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Microbiome and health implications for ethnic minorities after enforced lifestyle changes

Nature Medicine volume 26, pages 1089–1095 (2020)Cite this article

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Abstract

Modern lifestyles increase the risk of chronic diseases, in part by modifying the microbiome, but the health effects of lifestyles enforced on ethnic minorities are understudied1,2,3. Lifestyle affects the microbiome early in life, when the microbiome is assembled and the immune system is undergoing maturation4,5,6. Moreover, the influence of lifestyle has been separated from genetic and geographic factors by studies of genetically similar populations and ethnically distinct groups living in the same geographic location7,8,9,10,11. The lifestyle of Irish Travellers, an ethnically distinct subpopulation, changed with legislation in 2002 that effectively ended nomadism and altered their living conditions. Comparative metagenomics of gut microbiomes shows that Irish Travellers retain a microbiota similar to that of non-industrialized societies. Their microbiota is associated with non-dietary factors and is proportionately linked with risk of microbiome-related metabolic disease. Our findings suggest there are microbiome-related public health implications when ethnic minorities are pressured to change lifestyles.

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Fig. 1: Distinct microbiome composition of the Irish Travellers.
Fig. 2: Sample-to-sample similarity network across a global gut microbiome landscape.
Fig. 3: The microbiota of Irish Travellers in relation to a change in living conditions from childhood to adulthood.
Fig. 4: A non-industrialized-like microbiome correlates with Traveller lifestyle.

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Data availability

The sequence data for the project are publicly available through the European Nucleotide Archive (https://www.ebi.ac.uk/ena/) under accession number PRJEB36820.

Code availability

The key analysis code, commands and R data objects used in the project are deposited in the GitHub repository at https://github.com/tsg-microbiome/TravellerHealthMetAnalysis/.

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Acknowledgements

We are deeply grateful to the Irish Traveller community. We are also grateful to B. O’Donoghue, C. Bernard and the members of the Traveller Visibility Group Health Unit in Cork city and K. McDonagh and members of the Travellers of North Cork (TNC) organization. We also thank A. Moloney of APC Microbiome Ireland for laboratory support and clinical nurses K. Power, C. Tobin and M. Daly, as well as L. Horgan and staff of the Irish Centre for Arthritis Research and Education (ICARE) Bone Densitometry Unit in Cork University Hospital. The guiding assistance of J. Sheehan is also acknowledged. The authors are supported in part by Science Foundation Ireland (SFI) in the form of a research center grant (no. 12/RC/2273) to APC Microbiome Ireland and by ICARE.

Author information

Author notes

  1. These authors contributed equally: David M. Keohane, Tarini Shankar Ghosh.

Authors and Affiliations

  1. APC Microbiome Ireland, University College Cork, Cork, Ireland

    David M. Keohane, Tarini Shankar Ghosh, Ian B. Jeffery, Michael G. Molloy, Paul W. O’Toole & Fergus Shanahan

  2. Department of Medicine, University College Cork, Cork, Ireland

    David M. Keohane, Michael G. Molloy & Fergus Shanahan

  3. School of Microbiology, University College Cork, Cork, Ireland

    Tarini Shankar Ghosh & Paul W. O’Toole

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Contributions

D.M.K. and T.S.G. contributed equally in writing the manuscript, securing the clinical material (D.M.K.) and performing bioinformatic analyses (T.S.G.). I.B.J., M.G.M., P.W.O. and F.S. each participated in the study design, planning, interpretation and writing.

Corresponding author

Correspondence to Fergus Shanahan.

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Competing interests

F.S. is a cofounder and shareholder of three campus companies: Alimentary Health, Tucana Health (now named 4D Pharma Cork) and Atlantia Food Clinical Trials. P.W.O. is a cofounder and shareholder of 4D Pharma Cork.

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Peer review information Alison Farrell was the primary editor on this article and managed its editorial process and peer review in collaboration with the rest of the editorial team.

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Extended data

Extended Data Fig. 1 Characteristics of the study population.

Characteristics of the Irish Travellers (n = 118; for whom microbiome data was available) including change in living conditions (childhood to adulthood).

Extended Data Fig. 2 Dietary patterns of Irish Travellers as compared to other Irish Cohorts.

a, Heatmap displaying median ranked consumption frequencies of various macro- and micro- food categories for the Irish Travellers and previously published cohorts of Young (n = 49) and Elderly (n = 192) Irish controls. For each group, the values in each cell indicates the corrected P-values obtained for each food category, when consumption frequencies of this food category within the group is compared with individuals belonging to all other groups. Two-sided Mann-Whitney Tests were used for this purpose and the final p-values were corrected using the Benjamini-Hochberg procedure. Only those cases with corrected p-values < 0.1 are shown. b, Principal Coordinate Analysis (PCoA) plot displaying the macronutrient based dietary profiles of the indicated groups and showing the association of specific dietary nutrients within each group. Elderly Irish community and Elderly Irish longstay refer to community and longstay (nursing home) dwelling elderly controls. The Irish Traveller cohort is indicated in red. c, Boxplot showing the Healthy Food Diversity (HFD) index values for the various Irish cohorts, namely Elderly Irish community (n = 111), elderly Irish ongstay (n = 53), Young Irish (n = 85) and Travellers (n = 131). Only those individuals with complete dietary records were included. Boxes within the boxplots denote the inter-quartile range (with the median indicated in bold) and the upper and lower whiskers extend to values that are either +1.5 X interquartile range from the third quartile (upper whisker) or to -1.5 X interquartile range from the first quartile (lower whisker). For the pairwise across group comparisons, the indicated p-values were obtained using post-hoc Dunns’ test after correction using Benjamini-Hochberg for multiple comparisons. d, PERMANOVA analysis of the dietary profiles in the three sub-groups of Irish Travellers (Group sizes for Non-industrialized-like: 37, Intermediate:39, Industrialized-like: 41) showing the similarity of diet across the three Traveller sub-groups. The p-value and R-squared of the analysis are also indicated.

Extended Data Fig. 3 Lower Variations of the dietary patterns within the Traveller sub-groups as compared to other Irish groups.

a, Heatmap showing the ranked median consumption levels of the five major food groups across the six Irish population groups, namely Traveller groups with a non-industrialized-like (n = 37), intermediate (n = 39) and industrialized-like (n = 41) microbiome, along with Young Non-traveller Irish (n = 85), Elderly Irish community (n = 111) and Elderly Irish Longstay (n = 53). Only those individuals with complete dietary records were included for this analysis. P-values are indicated (within the cells) for those scenarios where in the consumption of a major food group is significantly higher in a given population group with respect to all other groups. The p-values were computed using two-sided Mann–Whitney Tests corrected using Benjamini-Hochberg procedure. This heatmap shows that the variance among the Travellers is low and the main split in diet is between the Travellers and the other non-Traveller Irish. b, Boxplots showing the variation of Healthy Food Diversity index values across the six population groups. Significant P-values of the across-group pairwise comparisons (performed using the post-hoc Dunns test (two-sided) with Benjamini-Hochberg corrected FDR) are indicated. (NI-Like = Travellers with a Non-Industrialized-Like microbiome, I-Like = Travellers with an Industrialized-Like microbiome). Boxes within the boxplots denote the inter-quartile range (with the median indicated in bold) and the upper and lower whiskers extend to values that are either +1.5 X interquartile range from the third quartile (upper whisker) or to -1.5 X interquartile range from the first quartile (lower whisker).

Extended Data Fig. 4 Differentially abundant taxa shared by subsets of Irish Travellers with global industrialized or non-industrialized cohorts.

The heatmap shows taxon differences between the global non-industrialized societies (Fijian, Hadza and Peruvian) and the industrialized non-Traveller Irish population. The Irish Travellers are in the middle of this spectrum (arranged in the same order as the heatmap of Fig. 1d), and their pattern of sharing taxa with the other populations defines 3 groups of listed species.

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Keohane, D.M., Ghosh, T.S., Jeffery, I.B. et al. Microbiome and health implications for ethnic minorities after enforced lifestyle changes. Nat Med 26, 1089–1095 (2020). https://doi.org/10.1038/s41591-020-0963-8

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