Fecal Microbiota Monitoring in Elite Soccer Players Along the
                    2019–2020 Competitive Season

Elisa Viciani; Monica Barone; Tindaro Bongiovanni; Sara Quercia; Roberta Di Gesu; Giulio Pasta; Paolo Manetti; F.Marcello Iaia; Athos Trecroci; Simone Rampelli; Marco Candela; Elena Biagi; Andrea Castagnetti

doi:10.1055/a-1858-1810

International Journal of Sports Medicine, Table of Contents

Int J Sports Med 2022; 43(13): 1137-1147
DOI: 10.1055/a-1858-1810

Nutrition

Fecal Microbiota Monitoring in Elite Soccer Players Along the 2019–2020 Competitive Season

Elisa Viciani

¹Wellmicro Srl, Wellmicro Srl, Bologna, Italy

,

Monica Barone

²Department of Medical and Surgical Sciences, University of Bologna, Bologna, Italy

,

Tindaro Bongiovanni

³Department of Health, Nutrition and Exercise Physiology, Parma Calcio, Parma, Italy

⁴Department of Biomedical Sciences for Health, Università degli Studi di Milano, Milano, Italy

,

Sara Quercia

¹Wellmicro Srl, Wellmicro Srl, Bologna, Italy

,

Roberta Di Gesu

¹Wellmicro Srl, Wellmicro Srl, Bologna, Italy

,

Giulio Pasta

⁵Medical Department, Parma Calcio, Parma, Italy

,

Paolo Manetti

⁵Medical Department, Parma Calcio, Parma, Italy

,

F.Marcello Iaia

⁴Department of Biomedical Sciences for Health, Università degli Studi di Milano, Milano, Italy

,

Athos Trecroci

⁴Department of Biomedical Sciences for Health, Università degli Studi di Milano, Milano, Italy

,

Simone Rampelli

⁶Department of Pharmacy and Biotechnology, University of Bologna, BOLOGNA, Italy

,

Marco Candela

⁶Department of Pharmacy and Biotechnology, University of Bologna, BOLOGNA, Italy

,

Elena Biagi

⁶Department of Pharmacy and Biotechnology, University of Bologna, BOLOGNA, Italy

,

Andrea Castagnetti

¹Wellmicro Srl, Wellmicro Srl, Bologna, Italy

› Author Affiliations

Abstract

Physical exercise affects the human gut microbiota, which in turn influences athletes’ performance. The current understanding of how the microbiota of professional athletes changes along with different phases of training is sparse. We aim to characterize the fecal microbiota in elite soccer players along with different phases of a competitive season using 16 S rRNA gene sequencing. Fecal samples were collected after the summer off-season period, the pre-season retreat, the first half of the competitive season, and the 8 weeks of COVID-19 lockdown that interrupted the season 2019–2020. According to our results, the gut microbiota of professional athletes changes along with the phases of the season, characterized by different training, diet, nutritional surveillance, and environment sharing. Pre-season retreat, during which nutritional surveillance and exercise intensity were at their peak, caused a decrease in bacterial groups related to unhealthy lifestyle and an increase in health-promoting symbionts. The competitive season and forced interruption affected other features of the athletes’ microbiota, i.e., bacterial groups that respond to dietary fiber load and stress levels. Our longitudinal study, focusing on one of the most followed sports worldwide, provides baseline data for future comparisons and microbiome-targeting interventions aimed at developing personalized training and nutrition plans for performance maximization.

Key words

gut microbiota - athletes - soccer - longitudinal - 16 S rRNA sequencing

Full Text

References

References
1 Berg G, Rybakova D, Fischer D. et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome 2020; 8: 103
2 Lynch SV, Pedersen O. The human intestinal microbiome in health and disease. N Engl J Med 2016; 375: 2369-2379
3 Dominguez-Bello MG, Godoy-Vitorino F, Knight R. et al. Role of the microbiome in human development. Gut 2019; 68: 1108-1114
4 Deschasaux M, Bouter KE, Prodan A. et al. Depicting the composition of gut microbiota in a population with varied ethnic origins but shared geography. Nat Med 2018; 24: 1526-1531
5 He Y, Wu W, Zheng H-M. et al. Regional variation limits applications of healthy gut microbiome reference ranges and disease models. Nat Med 2018; 24: 1532-1535
6 Dwiyanto J, Hussain MH, Reidpath D. et al. Ethnicity influences the gut microbiota of individuals sharing a geographical location: a cross-sectional study from a middle-income country. Sci Rep 2021; 11: 2618
7 Marttinen M, Ala-Jaakkola R, Laitila A. et al. Gut microbiota, probiotics and physical performance in athletes and physically active individuals. Nutrients 2020; 12: 2936
8 Mohr AE, Jäger R, Carpenter KC. et al. The athletic gut microbiota. J Int Soc Sports Nutr 2020; 17: 24
9 Pedersini P, Turroni S, Villafañe JH. Gut microbiota and physical activity: Is there an evidence-based link?. Sci Total Environ 2020; 727: 138648
10 Tzemah Shahar R, Koren O, Matarasso S. et al. Attributes of physical activity and gut microbiome in adults: a systematic review. Int J Sports Med 2020; 41: 801-814
11 Han M, Yang K, Yang P. et al. Stratification of athletes’ gut microbiota: the multifaceted hubs associated with dietary factors, physical characteristics and performance. Gut Microbes 2020; 12: 1-18
12 Penney N, Barton W, Posma JM. et al. Investigating the role of diet and exercise in gut microbe-host cometabolism. mSystems 2020; 5: e00677-20
13 Petersen LM, Bautista EJ, Nguyen H. et al. Community characteristics of the gut microbiomes of competitive cyclists. Microbiome 2017; 5: 98
14 Barton W, Penney NC, Cronin O. et al. The microbiome of professional athletes differs from that of more sedentary subjects in composition and particularly at the functional metabolic level. Gut 2018; 67: 625-633
15 Scheiman J, Luber JM, Chavkin TA. et al. Meta-omics analysis of elite athletes identifies a performance-enhancing microbe that functions via lactate metabolism. Nat Med 2019; 25: 1104-1109
16 Bielik V, Hric I, BaláŽ V. et al. Gut microbiota diversity in lean athletes is associated with positive energy balance. Ann Nutr Metab 2020; 76: 242-250
17 Hampton-Marcell JT, Eshoo TW, Cook MD. et al. Comparative analysis of gut microbiota following changes in training volume among swimmers. Int J Sports Med 2020; 41: 292-299
18 Kulecka M, Fraczek B, Mikula M. et al. The composition and richness of the gut microbiota differentiate the top Polish endurance athletes from sedentary controls. Gut Microbes 2020; 11: 1374-1384
19 O’Donovan CM, Madigan SM, Garcia-Perez I. et al. Distinct microbiome composition and metabolome exists across subgroups of elite Irish athletes. J Sci Med Sport 2020; 23: 63-68
20 Cani PD, Van Hul M, Lefort C. et al. Microbial regulation of organismal energy homeostasis. Nat Metab 2019; 1: 34-46
21 Crowson MM, McClave SA. Does the intestinal microbiome impact athletic performance?. Curr Gastroenterol Rep 2020; 22: 53
22 Hughes RL. A review of the role of the gut microbiome in personalized sports nutrition. Front Nutr 2020; 6: 191
23 Keohane DM, Cronin O, O’Sullivan O. et al. Infographic. Athlete health and performance: no guts no glory. Br J Sports Med 2020; 54: 250-250
24 Clark A, Mach N. Exercise-induced stress behavior, gut-microbiota-brain axis and diet: a systematic review for athletes. J Int Soc Sports Nutr 2016; 13: 43
25 O’Donovan CM, Connor B, Madigan SM. et al. Instances of altered gut microbiomes among Irish cricketers over periods of travel in the lead up to the 2016 World Cup: a sequencing analysis. Travel Med Infect Dis 2020; 35: 101553
26 Pane M, Amoruso A, Deidda F. et al. Gut microbiota, probiotics, and sport: from clinical evidence to agonistic performance. J Clin Gastroenterol 2018; 52: S46-S49
27 Zheng D, Liwinski T, Elinav E. Interaction between microbiota and immunity in health and disease. Cell Res 2020; 30: 492-506
28 Rankin A, O’Donavon C, Madigan SM. et al. 'Microbes in sport' – The potential role of the gut microbiota in athlete health and performance. Br J Sports Med 2017; 51: 698-699
29 Clarke G, Stilling RM, Kennedy PJ. et al. Minireview: Gut microbiota: the neglected endocrine organ. Mol Endocrinol 2014; 28: 1221-1238
30 Moloney RD, Desbonnet L, Clarke G. et al. The microbiome: stress, health and disease. Mamm Genome 2014; 25: 49-74
31 Bermon S, Petriz B, Kajėnienė A. et al. The microbiota: an exercise immunology perspective. Exerc Immunol Rev 2015; 21: 70-79
32 Cronin O, O’Sullivan O, Barton W. et al. Gut microbiota: implications for sports and exercise medicine. Br J Sports Med 2017; 51: 700-701
33 Lombardo B, Izzo V, Terracciano D. et al. Laboratory medicine: health evaluation in elite athletes. Clin Chem Lab Med 2019; 57: 1450-1473
34 Mennitti C, Brancaccio M, Gentile L. et al. Athlete’s passport: prevention of infections, inflammations, injuries and cardiovascular diseases. J Clin Med 2020; 9: 2540
35 Pintus R, Bongiovanni T, Corbu S. et al. Sportomics in professional soccer players: metabolomics results during preseason. J Sports Med Phys Fitness 2021; 61: 324-330
36 Keohane DM, Woods T, O’Connor P. et al. Four men in a boat: ultra-endurance exercise alters the gut microbiome. J Sci Med Sport 2019; 22: 1059-1064
37 Orendurff MS, Walker JD, Jovanovic M. et al. Intensity and duration of intermittent exercise and recovery during a soccer match. J Strength Cond Res 2010; 24: 2683-2692
38 Biagi E, Mengucci C, Barone M. et al. Effects of vitamin B2 supplementation in broilers microbiota and metabolome. Microorganisms 2020; 8: 1134
39 Klindworth A, Pruesse E, Schweer T. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res 2013; 41: e1
40 Masella AP, Bartram AK, Truszkowski JM. et al. PANDAseq: Paired-end assembler for illumina sequences. BMC Bioinformatics 2012; 13: 31
41 Bolyen E, Rideout JR, Dillon MR. et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019; 37: 852-857
42 Callahan BJ, McMurdie PJ, Rosen MJ. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 2016; 13: 581-583
43 Rognes T, Flouri T, Nichols B. et al. VSEARCH: A versatile open source tool for metagenomics. PeerJ 2016; 4: e2584
44 Segata N, Izard J, Waldron L. et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011; 12: R60
45 Gould AL, Zhang V, Lamberti L. et al. Microbiome interactions shape host fitness. Proc Natl Acad Sci U S A 2018; 115: E11951-E11960
46 Keohane DM, Ghosh TS, Jeffery IB. et al. Microbiome and health implications for ethnic minorities after enforced lifestyle changes. Nat Med 2020; 26: 1089-1095
47 Motiani KK, Collado MC, Eskelinen JJ. et al. Exercise training modulates gut microbiota profile and improves endotoxemia. Med Sci Sports Exerc 2020; 52: 94-104
48 Ye M, Sun J, Chen Y. et al. Oatmeal induced gut microbiota alteration and its relationship with improved lipid profiles: A secondary analysis of a randomized clinical trial. Nutr Metab (Lond) 2020; 17: 85
49 Liu X, Mao B, Gu J. et al. Blautia — a new functional genus with potential probiotic properties?. Gut Microbes 2021; 13: 1-21
50 Wang P, Wang J, Li D. et al. Targeting the gut microbiota with resveratrol: a demonstration of novel evidence for the management of hepatic steatosis. J Nutr Biochem 2020; 81: 108363
51 Moorthy M, Sundralingam U, Palanisamy UD. Polyphenols as prebiotics in the management of high-fat diet-induced obesity: a systematic review of animal studies. Foods 2021; 10: 299
52 Amirkhanzadeh Barandouzi Z, Starkweather AR, Henderson WA. et al. Altered composition of gut microbiota in depression: a systematic review. Front Psychiatry 2020; 11: 541
53 Leylabadlo HE, Ghotaslou R, Feizabadi MM. et al. The critical role of Faecalibacterium prausnitzii in human health: an overview. Microb Pathog 2020; 149: 104344
54 Ferreira-Halder CV, Faria AV, de S, Andrade SS. Action and function of Faecalibacterium prausnitzii in health and disease. Best Pract Res Clin Gastroenterol 2017; 31: 643-648
55 Lopez-Siles M, Duncan SH, Garcia-Gil LJ. et al. Faecalibacterium prausnitzii: from microbiology to diagnostics and prognostics. ISME J 2017; 11: 841-852
56 Lordan C, Thapa D, Ross RP. et al. Potential for enriching next-generation health-promoting gut bacteria through prebiotics and other dietary components. Gut Microbes 2020; 11: 1-20
57 Cronin P, Joyce SA, O’toole PW. et al. Dietary fibre modulates the gut microbiota. Nutrients 2021; 13: 1655
58 Martín R, Bermúdez-Humarán LG, Langella P. Searching for the bacterial effector: the example of the multi-skilled commensal bacterium Faecalibacterium prausnitzii. Front Microbiol 2018; 9: 346
59 Marin IA, Goertz JE, Ren T. et al. Microbiota alteration is associated with the development of stress-induced despair behavior. Sci Rep 2017; 7: 43859
60 Galley JD, Nelson MC, Yu Z. et al. Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol 2014; 14: 189
61 Pillay L, Janse van Rensburg DCC, Jansen van Rensburg A. et al. Nowhere to hide: the significant impact of coronavirus disease 2019 (COVID-19) measures on elite and semi-elite South African athletes. J Sci Med Sport 2020; 23: 670-679
62 Jangi S, Gandhi R, Cox LM. et al. Alterations of the human gut microbiome in multiple sclerosis. Nat Commun 2016; 7: 12015
63 Ding HT, Taur Y, Walkup JT. Gut microbiota and autism: key concepts and findings. J Autism Dev Disord 2017; 47: 480-489
64 Bezawada N, Phang TH, Hold GL. et al. Autism spectrum disorder and the gut microbiota in children: a systematic review. Ann Nutr Metab 2020; 76: 16-29
65 Wang LJ, Yang CY, Chou WJ. et al. Gut microbiota and dietary patterns in children with attention-deficit/hyperactivity disorder. Eur Child Adolesc Psychiatry 2020; 29: 287-297
66 Castellanos N, Diez GG, Antúnez-Almagro C. et al. Key bacteria in the gut microbiota network for the transition between sedentary and active lifestyle. Microorganisms 2020; 8: 785
67 Mayengbam S, Lambert JE, Parnell JA. et al. Impact of dietary fiber supplementation on modulating microbiota-host-metabolic axes in obesity. J Nutr Biochem 2019; 64: 228-236
68 Yu D, Nguyen SM, Yang Y. et al. Long-term diet quality is associated with gut microbiome diversity and composition among urban Chinese adults. Am J Clin Nutr 2021; 113: 684-694
69 Finnicum CT, Beck JJ, Dolan CV. et al. Cohabitation is associated with a greater resemblance in gut microbiota which can impact cardiometabolic and inflammatory risk. BMC Microbiol 2019; 19: 230
70 Koo H, Hakim JA, Crossman DK. et al. Sharing of gut microbial strains between selected individual sets of twins cohabitating for decades. PLoS One 2019; 14: e0226111
71 Lautenbach F, Leisterer S, Walter N. et al. Amateur and recreational athletes’ motivation to exercise, stress, and coping during the Corona crisis. Front Psychol 2021; 11: 4032
72 Pété E, Leprince C, Lienhart N. et al. Dealing with the impact of the COVID-19 outbreak: are some athletes' coping profiles more adaptive than others?. Eur J Sport Sci 2022; 22: 237-247
73 Mueller-Wohlfahrt HW, Haensel L, Mithoefer K. et al. Terminology and classification of muscle injuries in sport: the Munich consensus statement. Br J Sports Med 2013; 47: 342-350
74 Mancin L, Rollo I, Mota JF. et al. Optimizing microbiota profiles for athletes. Exerc Sport Sci Rev 2021; 49: 42-49
75 Stølen T, Chamari K, Castagna C. et al. Physiology of soccer: an update. Sports Med 2005; 35: 501-536
76 Fédération Internationale de Football Association. FIFA Survey: approximately 250 million footballers worldwide. 2001 Available from http://www.fifa.com/aboutfifa/news/y=2001/m=4/news=fifa-survey-approximately-250-million-footballers-worldwide-88048.html
77 Fédération Internationale de Football Association. FIFA: Professional Football Report 2019 Available from https://digitalhub.fifa.com/m/a59132e138824c1c/original/jlr5corccbsef4n4brde.pdf

Supplementary Material

Supplementary Material