monidarin Chou Faculty of Pharmacy, University of Health Sciences, Phnom Penh, Cambodia;

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Jianwei Wang MOH Key Laboratory of the Systems Biology of Pathogens and Dr. Christophe Mérieux Laboratory, Fondation Mérieux, Institute of Pathogen Biology, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China;

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Jean-William Pape Centres GHESKIO (Groupe Haïtien d’Etude du Sarcome de Kaposi et des Infections Opportunistes), Port-au-Prince, Haiti;

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Shally Awasthi Chatrapati Shahu Ji Maharaj Medical University, Lucknow, India;

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Ashish Bavdekar KEM Hospital Research Center, Pune, India;

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Mala Rakoto-Andrianarivelo Fondation Mérieux, Centre d’Infectiologie Charles Mérieux, Antananarivo, Madagascar;

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Mariam Sylla Gabriel Touré Hospital, Bamako, Mali;

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Pagbajabyn Nymadawa Mongolian Academy of Medical Sciences, Ulaanbaatar, Mongolia;

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Graciela Russomando Research Institute of Health, Asunción, Paraguay;

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Florence Komurian-Pradel Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France;

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Hubert Endtz Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France;
Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands

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Gláucia Paranhos-Baccalà Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France;

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Philippe Vanhems Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France;
Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France;

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for the GABRIEL Network Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France;
Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France;
Faculty of Pharmacy, University of Health Sciences, Phnom Penh, Cambodia;
MOH Key Laboratory of the Systems Biology of Pathogens and Dr. Christophe Mérieux Laboratory, Fondation Mérieux, Institute of Pathogen Biology, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China;
Centres GHESKIO (Groupe Haïtien d’Etude du Sarcome de Kaposi et des Infections Opportunistes), Port-au-Prince, Haiti;
Chatrapati Shahu Ji Maharaj Medical University, Lucknow, India;
KEM Hospital Research Center, Pune, India;
Fondation Mérieux, Centre d’Infectiologie Charles Mérieux, Antananarivo, Madagascar;
Gabriel Touré Hospital, Bamako, Mali;
Mongolian Academy of Medical Sciences, Ulaanbaatar, Mongolia;
Research Institute of Health, Asunción, Paraguay;
Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands

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This descriptive 4-year study reports the proportion of detection of influenza viruses in less than 5-year-old children hospitalized for pneumonia in eight developing and emerging countries and describes clinical and microbiological characteristics of influenza-related pneumonia cases. Hospitalized children presenting radiologically confirmed pneumonia aged 2–60 months were prospectively enrolled in this observational standardized study. Mean proportion of isolated influenza virus was 9.7% (95% confidence interval: 7.9–11.8%) among 888 pneumonia children analyzed, with moderate heterogeneity between countries—ranging from 6.2% in Cambodia to 18.8% in Haiti. The clinical characteristics of children with influenza-related pneumonia were not substantially different from those of other pneumonia cases. Influenza A H1N1-related pneumonia cases appeared as more severe than pneumonia cases related to other strains of influenza. Streptococcus pneumoniae was detected more often in blood samples from influenza-related cases than in those without detected influenza viruses (19.7% versus 9.5%, P = 0.018). Influenza-related pneumonia is frequent among children less than 5 years old with pneumonia, living in developing and emerging countries. Influenza might be a frequent etiologic agent responsible for pneumonia or a predisposing status factor for pneumococcal-related pneumonia in this population.

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Author Notes

Address correspondence to Cédric Dananché, Laboratoire des Pathogènes Émergents, Fondation Mérieux, Centre International de Recherche en Infectiologie, Inserm U1111, CNRS UMR5308, ENS de Lyon, Université Claude Bernard Lyon 1, 7-11, rue Guillaume Paradin, F-69372 Lyon Cedex 08, France. E-mail: cedric.dananche@chu-lyon.fr

Ethics statement: The study protocol, informed consent statement, clinical research form, amendments, and all other study documents were submitted to and approved by the Institutional Research Ethics Committee of each site.

Authors’ addresses: Cédric Dananché, Thomas Bénet, and Philippe Vanhems, Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France, and Service Hygiène, Epidémiologie et Prévention, Centre Hospitalier Universitaire de Lyon, Lyon, France, E-mails: cedric.dananche@chu-lyon.fr, thomas.benet@chu-lyon.fr, and philippe.vanhems@chu-lyon.fr. Valentina Sánchez Picot, Mélina Messaoudi, and Florence Komurian-Pradel, Emerging Pathogens Laboratory, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Lyon, France, E-mails: valentina.picot@fondation-merieux.org, melina.messaoudi@fondation-merieux.org, and florence.pradel@fondation-merieux.org. Monidarin Chou, Faculty of Pharmacy, University of Health Sciences, Phnom Penh, Cambodia, E-mail: cmonidarin@uhs.edu.kh. Jianwei Wang, MOH Key Laboratory of the Systems Biology of Pathogens and Dr. Christophe Mérieux Laboratory, Fondation Mérieux, Institute of Pathogen Biology, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China, E-mail: wangjw28@163.com. Jean-William Pape, Groupe Haïtien d’Etude du Sarcome de Kaposi et des Infections Opportunistes (GHESKIO), Port-au-Prince, Haiti, E-mail: jwpape@gheskio.org. Shally Awasthi, Chatrapati Shahuji Maharaj University, Lucknow, India, E-mail: shally07@gmail.com. Ashish Bavdekar, KEM Hospital, Pune, India, E-mail: bavdekar@vsnl.com. Mala Rakoto-Andrianarivelo, Centre d’Infectiologie Charles Mérieux, Antananarivo, Madagascar, E-mail: mala@cicm-madagascar.com. Mariam Sylla, Gabriel Touré Hospital, Bamako, Mali, E-mail: dr_mame@yahoo.fr. Pagbajabyn Nymadawa, Mongolian Academy of Medical Sciences, Ulaanbaatar, Mongolia, E-mail: nymadawa@gyals.mn. Graciela Russomando, Molecular Biology Department, Instituto de Investigaciones en Ciencias de la Salud, Universidad Nacional de Asunción, Asunción, Paraguay, E-mail: grusso@rieder.net.py. Hubert Endtz, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Emerging Pathogens Laboratory, Lyon, France, and Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands, E-mail: hubert.endtz@fondation-merieux.org. Gláucia Paranhos-Baccalà, Fondation Mérieux, Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, UCBL1, Emerging Pathogens Laboratory, Lyon, France, E-mail: glaucia.baccala@fondation-merieux.org.

  • 1.

    Nair H et al. 2011. Global burden of respiratory infections due to seasonal influenza in young children: a systematic review and meta-analysis. Lancet 378: 19171930.

    • Search Google Scholar
    • Export Citation
  • 2.

    Mina MJ, Klugman KP, 2014. The role of influenza in the severity and transmission of respiratory bacterial disease. Lancet Respir Med 2: 750763.

    • Search Google Scholar
    • Export Citation
  • 3.

    Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, O’Brien KL, Campbell H, Black RE, 2013. Global burden of childhood pneumonia and diarrhoea. Lancet 381: 14051416.

    • Search Google Scholar
    • Export Citation
  • 4.

    Rello J, Pop-Vicas A, 2009. Clinical review: primary influenza viral pneumonia. Crit Care 13: 235.

  • 5.

    Fischer WA 2nd, Gong M, Bhagwanjee S, Sevransky J, 2014. Global burden of influenza as a cause of cardiopulmonary morbidity and mortality. Glob Heart 9: 325336.

    • Search Google Scholar
    • Export Citation
  • 6.

    Komurian-Pradel F et al. 2013. Enhancing research capacities in infectious diseases: the GABRIEL network, a joint approach to major local health issues in developing countries. Clin Epidemiol Glob Health 1: 4043.

    • Search Google Scholar
    • Export Citation
  • 7.

    Picot VS et al. Pneumonia GABRIEL Network, 2014. Multicenter case-control study protocol of pneumonia etiology in children: global approach to biological research, infectious diseases and epidemics in low-income countries (GABRIEL network). BMC Infect Dis 14: 635.

    • Search Google Scholar
    • Export Citation
  • 8.

    Bénet T et al. for the GABRIEL Network, 2017. Severity of pneumonia in under 5-year-old children from developing countries: a multicenter, prospective, observational study. Am J Trop Med Hyg 97: 6876.

    • Search Google Scholar
    • Export Citation
  • 9.

    Bénet T et al. Global Approach to Biological Research, Infectious Diseases and Epidemics in Low-Income Countries (GABRIEL) Network, 2017. Microorganisms associated with pneumonia in children < 5 years of age in developing and emerging countries: the GABRIEL pneumonia multicenter, prospective, case-control study. Clin Infect Dis 65: 604612.

    • Search Google Scholar
    • Export Citation
  • 10.

    Cherian T et al. 2005. Standardized interpretation of paediatric chest radiographs for the diagnosis of pneumonia in epidemiological studies. Bull World Health Organ 83: 353359.

    • Search Google Scholar
    • Export Citation
  • 11.

    Albrich WC et al. 2014. Pneumococcal colonisation density: a new marker for disease severity in HIV-infected adults with pneumonia. BMJ Open 4: e005953.

    • Search Google Scholar
    • Export Citation
  • 12.

    Albrich WC, Madhi SA, Adrian PV, Telles JN, Paranhos-Baccalà G, Klugman KP, 2014. Genomic load from sputum samples and nasopharyngeal swabs for diagnosis of pneumococcal pneumonia in HIV-infected adults. J Clin Microbiol 52: 42244229.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ali A, Khowaja AR, Bashir MZ, Aziz F, Mustafa S, Zaidi A, 2013. Role of human metapneumovirus, influenza A virus and respiratory syncytial virus in causing WHO-defined severe pneumonia in children in a developing country. PLoS One 8: e74756.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ruuskanen O, Lahti E, Jennings LC, Murdoch DR, 2011. Viral pneumonia. Lancet 377: 12641275.

  • 15.

    Chiu SS, Tse CY, Lau YL, Peiris M, 2001. Influenza A infection is an important cause of febrile seizures. Pediatrics 108: E63.

  • 16.

    Izadnegahdar R, Cohen AL, Klugman KP, Qazi SA, 2013. Childhood pneumonia in developing countries. Lancet Respir Med 1: 574584.

  • 17.

    Gordon A, Saborío S, Videa E, López R, Kuan G, Balmaseda A, Harris E, 2010. Clinical attack rate and presentation of pandemic H1N1 influenza versus seasonal influenza A and B in a pediatric cohort in Nicaragua. Clin Infect Dis 50: 14621467.

    • Search Google Scholar
    • Export Citation
  • 18.

    Tenenbaum T, Franz A, Neuhausen N, Willems R, Brade J, Schweitzer-Krantz S, Adams O, Schroten H, Henrich B, 2012. Clinical characteristics of children with lower respiratory tract infections are dependent on the carriage of specific pathogens in the nasopharynx. Eur J Clin Microbiol Infect Dis 31: 31733182.

    • Search Google Scholar
    • Export Citation
  • 19.

    Madhi SA, Klugman KP; Vaccine Trialist Group, 2004. A role for Streptococcus pneumoniae in virus-associated pneumonia. Nat Med 10: 811813.

    • Search Google Scholar
    • Export Citation
  • 20.

    Klein EY, Monteforte B, Gupta A, Jiang W, May L, Hsieh YH, Dugas A, 2016. The frequency of influenza and bacterial coinfection: a systematic review and meta-analysis. Influenza Other Respir Viruses 10: 394403.

    • Search Google Scholar
    • Export Citation
  • 21.

    Qi L et al. 2016. Epidemiological and virological characteristics of influenza in Chongqing, China, 2011–2015. PLoS One 11: e0167866.

  • 22.

    Simmerman JM et al. 2009. Incidence, seasonality and mortality associated with influenza pneumonia in Thailand: 2005–2008. PLoS One 4: e7776.

  • 23.

    Tarnagda Z et al. 2014. Sentinel surveillance of influenza in Burkina Faso: identification of circulating strains during 2010–2012. Influenza Other Respir Viruses 8: 524529.

    • Search Google Scholar
    • Export Citation
  • 24.

    Rudan I, Boschi-Pinto C, Biloglav Z, Mulholland K, Campbell H, 2008. Epidemiology and etiology of childhood pneumonia. Bull World Health Organ 86: 408416.

    • Search Google Scholar
    • Export Citation
  • 25.

    Domínguez A et al. Cases and Controls in Pandemic Influenza Working Group Spain (CIBERESP), 2013. Benefit of conjugate pneumococcal vaccination in preventing influenza hospitalization in children: a case-control study. Pediatr Infect Dis J 32: 330334.

    • Search Google Scholar
    • Export Citation
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