Increased nasal Streptococcus pneumoniae presence in Western environment associated with allergic conditions in Chinese immigrants

Michelle J Schwager; Yong Song; Ingrid A Laing; Aarti Saiganesh; Jing Guo; Peter N Le Souëf; Guicheng Zhang

doi:10.1016/j.ijheh.2021.113735

Increased nasal Streptococcus pneumoniae presence in Western environment associated with allergic conditions in Chinese immigrants

Int J Hyg Environ Health. 2021 May:234:113735. doi: 10.1016/j.ijheh.2021.113735. Epub 2021 Mar 13.

Authors

Michelle J Schwager¹, Yong Song², Ingrid A Laing³, Aarti Saiganesh⁴, Jing Guo⁵, Peter N Le Souëf⁶, Guicheng Zhang⁷

Affiliations

¹ School of Public Health, Curtin University, GPO Box U1987, Perth, Western Australia, 6845, Australia; Centre for Genetic Origins of Health and Disease, Curtin University and the University of Western Australia (M409), Perth, Western Australia, 6009, Australia; Curtin Health Innovation Research Institute, Curtin University, GPO Box U1987, Perth, Western Australia, 6845, Australia; Telethon Kids Institute, The University of Western Australia, PO Box 855, West Perth, Western Australia, 6872, Australia. Electronic address: michelle.schwager@postgrad.curtin.edu.au.
² School of Public Health, Curtin University, GPO Box U1987, Perth, Western Australia, 6845, Australia; Centre for Genetic Origins of Health and Disease, Curtin University and the University of Western Australia (M409), Perth, Western Australia, 6009, Australia. Electronic address: yong.song@utas.edu.au.
³ Telethon Kids Institute, The University of Western Australia, PO Box 855, West Perth, Western Australia, 6872, Australia; Division of Cardiovascular and Respiratory Sciences, The University of Western Australia (M560), 35 Stirling Highway, Perth, Western Australia, 6009, Australia. Electronic address: ingrid.laing@telethonkids.org.au.
⁴ Telethon Kids Institute, The University of Western Australia, PO Box 855, West Perth, Western Australia, 6872, Australia. Electronic address: Aarti.Saiganesh@telethonkids.org.au.
⁵ School of Public Health, Curtin University, GPO Box U1987, Perth, Western Australia, 6845, Australia; Centre for Genetic Origins of Health and Disease, Curtin University and the University of Western Australia (M409), Perth, Western Australia, 6009, Australia. Electronic address: jing.guo2@postgrad.curtin.edu.au.
⁶ Telethon Kids Institute, The University of Western Australia, PO Box 855, West Perth, Western Australia, 6872, Australia; Division of Paediatrics, School of Medicine, The University of Western Australia (M561), 35 Stirling Highway, Perth, Western Australia, 6009, Australia. Electronic address: peter.lesouef@uwa.edu.au.
⁷ School of Public Health, Curtin University, GPO Box U1987, Perth, Western Australia, 6845, Australia; Centre for Genetic Origins of Health and Disease, Curtin University and the University of Western Australia (M409), Perth, Western Australia, 6009, Australia; Curtin Health Innovation Research Institute, Curtin University, GPO Box U1987, Perth, Western Australia, 6845, Australia; Telethon Kids Institute, The University of Western Australia, PO Box 855, West Perth, Western Australia, 6872, Australia. Electronic address: brad.zhang@curtin.edu.au.

PMID: 33725492
DOI: 10.1016/j.ijheh.2021.113735

Abstract

Background: Chinese immigrants living in Australia experience increased allergic conditions: asthma, eczema, hay fever and wheeze. Recently we reported diminished innate cytokine responses in long-term immigrants, potentially increasing their pathogenic viral load and microbial carriage. We hypothesise that a Western environment changes the nasal microbiome profile, and this altered profile may be associated with the development of allergic conditions. In this cross-sectional study, we aimed to examine the loading of viral and microbial respiratory pathogens in the upper airway.

Methods: Adult Chinese immigrants were grouped depending on time spent in Australia: short-term (<6 years) or long-term (≥6 years). First, age- and gender-matched immigrants were selected for an initial screen using quantitative polymerase chain reaction (qPCR) micro-array panels. Then based on initial results the viruses, human parainfluenza 3 and rhinovirus, and the bacteria, Burkholderia spp., Staphylococcus aureus and Streptococcus pneumoniae, were validated using qPCR in the population. Associations for bacterial prevalence with atopic phenotypes were investigated.

Results: Pooling the initial screen and validation subjects, S. aureus and S. pneumoniae had higher prevalence in long-term compared with short-term subjects (25.0% vs 8.1%, P = 0.012; and 76.8% vs 48.4%, P = 0.002). Those immigrants with nasal S. pneumoniae presence resided longer (average time 90.4 months) in Australia than immigrants without S. pneumoniae (52.7 months; P = 0.001). After adjusting for confounders, Chinese immigrants with S. pneumoniae carriage have a five-fold increased risk of doctor-diagnosed eczema (odds ratio, OR 5.36, 95% CI: 1.10-26.14; P = 0.038) compared to immigrants without S. pneumoniae carriage. There was a trend of S. pneumoniae abundance correlating with reduced host Toll-like receptor gene expression.

Conclusion: Our findings suggest that nasal S. pneumoniae may play a role in the development of allergic conditions in Chinese immigrants in a Western environment.

Keywords: Allergy; Atopic eczema; Immigrants; Nasal colonization; Streptococcus pneumoniae; Western environment.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

China / epidemiology
Cross-Sectional Studies
Emigrants and Immigrants*
Humans
Hypersensitivity*
Staphylococcus aureus
Streptococcus pneumoniae