Author:
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Nasopharyngeal Viral and Bacterial Co-Detection among Children from Low- and Middle-Income Countries with and without Pneumonia
Cédric Dananché
Cédric Dananché
CIRI, Centre International de Recherche en Infectiologie (team Public Health, Epidemiology and Evolutionnary Ecology of Infectious Diseases (PHE3ID)), Univ Lyon, Inserm, U1111, Université Claude Bernard Lyon 1, CNRS, UMR5308, ENS de Lyon, F-69007, Lyon, France;
Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France;
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Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France;
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Gláucia Paranhos-Baccalà
Gláucia Paranhos-Baccalà
Mérieux Foundation, Lyon, France;
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Mélina Messaoudi
Mélina Messaoudi
Mérieux Foundation, Lyon, France;
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Mariam Sylla
Mariam Sylla
Gabriel Touré Hospital, Bamako, Mali;
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Shally Awasthi
Shally Awasthi
Chatrapati Shahu Ji Maharaj Medical University, Lucknow, India;
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Ashish Bavdekar
Ashish Bavdekar
KEM Hospital Research Center, Pune, India;
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Jean-William Pape
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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Vanessa Rouzier
Vanessa Rouzier
Centres GHESKIO (Groupe Haïtien d'Etude du Sarcome de Kaposi et des Infections Opportunistes), Port-au-Prince, Haiti;
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Jianwei Wang
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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Sonali Sanghavi
Sonali Sanghavi
KEM Hospital Research Center, Pune, India;
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Souleymane Diallo
Souleymane Diallo
Centre d’Infectiologie Charles Mérieux, Bamako, Mali;
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Monidarin Chou
Monidarin Chou
Faculty of Pharmacy, University of Health Sciences, Phnom Penh, Cambodia;
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Tekchheng Eap
Tekchheng Eap
Department of Pneumology, National Pediatric Hospital, Phnom Penh, Cambodia;
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Mala Rakoto-Andrianarivelo
Mala Rakoto-Andrianarivelo
Fondation Mérieux, Centre d'Infectiologie Charles Mérieux, Antananarivo, Madagascar;
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Hubert Endtz
Hubert Endtz
Mérieux Foundation, Lyon, France;
Department of Clinical Microbiology & Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands;
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Department of Clinical Microbiology & Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands;
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Lili Ren
Lili Ren
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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Budragchaagiin Dash-Yandag
Budragchaagiin Dash-Yandag
Bayanzurkh District General Hospital, Ulaanbaatar, Mongolia;
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Rosa Guillen
Rosa Guillen
Instituto de Investigaciones en Ciencias de la Salud, National University of Asunción, Asunción, Paraguay;
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Pagbajabyn Nymadawa
Pagbajabyn Nymadawa
Mongolian Academy of Medical Sciences, Ulaanbaatar, Mongolia;
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Graciela Russomando
Graciela Russomando
Instituto de Investigaciones en Ciencias de la Salud, National University of Asunción, Asunción, Paraguay;
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Florence Komurian-Pradel
Florence Komurian-Pradel
Mérieux Foundation, Lyon, France;
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Philippe Vanhems
Philippe Vanhems
CIRI, Centre International de Recherche en Infectiologie (team Public Health, Epidemiology and Evolutionnary Ecology of Infectious Diseases (PHE3ID)), Univ Lyon, Inserm, U1111, Université Claude Bernard Lyon 1, CNRS, UMR5308, ENS de Lyon, F-69007, Lyon, France;
Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France;
Inserm, F-CRIN, Réseau Innovative Clinical Research in Vaccinology (I-REIVAC), Lyon center, France
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Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France;
Inserm, F-CRIN, Réseau Innovative Clinical Research in Vaccinology (I-REIVAC), Lyon center, France
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Valentina Sánchez Picot
Valentina Sánchez Picot
Mérieux Foundation, Lyon, France;
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for the Global Approach to Biological Research, Infectious Diseases and Epidemics in Low-Income Countries (GABRIEL) Network
for the Global Approach to Biological Research, Infectious Diseases and Epidemics in Low-Income Countries (GABRIEL) Network
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ABSTRACT.
The role of microbial coinfection in the pathogenesis of pneumonia in children is not well known. The aim of this work was to describe the prevalence of microorganism co-detection in nasopharyngeal samples (NPS) of pneumonia cases and control subjects and to study the potential association between nasopharyngeal microorganism co-detection and pneumonia. A case-control study was carried out from 2010 to 2014 in nine study sites located in low- or middle-income countries. The data from 888 children under 5 years of age with pneumonia (cases) and 870 children under 5 without pneumonia (controls) were analyzed. Nasopharyngeal samples were collected; reverse transcription polymerase chain reaction (RT-PCR) enabled the detection of five bacteria and 19 viruses. Multiple, mixed-effects logistic regression modeling was undertaken to evaluate the association between microorganism co-detection and pneumonia. A single Streptococcus pneumoniae colonization was observed in 15.2% of the controls and 10.1% of the cases (P = 0.001), whereas S. pneumoniae and a single virus co-detection was observed in 33.3% of the cases and in 14.6% of the controls (P < 0.001). Co-detections with rhinovirus, respiratory syncytial virus, parainfluenza virus, human metapneumovirus, and influenza virus were more frequent in the cases compared with the controls (P < 0.001) and were significantly associated with pneumonia in multiple regression analysis. The proportion of single virus detection without bacterial co-detection was not different between cases and controls (13.6% versus 11.3%, P = 0.13). This study suggests that coinfection of S. pneumoniae and certain viruses may play a role in the pathophysiology of pneumonia in children.
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Author Notes
Financial support: This study was supported by the GABRIEL Network of Fondation Mérieux.
Disclaimer: A. B. has received grants from Fondation Mérieux.
Authors’ addresses: Cédric Dananché, Team Public Health, Epidemiology and Evolutionary Ecology of Infectious Diseases (PHE3ID), Centre International de Recherche en Infectiologie, INSERM U1111, CNRS UMR5308, ENS de Lyon, Université Claude Bernard Lyon 1, France, and Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France, E-mail: cedric.dananche@chu-lyon.fr. Gláucia Paranhos-Baccalà, Mélina Messaoudi, and Valentina Sánchez Picot, Mérieux Foundation, Lyon, France, E-mails: glaucia.baccala@biomerieux.com, melina.messaoudi@fondation-merieux.org, and valentina.picot@fondation-merieux.org. Mariam Sylla, Gabriel Touré Hospital, Bamako, Mali, E-mail: dr_mame@yahoo.fr. Shally Awasthi, Chatrapati Shahu Ji Maharaj Medical University, Lucknow, India, E-mail: shally07@gmail.com. Ashish Bavdekar and Sonali Sanghavi, KEM Hospital Research Center, Pune, India, E-mails: bavdekar@vsnl.com and sanghsk@yahoo.com. Jean-William Pape and Vanessa Rouzier, Centres GHESKIO (Groupe Haïtien d’Etude du Sarcome de Kaposi et des Infections Opportunistes), Port-au-Prince, Haiti, E-mails: jwpape@gheskio.org and vrouzier@gheskio.org. Jianwei Wang and Lili Ren, 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-mails: wangjw28@163.com and skimmilk@163.com. Souleymane Diallo, Centre d’Infectiologie Charles Mérieux, Bamako, Mali, E-mail: souleymane.diallo@cicm-mali.org. Monidarin Chou, Faculty of Pharmacy, University of Health Sciences, Phnom Penh, Cambodia, E-mail: cmonidarin@uhs.edu.kh. Tekchheng Eap, Department of Pneumology, National Pediatric Hospital, Phnom Penh, Cambodia, E-mail: techheng@yahoo.com. Mala Rakoto-Andrianarivelo, Fondation Mérieux, Centre d’Infectiologie Charles Mérieux, Antananarivo, Madagascar, E-mail: mala@cicm-madagascar.com. Hubert Endtz, Mérieux Foundation, Lyon, France, and Department of Clinical Microbiology & Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands, E-mail: hubert.endtz@fondation-merieux.org. Budragchaagiin Dash-Yandag, Bayanzurkh District General Hospital, Ulaanbaatar, Mongolia, E-mail: dashyandag@mobinet.mn. Rosa Guillen and Graciela Russomando, Instituto de Investigaciones en Ciencias de la Salud, National University of Asunción, Asunciòn, Paraguay, E-mails: rmguillen@gmail.com and grusso@rieder.net.py. Pagbajabyn Nymadawa, Mongolian Academy of Medical Sciences, Ulaanbaatar, Mongolia, E-mail: nymadawa@gyals.mn. Florence Komurian-Pradel, Mérieux Foundation, Lyon, France, E-mail: florence.pradel@fondation-merieux.org. Philippe Vanhems, Team Public Health, Epidemiology and Evolutionnary Ecology of Infectious Diseases (PHE3ID), Centre International de Recherche en Infectiologie, Université Claude Bernard Lyon 1, France, Infection Control and Epidemiology Department, Hospices Civils de Lyon, Lyon, France, and INSERM, F-CRIN, Réseau Innovative Clinical Research in Vaccinology (I-REIVAC), Lyon center, France, E-mail: philippe.vanhems@chu-lyon.fr.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
GBD 2019 under-5 Mortality Collaborators , 2021. Global, regional, and national progress towards Sustainable Development Goal 3.2 for neonatal and child health: all-cause and cause-specific mortality findings from the Global Burden of Disease Study 2019. Lancet 398: 870–905.
-
2.
Pneumonia Etiology Research for Child Health (PERCH) Study Group , 2019. Causes of severe pneumonia requiring hospital admission in children without HIV infection from Africa and Asia: the PERCH multi-country case-control study. Lancet 394: 757–779.
-
3.
Principi N , Esposito S , 2011. Management of severe community-acquired pneumonia of children in developing and developed countries. Thorax 66: 815–822.
-
4.
Ruuskanen O , Lahti E , Jennings LC , Murdoch DR , 2011. Viral pneumonia. Lancet 377: 1264–1275.
-
5.
Bosch AATM , Biesbroek G , Trzcinski K , Sanders EAM , Bogaert D , 2013. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog 9: e1003057.
-
6.
King PT , Buttery J , 2018. Emerging role of viral and bacterial co-infection in early childhood. Respirology 23: 128–129.
-
7.
Michelow IC , Olsen K , Lozano J , Rollins NK , Duffy LB , Ziegler T , Kauppila J , Leinonen M , McCracken GH Jr , 2004. Epidemiology and clinical characteristics of community-acquired pneumonia in hospitalized children. Pediatrics 113: 701–707.
-
8.
Kwambana BA , Barer MR , Bottomley C , Adegbola RA , Antonio M , 2011. Early acquisition and high nasopharyngeal co-colonisation by Streptococcus pneumoniae and three respiratory pathogens amongst Gambian new-borns and infants. BMC Infect Dis 11: 175.
-
9.
Bakaletz LO , 2017. Viral-bacterial co-infections in the respiratory tract. Curr Opin Microbiol 35: 30–35.
-
10.
McCullers JA , 2014. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol 12: 252–262.
-
11.
Wolter N et al.2014. High nasopharyngeal pneumococcal density, increased by viral coinfection, is associated with invasive pneumococcal pneumonia. J Infect Dis 210: 1649–1657.
-
12.
Vissing NH , Chawes BLK , Bisgaard H , 2013. Increased risk of pneumonia and bronchiolitis after bacterial colonization of the airways as neonates. Am J Respir Crit Care Med 188: 1246–1252.
-
13.
Madhi SA , Klugman KP , Vaccine Trialist Group , 2004. A role for Streptococcus pneumoniae in virus-associated pneumonia. Nat Med 10: 811–813.
-
14.
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: 40–43.
-
15.
Picot VS et al.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.
-
16.
Bénet T et al.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: 604–612.
-
17.
World Health Organization , 2013. Pocket Book of Hospital Care for Children: Guidelines for the Management of Common Illnesses with Limited Resources, 2nd edition. Geneva, Switzerland: WHO. Available at: https://apps.who.int/iris/bitstream/handle/10665/81170/9789241548373_eng.pdf?sequence=1&isAllowed=y. Accessed August 31, 2021.
-
18.
Anderson TP , Werno AM , Barratt K , Mahagamasekera P , Murdoch DR , Jennings LC , 2013. Comparison of four multiplex PCR assays for the detection of viral pathogens in respiratory specimens. J Virol Methods 191: 118–121.
-
19.
Dananché C et al.2020. Serotypes of Streptococcus pneumoniae in children aged <5 years hospitalized with or without pneumonia in developing and emerging countries: a descriptive, multicenter study. Clin Infect Dis 70: 875–883.
-
20.
Ege M , von Mutius E , 2013. Microbial airway colonization: a cause of asthma and pneumonia? Am J Respir Crit Care Med 188: 1188–1189.
-
21.
Haq IJ , Battersby AC , Eastham K , McKean M , 2017. Community acquired pneumonia in children. BMJ 356: j686.
-
22.
Almand EA , Moore MD , Jaykus LA , 2017. Virus-bacteria interactions: an emerging topic in human infection. Viruses 9: 58.
-
23.
Cilla G , Oñate E , Perez-Yarza EG , Montes M , Vicente D , Perez-Trallero E , 2008. Viruses in community-acquired pneumonia in children aged less than 3 years old: high rate of viral coinfection. J Med Virol 80: 1843–1849.
-
24.
Palacios G et al.2009. Streptococcus pneumoniae coinfection is correlated with the severity of H1N1 pandemic influenza. PLOS ONE 4: e8540.
-
25.
Centers for Disease Control and Prevention , 2009. Bacterial coinfections in lung tissue specimens from fatal cases of 2009 pandemic influenza A (H1N1)-United States, May–August 2009. MMWR Morb Mortal Wkly Rep 58: 1071–1074.
-
26.
Sender V , Hentrich K , Henriques-Normark B , 2021. Virus-induced changes of the respiratory tract environment promote secondary infections with Streptococcus pneumoniae. Front Cell Infect Microbiol 11: 643326.
-
27.
Brealey JC , Chappell KJ , Galbraith S , Fantino E , Gaydon J , Tozer S , Young PR , Holt PG , Sly PD , 2018. Streptococcus pneumoniae colonization of the nasopharynx is associated with increased severity during respiratory syncytial virus infection in young children. Respirology 23: 220–227.
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