Neonates colonized with pathogenic bacteria in the airways have a low-grade systemic inflammation

Nadia Rahman Fink, Bo Lund Chawes, Jonathan Thorsen, Jakob Stokholm, Karen Krogfelt, Susanne Schjørring, Marie Kragh, Klaus Bønnelykke, Susanne Brix, Hans Bisgaard*

*Corresponding author for this work

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Abstract

Background and Objectives: The development of childhood asthma is associated with neonatal colonization with pathogenic bacteria in hypopharynx. Furthermore, established asthma is associated with systemic low-grade inflammation. We here report on the association between neonatal colonization with pathogenic bacteria in hypopharynx and the development of systemic low-grade inflammation. Methods: Bacterial colonization of the hypopharynx with M. catharralis, H. influenzae and/or S. pneumoniae was assessed in asymptomatic children from the Copenhagen Prospective Studies on Asthma in Childhood2000 (COPSAC2000 ) cohort at age 1 month by culturing technique (N=238) and by quantitative polymerase chain reaction (qPCR) technique (N=249) and in the COPSAC2010 cohort by culturing at age 1 month (N=622) and again at age 3 months (N=613). Systemic low-grade inflammation was determined in both cohorts at age 6 months by measuring plasma levels of high-sensitivity C-reactive protein (hs-CRP), tumor necrosis factor-α (TNF-α) and interleukine-6 (lL-6). Results: In both cohorts, bacterial colonization was associated with increased levels of hs-CRP: COPSAC2000 , 1 month culturing (geometric mean ratio of colonized/non-colonized [95% CI]), 1.39 [0.97-2.01], p=0.08, 1 month qPCR, 1.55 [1.14-2.10], p<0.01. A multi‐parametric principal component analysis incorporating hs‐CRP, TNF‐α and IL‐6 confirmed a systemic inflammatory profile in children colonized with M. catharralis, H. influenzae and/or S. pneumoniae in the hypopharynx compared to non‐colonized children (p‐values<0.05). Conclusion: The composition of the upper airway microbiome in early life may cause systemic low‐grade inflammation.
Original languageEnglish
JournalAllergy
Volume73
Issue number11
Pages (from-to)2150-2159
ISSN0105-4538
DOIs
Publication statusPublished - 2018

Keywords

  • Asthma
  • Clinical immunology
  • Environment and hygiene hypothesis
  • Innate immunity
  • Pediatrics

Cite this

Rahman Fink, N., Chawes, B. L., Thorsen, J., Stokholm, J., Krogfelt, K., Schjørring, S., ... Bisgaard, H. (2018). Neonates colonized with pathogenic bacteria in the airways have a low-grade systemic inflammation. Allergy, 73(11), 2150-2159. https://doi.org/10.1111/all.13461
Rahman Fink, Nadia ; Chawes, Bo Lund ; Thorsen, Jonathan ; Stokholm, Jakob ; Krogfelt, Karen ; Schjørring, Susanne ; Kragh, Marie ; Bønnelykke, Klaus ; Brix, Susanne ; Bisgaard, Hans . / Neonates colonized with pathogenic bacteria in the airways have a low-grade systemic inflammation. In: Allergy. 2018 ; Vol. 73, No. 11. pp. 2150-2159.
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title = "Neonates colonized with pathogenic bacteria in the airways have a low-grade systemic inflammation",
abstract = "Background and Objectives: The development of childhood asthma is associated with neonatal colonization with pathogenic bacteria in hypopharynx. Furthermore, established asthma is associated with systemic low-grade inflammation. We here report on the association between neonatal colonization with pathogenic bacteria in hypopharynx and the development of systemic low-grade inflammation. Methods: Bacterial colonization of the hypopharynx with M. catharralis, H. influenzae and/or S. pneumoniae was assessed in asymptomatic children from the Copenhagen Prospective Studies on Asthma in Childhood2000 (COPSAC2000 ) cohort at age 1 month by culturing technique (N=238) and by quantitative polymerase chain reaction (qPCR) technique (N=249) and in the COPSAC2010 cohort by culturing at age 1 month (N=622) and again at age 3 months (N=613). Systemic low-grade inflammation was determined in both cohorts at age 6 months by measuring plasma levels of high-sensitivity C-reactive protein (hs-CRP), tumor necrosis factor-α (TNF-α) and interleukine-6 (lL-6). Results: In both cohorts, bacterial colonization was associated with increased levels of hs-CRP: COPSAC2000 , 1 month culturing (geometric mean ratio of colonized/non-colonized [95{\%} CI]), 1.39 [0.97-2.01], p=0.08, 1 month qPCR, 1.55 [1.14-2.10], p<0.01. A multi‐parametric principal component analysis incorporating hs‐CRP, TNF‐α and IL‐6 confirmed a systemic inflammatory profile in children colonized with M. catharralis, H. influenzae and/or S. pneumoniae in the hypopharynx compared to non‐colonized children (p‐values<0.05). Conclusion: The composition of the upper airway microbiome in early life may cause systemic low‐grade inflammation.",
keywords = "Asthma, Clinical immunology, Environment and hygiene hypothesis, Innate immunity, Pediatrics",
author = "{Rahman Fink}, Nadia and Chawes, {Bo Lund} and Jonathan Thorsen and Jakob Stokholm and Karen Krogfelt and Susanne Schj{\o}rring and Marie Kragh and Klaus B{\o}nnelykke and Susanne Brix and Hans Bisgaard",
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Rahman Fink, N, Chawes, BL, Thorsen, J, Stokholm, J, Krogfelt, K, Schjørring, S, Kragh, M, Bønnelykke, K, Brix, S & Bisgaard, H 2018, 'Neonates colonized with pathogenic bacteria in the airways have a low-grade systemic inflammation', Allergy, vol. 73, no. 11, pp. 2150-2159. https://doi.org/10.1111/all.13461

Neonates colonized with pathogenic bacteria in the airways have a low-grade systemic inflammation. / Rahman Fink, Nadia; Chawes, Bo Lund; Thorsen, Jonathan; Stokholm, Jakob; Krogfelt, Karen ; Schjørring, Susanne; Kragh, Marie; Bønnelykke, Klaus; Brix, Susanne; Bisgaard, Hans .

In: Allergy, Vol. 73, No. 11, 2018, p. 2150-2159.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Neonates colonized with pathogenic bacteria in the airways have a low-grade systemic inflammation

AU - Rahman Fink, Nadia

AU - Chawes, Bo Lund

AU - Thorsen, Jonathan

AU - Stokholm, Jakob

AU - Krogfelt, Karen

AU - Schjørring, Susanne

AU - Kragh, Marie

AU - Bønnelykke, Klaus

AU - Brix, Susanne

AU - Bisgaard, Hans

PY - 2018

Y1 - 2018

N2 - Background and Objectives: The development of childhood asthma is associated with neonatal colonization with pathogenic bacteria in hypopharynx. Furthermore, established asthma is associated with systemic low-grade inflammation. We here report on the association between neonatal colonization with pathogenic bacteria in hypopharynx and the development of systemic low-grade inflammation. Methods: Bacterial colonization of the hypopharynx with M. catharralis, H. influenzae and/or S. pneumoniae was assessed in asymptomatic children from the Copenhagen Prospective Studies on Asthma in Childhood2000 (COPSAC2000 ) cohort at age 1 month by culturing technique (N=238) and by quantitative polymerase chain reaction (qPCR) technique (N=249) and in the COPSAC2010 cohort by culturing at age 1 month (N=622) and again at age 3 months (N=613). Systemic low-grade inflammation was determined in both cohorts at age 6 months by measuring plasma levels of high-sensitivity C-reactive protein (hs-CRP), tumor necrosis factor-α (TNF-α) and interleukine-6 (lL-6). Results: In both cohorts, bacterial colonization was associated with increased levels of hs-CRP: COPSAC2000 , 1 month culturing (geometric mean ratio of colonized/non-colonized [95% CI]), 1.39 [0.97-2.01], p=0.08, 1 month qPCR, 1.55 [1.14-2.10], p<0.01. A multi‐parametric principal component analysis incorporating hs‐CRP, TNF‐α and IL‐6 confirmed a systemic inflammatory profile in children colonized with M. catharralis, H. influenzae and/or S. pneumoniae in the hypopharynx compared to non‐colonized children (p‐values<0.05). Conclusion: The composition of the upper airway microbiome in early life may cause systemic low‐grade inflammation.

AB - Background and Objectives: The development of childhood asthma is associated with neonatal colonization with pathogenic bacteria in hypopharynx. Furthermore, established asthma is associated with systemic low-grade inflammation. We here report on the association between neonatal colonization with pathogenic bacteria in hypopharynx and the development of systemic low-grade inflammation. Methods: Bacterial colonization of the hypopharynx with M. catharralis, H. influenzae and/or S. pneumoniae was assessed in asymptomatic children from the Copenhagen Prospective Studies on Asthma in Childhood2000 (COPSAC2000 ) cohort at age 1 month by culturing technique (N=238) and by quantitative polymerase chain reaction (qPCR) technique (N=249) and in the COPSAC2010 cohort by culturing at age 1 month (N=622) and again at age 3 months (N=613). Systemic low-grade inflammation was determined in both cohorts at age 6 months by measuring plasma levels of high-sensitivity C-reactive protein (hs-CRP), tumor necrosis factor-α (TNF-α) and interleukine-6 (lL-6). Results: In both cohorts, bacterial colonization was associated with increased levels of hs-CRP: COPSAC2000 , 1 month culturing (geometric mean ratio of colonized/non-colonized [95% CI]), 1.39 [0.97-2.01], p=0.08, 1 month qPCR, 1.55 [1.14-2.10], p<0.01. A multi‐parametric principal component analysis incorporating hs‐CRP, TNF‐α and IL‐6 confirmed a systemic inflammatory profile in children colonized with M. catharralis, H. influenzae and/or S. pneumoniae in the hypopharynx compared to non‐colonized children (p‐values<0.05). Conclusion: The composition of the upper airway microbiome in early life may cause systemic low‐grade inflammation.

KW - Asthma

KW - Clinical immunology

KW - Environment and hygiene hypothesis

KW - Innate immunity

KW - Pediatrics

U2 - 10.1111/all.13461

DO - 10.1111/all.13461

M3 - Journal article

VL - 73

SP - 2150

EP - 2159

JO - Allergy: European Journal of Allergy and Clinical Immunology

JF - Allergy: European Journal of Allergy and Clinical Immunology

SN - 0105-4538

IS - 11

ER -

Rahman Fink N, Chawes BL, Thorsen J, Stokholm J, Krogfelt K, Schjørring S et al. Neonates colonized with pathogenic bacteria in the airways have a low-grade systemic inflammation. Allergy. 2018;73(11):2150-2159. https://doi.org/10.1111/all.13461