Download PDF
Planta Med 2022; 88(13): 1245-1255
DOI: 10.1055/a-1671-5766
Natural Product Chemistry and Analytical Studies
Original Papers

Evaluation of a Zingiber officinale and Bixa orellana Supplement on the Gut Microbiota of Male Athletes: A Randomized Placebo-Controlled Trial

Diego Domínguez-Balmaseda
1   Masmicrobiota Group, Faculty of Health Sciences, Universidad Europea de Madrid, Villaviciosa de Odón, Madrid, Spain
,
Carlo Bressa
1   Masmicrobiota Group, Faculty of Health Sciences, Universidad Europea de Madrid, Villaviciosa de Odón, Madrid, Spain
2   Biomedicine Department, Universidad Francisco de Vitoria, Pozuelo de Alarcón, Madrid, Spain
,
Arantxa Fernández-Romero
1   Masmicrobiota Group, Faculty of Health Sciences, Universidad Europea de Madrid, Villaviciosa de Odón, Madrid, Spain
,
Beatriz de Lucas
1   Masmicrobiota Group, Faculty of Health Sciences, Universidad Europea de Madrid, Villaviciosa de Odón, Madrid, Spain
,
Margarita Pérez-Ruiz
3   Research Group on Exercise, health and biomarkers applied, Faculty of Sport Sciences, Universidad Europea de Madrid, Villaviciosa de Odón, Madrid, Spain
,
Alejandro F. San Juan
4   Department of Health and Human Performance, Sport Biomechanics Laboratory, Faculty of Physical Activity and Sport Sciences, INEF, Universidad Politécnica de Madrid, Madrid, Spain
,
Marc Roller
5   Natural Origins, Lozanne, France
,
Nicolas Issaly
6   Nicolas Issaly, Valencia, Spain
,
Mar Larrosa 
1   Masmicrobiota Group, Faculty of Health Sciences, Universidad Europea de Madrid, Villaviciosa de Odón, Madrid, Spain
7   Department of Nutrition and Food Science, School of Pharmacy, Complutense University of Madrid (UCM), Madrid, Spain
› Author AffiliationsSupported by: Secretaría de Estado de Investigación, Desarrollo e Innovación AGL2016-77288-R
Supported by: European Social Fund through the Operational Program for Youth Employment and the Youth Employment Initiative of the Community of Madrid PEJ-2017-TL/SAL-6114
Supported by: European Social Fund through the Operational Program for Youth Employment and the Youth Employment Initiative of the Community of Madrid PEJD-2018-POST/SAL-8404
› Further Information
    Permissions and Reprints

Abstract

The gut microbiota has emerged as a factor that influences exercise performance and recovery. The present study aimed to test the effect of a polyherbal supplement containing ginger and annatto called “ReWin(d)” on the gut microbiota of recreational athletes in a pilot, randomized, triple-blind, placebo-controlled trial. Thirty-four participants who practice physical activity at least three times weekly were randomly allocated to two groups, a ReWin(d) group or a maltodextrin (placebo) group. We evaluated the gut microbiota, the production of short-chain fatty acids, and the serum levels of interleukin-6 and lipopolysaccharide at baseline and after 4 weeks. Results showed that ReWin(d) supplementation slightly increased gut microbiota diversity. Pairwise analysis revealed an increase in the relative abundance of Lachnospira (β-coefficient = 0.013; p = 0.001), Subdoligranulum (β-coefficient = 0.016; p = 0.016), Roseburia (β-coefficient = 0.019; p = 0.001), and Butyricicoccus (β-coefficient = 0.005; p = 0.035) genera in the ReWin(d) group, and a decrease in Lachnoclostridium (β-coefficient = − 0.008; p = 0.009) and the Christensenellaceae R7 group (β-coefficient = − 0.010; p < 0.001). Moreover, the Christensenellaceae R-7 group correlated positively with serum interleukin-6 (ρ = 0.4122; p = 0.032), whereas the Lachnospira genus correlated negatively with interleukin-6 (ρ = − 0.399; p = 0.032). ReWin(d) supplementation had no effect on short-chain fatty acid production or on interleukin-6 or lipopolysaccharide levels.

Key words

Zingiber officinale - Zingiberaceae - Bixa orellana - Bixaceae - gingerol - gut microbiota - alpha-diversity

Supporting Information

    Bacterial genera abundance distribution and distribution of the significantly different genera are available as Supporting Information.

  • Supporting Information


Publication History

Received: 17 June 2021

Accepted after revision: 14 October 2021

Article published online:
28 February 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Garthe I, Maughan RJ. Athletes and supplements: prevalence and perspectives. Int J Sport Nutr Exerc Metab 2018; 28: 126-138
    CrossrefPubMedGoogle Scholar
  • 2 Sellami M, Slimeni O, Pokrywka A, Kuvačić G, Hayes LD, Milic M, Padulo J. Herbal medicine for sports: A review. J Int Soc Sports Nutr 2018; 15: 14
    CrossrefPubMedGoogle Scholar
  • 3 Amico AP, Terlizzi A, Damiani S, Ranieri M, Megna M, Fiore P. Immunopharmacology of the main herbal supplements: A review. Endocr Metab Immune Disord Drug Targets 2013; 13: 283-288
    CrossrefPubMedGoogle Scholar
  • 4 Laparra JM, Sanz Y. Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacol Res 2010; 61: 219-225
    CrossrefPubMedGoogle Scholar
  • 5 Cerdá B, Tornero-Aguilera JF, Pérez M, Pérez-Santiago JD, Tornero-Aguilera JF, González-Soltero R, Larrosa M. Gut microbiota modification: another piece in the puzzle of the benefits of physical exercise in health?. Front Physiol 2016; 7: 51
    CrossrefPubMedGoogle Scholar
  • 6 Mach N, Fuster-Botella D. Endurance exercise and gut microbiota: A review. J Sport Heal Sci 2017; 6: 179-197
    CrossrefPubMedGoogle Scholar
  • 7 Wilson PB. Ginger (Zingiber officinale) as an analgesic and ergogenic aid in sport: A systemic review. J Strength Cond Res 2015; 29: 2980-2995
    CrossrefPubMedGoogle Scholar
  • 8 Lu QY, Summanen PH, Lee RP, Huang J, Henning SM, Heber D, Finegold SM, Li Z. Prebiotic potential and chemical composition of seven culinary spice extracts. J Food Sci 2017; 82: 1807-1813
    CrossrefPubMedGoogle Scholar
  • 9 Wang J, Wang P, Li D, Hu X, Chen F. Beneficial effects of ginger on prevention of obesity through modulation of gut microbiota in mice. Eur J Nutr 2020; 59: 699-718
    CrossrefPubMedGoogle Scholar
  • 10 Lyu Y, Wu L, Wang F, Shen X, Lin D. Carotenoid supplementation and retinoic acid in immunoglobulin A regulation of the gut microbiota dysbiosis. Exp Biol Med (Maywood) 2018; 243: 613-620
    CrossrefPubMedGoogle Scholar
  • 11 Vilar DA, Vilar MS, de Lima e Moura TF, Raffin FN, de Oliveira MR, Franco CF, de Athayde-Filho PF, Diniz MF, Barbosa-Filho JM. Traditional uses, chemical constituents, and biological activities of Bixa orellana L.: A review. Sci World J 2014; 2014: 857292
    CrossrefPubMedGoogle Scholar
  • 12 Shahid-ul-Islam. Rather LJ, Mohammad F. Phytochemistry, biological activities and potential of annatto in natural colorant production for industrial applications – a review. J Adv Res 2016; 7: 499-514
    CrossrefPubMedGoogle Scholar
  • 13 Galindo-Cuspinera V, Rankin SA. Bioautography and chemical characterization of antimicrobial compound(s) in commercial water-soluble annatto extracts. J Agric Food Chem 2005; 53: 2524-2529
    CrossrefPubMedGoogle Scholar
  • 14 Dominguez-Balmaseda D, Diez-Vega I, Larrosa M, San Juan AF, Issaly N, Moreno-Pérez D, Burgos S, Sillero-Quintana M, Gonzalez C, Bas A, Roller M, Pérez-Ruiz M. Effect of a blend of Zingiber officinale Roscoe and Bixa orellana L. herbal supplement on the recovery of delayed-onset muscle soreness induced by unaccustomed eccentric resistance training: a randomized, triple-blind, placebo-controlled trial. Front Physiol 2020; 11: 826
    CrossrefPubMedGoogle Scholar
  • 15 Donati Zeppa S, Agostini D, Gervasi M, Annibalini G, Amatori S, Ferrini F, Sisti D, Piccoli G, Barbieri E, Sestili P, Stocchi V. Mutual interactions among exercise, sport supplements and microbiota. Nutrients 2019; 12: 17
    CrossrefPubMedGoogle Scholar
  • 16 Bindels LB, Delzenne NM, Cani PD, Walter J. Towards a more comprehensive concept for prebiotics. Nat Rev Gastroenterol Hepatol 2015; 12: 303-310
    CrossrefPubMedGoogle Scholar
  • 17 Sonnenburg ED, Smits SA, Tikhonov M, Higginbottom SK, Wingreen NS, Sonnenburg JL. Diet-induced extinctions in the gut microbiota compound over generations. Nature 2016; 529: 212-215
    CrossrefPubMedGoogle Scholar
  • 18 De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 2010; 107: 14691-14696
    CrossrefPubMedGoogle Scholar
  • 19 Cardona F, Andrés-Lacueva C, Tulipani S, Tinahones FJ, Queipo-Ortuño MI. Benefits of polyphenols on gut microbiota and implications in human health. J Nutr Biochem 2013; 24: 1415-1422
    CrossrefPubMedGoogle Scholar
  • 20 Biswal P, Pal A, Das AP. Chapter 3: Current Trends and Future Prospective of Prebiotics as Therapeutic Food. In: Holban AM, Grumezescu AM. eds. Handbook of Food Bioengineering. Microbial Production of Food Ingredients and Additives. Academic Press. London: Elsevier; 2017: 57-88
    Google Scholar
  • 21 European Food Safety Agency. Technical report dietary reference values for nutrients summary report (2017). Accessed November 08, 2021 at: https://efsa.onlinelibrary.wiley.com/doi/pdf/10.2903/sp.efsa.2017.e15121
    PubMedGoogle Scholar
  • 22 Table M. Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids. Washington, DC, USA: National Academy Press; 2005
    Google Scholar
  • 23 Wang J, Chen Y, Hu X, Feng F, Cai L, Chen F. Assessing the effects of ginger extract on polyphenol profiles and the subsequent impact on the fecal microbiota by simulating digestion and fermentation in vitro . Nutrients 2020; 12: 3194
    CrossrefPubMedGoogle Scholar
  • 24 De Angelis M, Ferrocino I, Calabrese FM, De Filippis F, Cavallo N, Siragusa S, Rampelli S, Di Cagno R, Rantsiou K, Vannini L, Pellegrini N, Lazzi C, Turroni S, Lorusso N, Ventura M, Chieppa M, Neviani E, Brigidi P, OʼToole PW, Ercolini D, Gobbetti M, Cocolin L. Diet influences the functions of the human intestinal microbiome. Sci Rep 2020; 10: 4247
    CrossrefPubMedGoogle Scholar
  • 25 Chung E, Elmassry MM, Kottapalli P, Kottapalli KR, Kaur G, Dufour JM, Wright K, Ramalingam L, Moustaid-Moussa N, Wang R, Hamood AN, Shen CL. Metabolic benefits of annatto-extracted tocotrienol on glucose homeostasis, inflammation, and gut microbiome. Nutr Res 2020; 77: 97-107
    CrossrefPubMedGoogle Scholar
  • 26 Eeckhaut V, Machiels K, Perrier C, Romero C, Maes S, Flahou B, Steppe M, Haesebrouck F, Sas B, Ducatelle R, Vermeire S, Van Immerseel F. Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut 2013; 62: 1745-1752
    CrossrefPubMedGoogle Scholar
  • 27 Tung YT, Hsu YJ, Liao CC, Ho ST, Huang CC, Huang WC. Physiological and biochemical effects of intrinsically high and low exercise capacities through multiomics approaches. Front Physiol 2019; 10: 1201
    CrossrefPubMedGoogle Scholar
  • 28 Liu Y, Ajami NJ, El-Serag HB, Hair C, Graham DY, White DL, Chen L, Wang Z, Plew S, Kramer J, Cole R, Hernaez R, Hou J, Husain N, Jarbrink-Sehgal ME, Kanwal F, Ketwaroo G, Natarajan Y, Shah R, Velez M, Mallepally N, Petrosino JF, Jiao L. Dietary quality and the colonic mucosa-associated gut microbiome in humans. Am J Clin Nutr 2019; 110: 701-712
    CrossrefPubMedGoogle Scholar
  • 29 Zhu Q, Gao R, Zhang Y, Pan D, Zhu Y, Zhang X, Yang R, Jiang R, Xu Y, Qin H. Dysbiosis signatures of gut microbiota in coronary artery disease. Physiol Genomics 2018; 50: 893-903
    CrossrefPubMedGoogle Scholar
  • 30 Tan J, McKenzie C, Potamitis M, Thorburn AN, Mackay CR, Macia L. The role of short-chain fatty acids in health and disease. Adv Immunol 2014; 121: 91-119
    CrossrefPubMedGoogle Scholar
  • 31 Meehan CJ, Beiko RG. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol 2014; 6: 703-713
    CrossrefPubMedGoogle Scholar
  • 32 Waters JL, Ley RE. The human gut bacteria Christensenellaceae are widespread, heritable, and associated with health. BMC Biol 2019; 17: 1-11
    CrossrefPubMedGoogle Scholar
  • 33 Reihmane D, Dela F. Interleukin-6: possible biological roles during exercise. Eur J Sport Sci 2014; 14: 242-250
    CrossrefPubMedGoogle Scholar
  • 34 Ortiz-Alvarez L, Xu H, Martinez-Tellez B. Influence of exercise on the human gut microbiota of healthy adults: A systematic review. Clin Transl Gastroenterol 2020; 11: e00126
    CrossrefPubMedGoogle Scholar
  • 35 Clarke SF, Murphy EF, OʼSullivan O, Lucey AJ, Humphreys M, Hogan A, Hayes P, OʼReilly M, Jeffery IB, Wood-Martin R, Kerins DM, Quigley E, Ross RP, OʼToole PW, Molloy MG, Falvey E, Shanahan F, Cotter PD. Exercise and associated dietary extremes impact on gut microbial diversity. Gut 2014; 63: 1913-1920
    CrossrefPubMedGoogle Scholar
  • 36 Bressa C, Bailén-Andrino M, Pérez-Santiago J, González-Soltero R, Pérez M, Montalvo-Lominchar MG, Maté-Muñoz JL, Domínguez R, Moreno D, Larrosa M. Differences in gut microbiota profile between women with active lifestyle and sedentary women. PLoS One 2017; 12: e0171352
    CrossrefPubMedGoogle Scholar
  • 37 Whisner CM, Maldonado J, Dente B, Krajmalnik-Brown R, Bruening M. Diet, physical activity and screen time but not body mass index are associated with the gut microbiome of a diverse cohort of college students living in university housing: a cross-sectional study. BMC Microbiol 2018; 18: 210
    CrossrefPubMedGoogle Scholar
  • 38 Gagnier JJ, Boon H, Rochon P, Moher D, Barnes J, Bombardier C. CONSORT Group. Reporting randomized, controlled trials of herbal interventions: An elaborated CONSORT Statement. Ann Intern Med 2006; 144: 364-367
    CrossrefPubMedGoogle Scholar
  • 39 Wilson PB. Ginger (Zingiber officinale) as an analgesic and ergogenic aid in sport: a systemic review. J Strength Cond Res 2015; 29: 2980-2995
    CrossrefPubMedGoogle Scholar
  • 40 González-Sarrías A, Romo-Vaquero M, García-Villalba R, Cortés-Martín A, Selma MV, Espín JC. The endotoxemia marker lipopolysaccharide-binding protein is reduced in overweight-obese subjects consuming pomegranate extract by modulating the gut microbiota: A randomized clinical trial. Mol Nutr Food Res 2018; 62: e1800160
    CrossrefPubMedGoogle Scholar
  • 41 Molan AL, Liu Z, Plimmer G. Evaluation of the effect of blackcurrant products on gut microbiota and on markers of risk for colon cancer in humans. Phyther Res 2013; 28: 416-422
    CrossrefPubMedGoogle Scholar
  • 42 Vioque J, Quiles J. Encuesta de Nutrición y Salud de la Comunidad Valenciana. Alicante: Departamento Salud Pública; 2003
    Google Scholar
  • 43 Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson 2nd MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019; 37: 852-857
    CrossrefPubMedGoogle Scholar
  • 44 García-Villalba R, Giménez-Bastida JA, García-Conesa MT, Tomás-Barberán FA, Espín JC, Larrosa M. Alternative method for gas chromatography-mass spectrometry analysis of short-chain fatty acids in faecal samples. J Sep Sci 2012; 35: 1906-1913
    CrossrefPubMedGoogle Scholar
  • 45 Bokulich NA, Dillon MR, Zhang Y, Rideout JR, Bolyen E, Li H, Albert PS, Caporaso JG. q2-longitudinal: Longitudinal and paired-sample analyses of microbiome data. mSystems 2018; 3: 1-9
    CrossrefPubMedGoogle Scholar