Skip to main content
Top
Published in: Gut Pathogens 1/2018

Open Access 01-12-2018 | Research

Possible correlation between gut microbiota and immunity among healthy middle-aged and elderly people in southwest China

Authors: Xi Shen, Junjie Miao, Qun Wan, Shuyue Wang, Ming Li, Fangfang Pu, Guoqing Wang, Wei Qian, Qian Yu, Francesco Marotta, Fang He

Published in: Gut Pathogens | Issue 1/2018

Login to get access

Abstract

Background

The present study was conducted to investigate the possible association between gut microbes and immunity among healthy middle-aged and elderly individuals in southwest China. A total of 148 healthy adults aged ≥ 50 years were divided into two age groups: middle-aged group (50–59 years; n = 67, 54.13 ± 3.32) and elderly group (≥ 60 years; n = 81, 64.70 ± 3.93). Blood samples were collected to measure serum immune and biochemical indices. Gut microbiota compositions of the groups were characterized on the basis of faecal DNA using 16S rRNA gene sequencing.

Results

Among the detected gut microbes, the presence of Alistipes was negatively correlated with age in both groups. In the middle-aged group, age was negatively correlated with the presence of Desulfovibrio and Faecalibacterium. In the elderly group, Coprococcus was present at significantly higher levels; age was negatively correlated with the presence of Lachnobacterium, Oxalobacter and the Chao index, whereas positively correlated with the presence of Sutterella. In the middle-aged group, the presence of Bacteroidetes was positively correlated with serum immunoglobulin G (IgG) levels and the percent of CD8+ T cells and negatively correlated with the CD4+/CD8+ ratio; the presence of Firmicutes was negatively correlated with IgM levels; Bacteroidetes/Firmicutes ratio was positively correlated with IgG and IgM levels and Simpson index was negatively correlated with the percent of CD8+ T cells and positively correlated with CD4+/CD8+ ratio. In the elderly group, the presence of Verrucomicrobia (identified as genus Akkermansia) was positively correlated with IgA levels and the percent of CD8+ T cells and negatively correlated with the percent of CD4+ T cells and CD4+/CD8+ ratio; the Chao index and observed species were positively correlated with IgA levels.

Conclusions

These results indicated that ageing could significantly correlate with the composition of gut microbiota in terms of quantity and quality. Changes in gut microbiota caused by ageing, characterized by decreased Bacteroidetes levels, might be associated with immunosenescence among healthy middle-aged and elderly people in southwest China.
Appendix
Available only for authorised users
Literature
1.
go back to reference Alonso-Fernández P, De la Fuente M. Role of the immune system in aging and longevity. Curr Aging Sci. 2011;4(2):78–1002.CrossRefPubMed Alonso-Fernández P, De la Fuente M. Role of the immune system in aging and longevity. Curr Aging Sci. 2011;4(2):78–1002.CrossRefPubMed
3.
go back to reference Perez Martinez G, Bäuerl C, Collado MC. Understanding gut microbiota in elderly’s health will enable intervention through probiotics. Benef Microb. 2014;5(3):235–46.CrossRef Perez Martinez G, Bäuerl C, Collado MC. Understanding gut microbiota in elderly’s health will enable intervention through probiotics. Benef Microb. 2014;5(3):235–46.CrossRef
4.
go back to reference Ginaldi L, et al. Immunological changes in the elderly. Aging Clin Exp Res. 1999;11(5):281–6.CrossRef Ginaldi L, et al. Immunological changes in the elderly. Aging Clin Exp Res. 1999;11(5):281–6.CrossRef
5.
go back to reference Castle SC. Clinical relevance of age-related immune dysfunction. Clin Infect Dis. 2000;31(2):578–85.CrossRefPubMed Castle SC. Clinical relevance of age-related immune dysfunction. Clin Infect Dis. 2000;31(2):578–85.CrossRefPubMed
6.
go back to reference Fulop T, et al. Cellular signaling in the aging immune system. Curr Opin Immunol. 2014;29:105–11.CrossRefPubMed Fulop T, et al. Cellular signaling in the aging immune system. Curr Opin Immunol. 2014;29:105–11.CrossRefPubMed
7.
go back to reference Ostan R, et al. Immunosenescence and immunogenetics of humanlongevity. Neuroimmunomodulation. 2008;15(4–6):224–40.CrossRefPubMed Ostan R, et al. Immunosenescence and immunogenetics of humanlongevity. Neuroimmunomodulation. 2008;15(4–6):224–40.CrossRefPubMed
8.
go back to reference Castelo-Branco Camil, Soveral Iris. The immune system and aging: a review. Gynecol Endocrinol. 2014;30(1):16–22.CrossRefPubMed Castelo-Branco Camil, Soveral Iris. The immune system and aging: a review. Gynecol Endocrinol. 2014;30(1):16–22.CrossRefPubMed
10.
go back to reference Mäkivuokko H, et al. The effect of age and non-steroidal anti-inflammatory drugs on human intestinal microbiota composition. Br J Nutr. 2010;103(2):227–34.CrossRefPubMed Mäkivuokko H, et al. The effect of age and non-steroidal anti-inflammatory drugs on human intestinal microbiota composition. Br J Nutr. 2010;103(2):227–34.CrossRefPubMed
11.
go back to reference Sommer Felix, Bäckhed Fredrik. The gut microbiota—masters of host development and physiology. Nat Rev Microbiol. 2013;11(4):227.CrossRefPubMed Sommer Felix, Bäckhed Fredrik. The gut microbiota—masters of host development and physiology. Nat Rev Microbiol. 2013;11(4):227.CrossRefPubMed
12.
go back to reference Dethlefsen L, et al. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008;6(11):e280.CrossRefPubMedPubMedCentral Dethlefsen L, et al. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008;6(11):e280.CrossRefPubMedPubMedCentral
13.
14.
go back to reference Guigoz Yves, Doré Joël, Schiffrin Eduardo J. The inflammatory status of old age can be nurtured from the intestinal environment. Curr Opin Clin Nutr Metab Care. 2008;11(1):13–20.CrossRefPubMed Guigoz Yves, Doré Joël, Schiffrin Eduardo J. The inflammatory status of old age can be nurtured from the intestinal environment. Curr Opin Clin Nutr Metab Care. 2008;11(1):13–20.CrossRefPubMed
15.
16.
go back to reference Kawase M, et al. Orally administered heat-killed Lactobacillus gasseri TMC0356 can upregulate cell-mediated immunity in senescence-accelerated mice. FEMS Microbiol Lett. 2011;326(2):125–30.CrossRefPubMed Kawase M, et al. Orally administered heat-killed Lactobacillus gasseri TMC0356 can upregulate cell-mediated immunity in senescence-accelerated mice. FEMS Microbiol Lett. 2011;326(2):125–30.CrossRefPubMed
17.
go back to reference Fangfang P, Yue G, et al. Yogurt supplemented with probiotics can protect the healthy elderly from respiratory infections: a randomized controlled open-label trial. Clin Interv Aging. 2017;12:1223–31.CrossRef Fangfang P, Yue G, et al. Yogurt supplemented with probiotics can protect the healthy elderly from respiratory infections: a randomized controlled open-label trial. Clin Interv Aging. 2017;12:1223–31.CrossRef
18.
go back to reference Harata G, Kumar H, He F, Miyazawa K, Yoda K, Kawase M, et al. Probiotics modulate gut microbiota and health status in Japanese cedar pollinosis patients during the pollen season. Eur J Nutr. 2017;56(7):2245–53.CrossRefPubMed Harata G, Kumar H, He F, Miyazawa K, Yoda K, Kawase M, et al. Probiotics modulate gut microbiota and health status in Japanese cedar pollinosis patients during the pollen season. Eur J Nutr. 2017;56(7):2245–53.CrossRefPubMed
19.
go back to reference Mueller S, et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol. 2006;72(2):1027–33.CrossRefPubMedPubMedCentral Mueller S, et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol. 2006;72(2):1027–33.CrossRefPubMedPubMedCentral
20.
go back to reference Guigoz Y, et al. Effects of oligosaccharide on the faecal flora and non-specific immune system in elderly people. Nutr Res. 2002;22(1):13–25.CrossRef Guigoz Y, et al. Effects of oligosaccharide on the faecal flora and non-specific immune system in elderly people. Nutr Res. 2002;22(1):13–25.CrossRef
21.
go back to reference Tiihonen Kirsti, Ouwehand Arthur C, Rautonen Nina. Human intestinal microbiota and healthy ageing. Ageing Res Rev. 2010;9(2):107–16.CrossRefPubMed Tiihonen Kirsti, Ouwehand Arthur C, Rautonen Nina. Human intestinal microbiota and healthy ageing. Ageing Res Rev. 2010;9(2):107–16.CrossRefPubMed
22.
go back to reference Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207.CrossRef Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486(7402):207.CrossRef
24.
25.
go back to reference Sokol H, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci. 2008;105(43):16731–6.CrossRefPubMedPubMedCentral Sokol H, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci. 2008;105(43):16731–6.CrossRefPubMedPubMedCentral
27.
go back to reference Jiang H, et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun. 2015;48:186–94.CrossRefPubMed Jiang H, et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun. 2015;48:186–94.CrossRefPubMed
28.
go back to reference De Vos P, et al. The firmicutes, vol. 3. Berlin: Springer; 2009. De Vos P, et al. The firmicutes, vol. 3. Berlin: Springer; 2009.
29.
go back to reference Zwielehner J, et al. Combined PCR-DGGE fingerprinting and quantitative-PCR indicates shifts in fecal population sizes and diversity of Bacteroides, bifidobacteria and Clostridium cluster IV in institutionalized elderly. Exp Gerontol. 2009;44(6):440–6.CrossRefPubMed Zwielehner J, et al. Combined PCR-DGGE fingerprinting and quantitative-PCR indicates shifts in fecal population sizes and diversity of Bacteroides, bifidobacteria and Clostridium cluster IV in institutionalized elderly. Exp Gerontol. 2009;44(6):440–6.CrossRefPubMed
30.
go back to reference Thevaranjan N, et al. Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host Microb. 2017;21(4):455–66.CrossRef Thevaranjan N, et al. Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host Microb. 2017;21(4):455–66.CrossRef
31.
go back to reference Franceschi C, et al. Inflamm-aging: an evolutionary perspective on immunosenescence. Ann NY Acad Sci. 2000;908(1):244–54.CrossRefPubMed Franceschi C, et al. Inflamm-aging: an evolutionary perspective on immunosenescence. Ann NY Acad Sci. 2000;908(1):244–54.CrossRefPubMed
32.
33.
go back to reference Ligthart GJ, et al. Admission criteria for immunogerontological studies in man: the SENIEUR protocol. Mech Ageing Dev. 1984;28(1):47–55.CrossRefPubMed Ligthart GJ, et al. Admission criteria for immunogerontological studies in man: the SENIEUR protocol. Mech Ageing Dev. 1984;28(1):47–55.CrossRefPubMed
35.
go back to reference van Passel MWJ, et al. The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PloS ONE. 2011;6(3):16876.CrossRef van Passel MWJ, et al. The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes. PloS ONE. 2011;6(3):16876.CrossRef
36.
go back to reference Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Nat Acad Sci. 2013;110(22):9066–71.CrossRefPubMedPubMedCentral Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Nat Acad Sci. 2013;110(22):9066–71.CrossRefPubMedPubMedCentral
Metadata
Title
Possible correlation between gut microbiota and immunity among healthy middle-aged and elderly people in southwest China
Authors
Xi Shen
Junjie Miao
Qun Wan
Shuyue Wang
Ming Li
Fangfang Pu
Guoqing Wang
Wei Qian
Qian Yu
Francesco Marotta
Fang He
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2018
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-018-0231-3

Other articles of this Issue 1/2018

Gut Pathogens 1/2018 Go to the issue
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 discuss last year's major advances in heart failure and cardiomyopathies.