Fungal allergic sensitisation in young rural Zimbabwean children: Gut mycobiome and seroreactivity characteristics

Summary: Background: The prevalence of allergic diseases has increased over the last few decades, with sensitisation to fungal allergens and gut microbiome dysbiosis implicated in this trend. The fungal community in the gut (mycobiome) has yet to be characterised and related to fungal allergic sens...

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Main Authors: Lorraine Tsitsi Pfavayi, Elopy Nimele Sibanda, Stephen Baker, Mark Woolhouse, Takafira Mduluza, Francisca Mutapi
Format: Article
Language:English
Published: Elsevier 2021-12-01
Series:Current Research in Microbial Sciences
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2666517421000626
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author Lorraine Tsitsi Pfavayi
Elopy Nimele Sibanda
Stephen Baker
Mark Woolhouse
Takafira Mduluza
Francisca Mutapi
author_facet Lorraine Tsitsi Pfavayi
Elopy Nimele Sibanda
Stephen Baker
Mark Woolhouse
Takafira Mduluza
Francisca Mutapi
author_sort Lorraine Tsitsi Pfavayi
collection DOAJ
description Summary: Background: The prevalence of allergic diseases has increased over the last few decades, with sensitisation to fungal allergens and gut microbiome dysbiosis implicated in this trend. The fungal community in the gut (mycobiome) has yet to be characterised and related to fungal allergic sensitisation. Thus, we characterised the gut mycobiome and related it to fungal sensitisation and seroreactivity among Zimbabwean children. We further determined the effect of host age, sex, Schistosoma haematobium infection and mycobiome composition on fungal sensitisation and seroreactivity. Methods: Using shotgun metagenomic sequencing, we characterised the gut microbiome of stool samples of 116 preschool aged children (PSAC) (≤5 years old, 57(49.1%) male and 59 (50.9%) female). Sensitisation to common fungi in Zimbabwe was assessed using skin prick tests (SPTs). Allergen-specific IgM, IgA, IgG, IgE and IgG4 antibodies were quantified by ELISA. We analysed the relationship between fungal genera and SPT reactivity by ANOVA; fungal genera and IgE antibody reactivity by linear regression; variation in mycobiome abundance with host and environmental factors by PERMANOVA; SPT reactivity and host and environmental factors by logistic regression; seroreactivity and host and environmental factors by ANOVA. Results: The mycobiome formed <1% of the sequenced gut microbiome and 228 fungal genera were identified. The most abundant genera detected were Protomyces, Taphrina, and Aspergillus. S.haematobium infection had a significant effect on fungal genera. Prevalence of SPT sensitisation to ≥1 fungal species was 96%, and individuals were frequently sensitised to Saccharomyces cerevisiae. Antibodies were detected in 100% of the population. There was no relationship between mycobiome abundance and IgE titres or IgE/IgG4 ratios for each fungal species; no significant differences between SPT reactivity and abundance of fungal species except for S. cerevisiae; and fungal seroreactivity did not significantly differ with age. There were some sex (m>f for, Epicoccum nigrum and Penicillium chrysogenum) and SPT reactivity –related differences in seroreactivity. Conclusion: This is the first comprehensive characterisation of gut mycobiome and fungal allergic sensitisation of rural children in Zimbabwe. Although reported allergic disease is low there is a high percentage of sensitisation. Further studies with larger populations are required to understand the role of the mycobiome in allergic diseases.
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spelling doaj.art-f560d4627bfd43feb9374e7bccb90b052022-12-21T19:33:56ZengElsevierCurrent Research in Microbial Sciences2666-51742021-12-012100082Fungal allergic sensitisation in young rural Zimbabwean children: Gut mycobiome and seroreactivity characteristicsLorraine Tsitsi Pfavayi0Elopy Nimele Sibanda1Stephen Baker2Mark Woolhouse3Takafira Mduluza4Francisca Mutapi5Nuffield Department of Medicine, Centre for Tropical Medicine and Global Health, University of Oxford, Old Road Campus, Headington, Oxford OX3 7BN, UK; Institute of Immunology &amp; Infection Research, University of Edinburgh, Ashworth Laboratories, King's Buildings, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK; NIHR Global Health Research Unit Tackling Infections to Benefit Africa (TIBA), University of Edinburgh, Ashworth Laboratories, King's Buildings, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK; Corresponding author at: Institute of Immunology &amp; Infection Research, University of Edinburgh, Ashworth Laboratories, King's Buildings, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK.Asthma Allergy and Immunology Clinic, Twin Palms Medical Centre, Harare, Zimbabwe; Department of Pathology, National University of Science and Technology (NUST) Medical School, Bulawayo, Zimbabwe; TIBA Zimbabwe, NIHR Global Health Research Unit Tackling Infections to Benefit Africa (TIBA), University of Edinburgh, Edinburgh, UKDepartment of Medicine, Cambridge Institute of Therapeutic Immunology and Infectious Disease (CITIID), Cambridge Biomedical Campus, University of Cambridge, Cambridge CB2 0AW, UKNIHR Global Health Research Unit Tackling Infections to Benefit Africa (TIBA), University of Edinburgh, Ashworth Laboratories, King's Buildings, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK; Usher Institute of Population Health Sciences and Informatics, Ashworth Laboratories, University of Edinburgh, Edinburgh, UKTIBA Zimbabwe, NIHR Global Health Research Unit Tackling Infections to Benefit Africa (TIBA), University of Edinburgh, Edinburgh, UK; Department of Biochemistry, University of Zimbabwe, Mount Pleasant, Harare, ZimbabweInstitute of Immunology &amp; Infection Research, University of Edinburgh, Ashworth Laboratories, King's Buildings, Charlotte Auerbach Road, Edinburgh EH9 3FL, UK; NIHR Global Health Research Unit Tackling Infections to Benefit Africa (TIBA), University of Edinburgh, Ashworth Laboratories, King's Buildings, Charlotte Auerbach Road, Edinburgh EH9 3FL, UKSummary: Background: The prevalence of allergic diseases has increased over the last few decades, with sensitisation to fungal allergens and gut microbiome dysbiosis implicated in this trend. The fungal community in the gut (mycobiome) has yet to be characterised and related to fungal allergic sensitisation. Thus, we characterised the gut mycobiome and related it to fungal sensitisation and seroreactivity among Zimbabwean children. We further determined the effect of host age, sex, Schistosoma haematobium infection and mycobiome composition on fungal sensitisation and seroreactivity. Methods: Using shotgun metagenomic sequencing, we characterised the gut microbiome of stool samples of 116 preschool aged children (PSAC) (≤5 years old, 57(49.1%) male and 59 (50.9%) female). Sensitisation to common fungi in Zimbabwe was assessed using skin prick tests (SPTs). Allergen-specific IgM, IgA, IgG, IgE and IgG4 antibodies were quantified by ELISA. We analysed the relationship between fungal genera and SPT reactivity by ANOVA; fungal genera and IgE antibody reactivity by linear regression; variation in mycobiome abundance with host and environmental factors by PERMANOVA; SPT reactivity and host and environmental factors by logistic regression; seroreactivity and host and environmental factors by ANOVA. Results: The mycobiome formed <1% of the sequenced gut microbiome and 228 fungal genera were identified. The most abundant genera detected were Protomyces, Taphrina, and Aspergillus. S.haematobium infection had a significant effect on fungal genera. Prevalence of SPT sensitisation to ≥1 fungal species was 96%, and individuals were frequently sensitised to Saccharomyces cerevisiae. Antibodies were detected in 100% of the population. There was no relationship between mycobiome abundance and IgE titres or IgE/IgG4 ratios for each fungal species; no significant differences between SPT reactivity and abundance of fungal species except for S. cerevisiae; and fungal seroreactivity did not significantly differ with age. There were some sex (m>f for, Epicoccum nigrum and Penicillium chrysogenum) and SPT reactivity –related differences in seroreactivity. Conclusion: This is the first comprehensive characterisation of gut mycobiome and fungal allergic sensitisation of rural children in Zimbabwe. Although reported allergic disease is low there is a high percentage of sensitisation. Further studies with larger populations are required to understand the role of the mycobiome in allergic diseases.http://www.sciencedirect.com/science/article/pii/S2666517421000626Fungal sensitisationMycobiomeChildrenZimbabweSeroreactivity
spellingShingle Lorraine Tsitsi Pfavayi
Elopy Nimele Sibanda
Stephen Baker
Mark Woolhouse
Takafira Mduluza
Francisca Mutapi
Fungal allergic sensitisation in young rural Zimbabwean children: Gut mycobiome and seroreactivity characteristics
Current Research in Microbial Sciences
Fungal sensitisation
Mycobiome
Children
Zimbabwe
Seroreactivity
title Fungal allergic sensitisation in young rural Zimbabwean children: Gut mycobiome and seroreactivity characteristics
title_full Fungal allergic sensitisation in young rural Zimbabwean children: Gut mycobiome and seroreactivity characteristics
title_fullStr Fungal allergic sensitisation in young rural Zimbabwean children: Gut mycobiome and seroreactivity characteristics
title_full_unstemmed Fungal allergic sensitisation in young rural Zimbabwean children: Gut mycobiome and seroreactivity characteristics
title_short Fungal allergic sensitisation in young rural Zimbabwean children: Gut mycobiome and seroreactivity characteristics
title_sort fungal allergic sensitisation in young rural zimbabwean children gut mycobiome and seroreactivity characteristics
topic Fungal sensitisation
Mycobiome
Children
Zimbabwe
Seroreactivity
url http://www.sciencedirect.com/science/article/pii/S2666517421000626
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