Skip to main content
Top
Published in: BMC Infectious Diseases 1/2022

Open Access 01-12-2022 | SARS-CoV-2 | Research

Bacterial colonization of the upper airways of children positive and negative for SARS-CoV-2 during the COVID-19 pandemic

Authors: Vincentia Rizke Ciptaningtyas, Rebriarina Hapsari, Endang Sri Lestari, Helmia Farida, Quirijn de Mast, Marinus Isaäk de Jonge

Published in: BMC Infectious Diseases | Issue 1/2022

Login to get access

Abstract

Background

Our understanding of the influence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection on bacterial colonization in the children’s upper nasopharyngeal tract during the coronavirus infectious disease (COVID-19) pandemic is limited. This study aimed to determine whether there were any differences in bacterial colonization between asymptomatic children with or without a positive SARS-CoV-2 quantitative reverse transcriptase-polymerase chain reaction (RT-qPCR) results in the community setting.

Methods

A cross-sectional community-based exploratory study was conducted from March to May 2021 in Semarang, Central Java Province, Indonesia. Using stored nasopharyngeal swabs collected from children under 18 years as a contact tracing program, we performed a real-time quantitative (qPCR) for the most important bacterial colonizing pathogens: Streptococcus pneumoniae, Haemophilus influenzae, Staphylococcus aureus, and Klebsiella pneumoniae.

Results

Swabs from a total of 440 children were included in this study, of which 228 (51.8%) were RT-qPCR-confirmed SARS-CoV-2 positive. In the 440 children, colonization rates were highest for H. influenzae (61.4%), followed by S. pneumoniae (17.5%), S. aureus (12.0%), and K. pneumoniae (1.8%). The co-occurrence of both S. pneumoniae and H. influenzae in the upper respiratory tract was significantly associated with a SARS-CoV-2 negative RT-qPCR. In contrast, colonization with only S. aureus was more common in SARS-CoV-2-positive children.

Conclusion

Overall, this exploratory study concludes that there is a significant difference in the bacterial nasopharyngeal colonization pattern between SARS-CoV-2 positive and negative in asymptomatic children in the community in Indonesia.
Appendix
Available only for authorised users
Literature
1.
go back to reference Hu B, Guo H, Zhou P, Shi ZL. Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol. 2021;19(3):141–54.CrossRefPubMed Hu B, Guo H, Zhou P, Shi ZL. Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol. 2021;19(3):141–54.CrossRefPubMed
2.
go back to reference Wolfel R, Corman VM, Guggemos W, Seilmaier M, Zange S, Muller MA, et al. Virological assessment of hospitalized patients with COVID-2019. Nature. 2020;581(7809):465–9.CrossRefPubMed Wolfel R, Corman VM, Guggemos W, Seilmaier M, Zange S, Muller MA, et al. Virological assessment of hospitalized patients with COVID-2019. Nature. 2020;581(7809):465–9.CrossRefPubMed
3.
go back to reference Bhuiyan MU, Stiboy E, Hassan MZ, Chan M, Islam MS, Haider N, et al. Epidemiology of COVID-19 infection in young children under five years: a systematic review and meta-analysis. Vaccine. 2021;39(4):667–77.CrossRefPubMed Bhuiyan MU, Stiboy E, Hassan MZ, Chan M, Islam MS, Haider N, et al. Epidemiology of COVID-19 infection in young children under five years: a systematic review and meta-analysis. Vaccine. 2021;39(4):667–77.CrossRefPubMed
4.
go back to reference Langford BJ, So M, Raybardhan S, Leung V, Westwood D, MacFadden DR, et al. Bacterial co-infection and secondary infection in patients with COVID-19: a living rapid review and meta-analysis. Clin Microbiol Infect. 2020;26(12):1622–9.CrossRefPubMedPubMedCentral Langford BJ, So M, Raybardhan S, Leung V, Westwood D, MacFadden DR, et al. Bacterial co-infection and secondary infection in patients with COVID-19: a living rapid review and meta-analysis. Clin Microbiol Infect. 2020;26(12):1622–9.CrossRefPubMedPubMedCentral
5.
go back to reference Rawson TM, Moore LSP, Zhu N, Ranganathan N, Skolimowska K, Gilchrist M, et al. Bacterial and fungal coinfection in individuals with coronavirus: a rapid review to support COVID-19 antimicrobial prescribing. Clin Infect Dis. 2020;71(9):2459–68.PubMed Rawson TM, Moore LSP, Zhu N, Ranganathan N, Skolimowska K, Gilchrist M, et al. Bacterial and fungal coinfection in individuals with coronavirus: a rapid review to support COVID-19 antimicrobial prescribing. Clin Infect Dis. 2020;71(9):2459–68.PubMed
6.
go back to reference Garcia-Vidal C, Sanjuan G, Moreno-Garcia E, Puerta-Alcalde P, Garcia-Pouton N, Chumbita M, et al. Incidence of co-infections and superinfections in hospitalized patients with COVID-19: a retrospective cohort study. Clin Microbiol Infect. 2021;27(1):83–8.CrossRefPubMed Garcia-Vidal C, Sanjuan G, Moreno-Garcia E, Puerta-Alcalde P, Garcia-Pouton N, Chumbita M, et al. Incidence of co-infections and superinfections in hospitalized patients with COVID-19: a retrospective cohort study. Clin Microbiol Infect. 2021;27(1):83–8.CrossRefPubMed
8.
go back to reference Giufre M, Daprai L, Cardines R, Bernaschi P, Rava L, Accogli M, et al. Carriage of Haemophilus influenzae in the oropharynx of young children and molecular epidemiology of the isolates after fifteen years of H. influenzae type b vaccination in Italy. Vaccine. 2015;33(46):6227–34.CrossRefPubMed Giufre M, Daprai L, Cardines R, Bernaschi P, Rava L, Accogli M, et al. Carriage of Haemophilus influenzae in the oropharynx of young children and molecular epidemiology of the isolates after fifteen years of H. influenzae type b vaccination in Italy. Vaccine. 2015;33(46):6227–34.CrossRefPubMed
9.
go back to reference Grousd JA, Rich HE, Alcorn JF. Host-pathogen interactions in gram-positive bacterial pneumonia. Clin Microbiol Rev. 2019;32(3). Grousd JA, Rich HE, Alcorn JF. Host-pathogen interactions in gram-positive bacterial pneumonia. Clin Microbiol Rev. 2019;32(3).
10.
go back to reference Juan CH, Fang SY, Chou CH, Tsai TY, Lin YT. Clinical characteristics of patients with pneumonia caused by Klebsiella pneumoniae in Taiwan and prevalence of antimicrobial-resistant and hypervirulent strains: a retrospective study. Antimicrob Resist Infect Control. 2020;9(1):4.CrossRefPubMedPubMedCentral Juan CH, Fang SY, Chou CH, Tsai TY, Lin YT. Clinical characteristics of patients with pneumonia caused by Klebsiella pneumoniae in Taiwan and prevalence of antimicrobial-resistant and hypervirulent strains: a retrospective study. Antimicrob Resist Infect Control. 2020;9(1):4.CrossRefPubMedPubMedCentral
12.
go back to reference Ciptaningtyas VR, De Mast Q, De Jonge MI. The burden and etiology of lower respiratory tract infections in children under five years of age in Indonesia. J Infect Dev Ctries. 2021;15(5):603–14.CrossRefPubMed Ciptaningtyas VR, De Mast Q, De Jonge MI. The burden and etiology of lower respiratory tract infections in children under five years of age in Indonesia. J Infect Dev Ctries. 2021;15(5):603–14.CrossRefPubMed
13.
go back to reference Carvalho Mda G, Tondella ML, McCaustland K, Weidlich L, McGee L, Mayer LW, et al. Evaluation and improvement of real-time PCR assays targeting lytA, ply, and psaA genes for detection of pneumococcal DNA. J Clin Microbiol. 2007;45(8):2460–6.CrossRefPubMed Carvalho Mda G, Tondella ML, McCaustland K, Weidlich L, McGee L, Mayer LW, et al. Evaluation and improvement of real-time PCR assays targeting lytA, ply, and psaA genes for detection of pneumococcal DNA. J Clin Microbiol. 2007;45(8):2460–6.CrossRefPubMed
14.
go back to reference Wang X, Mair R, Hatcher C, Theodore MJ, Edmond K, Wu HM, et al. Detection of bacterial pathogens in Mongolia meningitis surveillance with a new real-time PCR assay to detect Haemophilus influenzae. Int J Med Microbiol. 2011;301(4):303–9.CrossRefPubMed Wang X, Mair R, Hatcher C, Theodore MJ, Edmond K, Wu HM, et al. Detection of bacterial pathogens in Mongolia meningitis surveillance with a new real-time PCR assay to detect Haemophilus influenzae. Int J Med Microbiol. 2011;301(4):303–9.CrossRefPubMed
15.
go back to reference Kilic A, Muldrew KL, Tang YW, Basustaoglu AC. Triplex real-time polymerase chain reaction assay for simultaneous detection of Staphylococcus aureus and coagulase-negative staphylococci and determination of methicillin resistance directly from positive blood culture bottles. Diagn Microbiol Infect Dis. 2010;66(4):349–55.CrossRefPubMed Kilic A, Muldrew KL, Tang YW, Basustaoglu AC. Triplex real-time polymerase chain reaction assay for simultaneous detection of Staphylococcus aureus and coagulase-negative staphylococci and determination of methicillin resistance directly from positive blood culture bottles. Diagn Microbiol Infect Dis. 2010;66(4):349–55.CrossRefPubMed
16.
go back to reference Fukumoto H, Sato Y, Hasegawa H, Saeki H, Katano H. Development of a new real-time PCR system for simultaneous detection of bacteria and fungi in pathological samples. Int J Clin Exp Pathol. 2015;8(11):15479–88.PubMedPubMedCentral Fukumoto H, Sato Y, Hasegawa H, Saeki H, Katano H. Development of a new real-time PCR system for simultaneous detection of bacteria and fungi in pathological samples. Int J Clin Exp Pathol. 2015;8(11):15479–88.PubMedPubMedCentral
18.
go back to reference Dunne EM, Murad C, Sudigdoadi S, Fadlyana E, Tarigan R, Indriyani SAK, et al. Carriage of Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, and Staphylococcus aureus in Indonesian children: a cross-sectional study. PLoS ONE. 2018;13(4): e0195098.CrossRefPubMedPubMedCentral Dunne EM, Murad C, Sudigdoadi S, Fadlyana E, Tarigan R, Indriyani SAK, et al. Carriage of Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, and Staphylococcus aureus in Indonesian children: a cross-sectional study. PLoS ONE. 2018;13(4): e0195098.CrossRefPubMedPubMedCentral
19.
go back to reference Safari D, Lestari AN, Khoeri MM, Tafroji W, Giri-Rachman EA, Harimurti K, et al. Nasopharyngeal carriage and antimicrobial susceptibility profile of Haemophilus influenzae among patients infected with HIV in Jakarta, Indonesia. Access Microbiol. 2020;2(12): acmi000165.CrossRefPubMedPubMedCentral Safari D, Lestari AN, Khoeri MM, Tafroji W, Giri-Rachman EA, Harimurti K, et al. Nasopharyngeal carriage and antimicrobial susceptibility profile of Haemophilus influenzae among patients infected with HIV in Jakarta, Indonesia. Access Microbiol. 2020;2(12): acmi000165.CrossRefPubMedPubMedCentral
20.
go back to reference Palaniappan PA, Mohamed Sukur S, Liow YL, Maniam S, Sherina F, Ahmad N. Carriage of Haemophilus influenzae among children attending childcare centres in Kuala Lumpur, Malaysia in the post vaccination era: a cross-sectional study. Vaccine. 2020;38(51):8232–7.CrossRefPubMed Palaniappan PA, Mohamed Sukur S, Liow YL, Maniam S, Sherina F, Ahmad N. Carriage of Haemophilus influenzae among children attending childcare centres in Kuala Lumpur, Malaysia in the post vaccination era: a cross-sectional study. Vaccine. 2020;38(51):8232–7.CrossRefPubMed
21.
go back to reference Ngocho JS, Minja L, van der Gaast-de Jongh CE, Rahamat-Langendoen JC, Langereis JD, Mmbaga BT, et al. Viral-bacterial (co-) occurrence in the upper airways and the risk of childhood pneumonia in resource-limited settings. J Infect. 2020;81(2):213–20.CrossRefPubMedPubMedCentral Ngocho JS, Minja L, van der Gaast-de Jongh CE, Rahamat-Langendoen JC, Langereis JD, Mmbaga BT, et al. Viral-bacterial (co-) occurrence in the upper airways and the risk of childhood pneumonia in resource-limited settings. J Infect. 2020;81(2):213–20.CrossRefPubMedPubMedCentral
23.
go back to reference Margolis E, Yates A, Levin BR. The ecology of nasal colonization of Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus: the role of competition and interactions with host’s immune response. BMC Microbiol. 2010;10:59.CrossRefPubMedPubMedCentral Margolis E, Yates A, Levin BR. The ecology of nasal colonization of Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus: the role of competition and interactions with host’s immune response. BMC Microbiol. 2010;10:59.CrossRefPubMedPubMedCentral
24.
go back to reference Farida H, Severin JA, Gasem MH, Keuter M, van den Broek P, Hermans PW, et al. Nasopharyngeal carriage of Klebsiella pneumoniae and other Gram-negative bacilli in pneumonia-prone age groups in Semarang, Indonesia. J Clin Microbiol. 2013;51(5):1614–6.CrossRefPubMedPubMedCentral Farida H, Severin JA, Gasem MH, Keuter M, van den Broek P, Hermans PW, et al. Nasopharyngeal carriage of Klebsiella pneumoniae and other Gram-negative bacilli in pneumonia-prone age groups in Semarang, Indonesia. J Clin Microbiol. 2013;51(5):1614–6.CrossRefPubMedPubMedCentral
Metadata
Title
Bacterial colonization of the upper airways of children positive and negative for SARS-CoV-2 during the COVID-19 pandemic
Authors
Vincentia Rizke Ciptaningtyas
Rebriarina Hapsari
Endang Sri Lestari
Helmia Farida
Quirijn de Mast
Marinus Isaäk de Jonge
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2022
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-022-07851-z

Other articles of this Issue 1/2022

BMC Infectious Diseases 1/2022 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.