Journal of Eexercise & Organ Cross Talk

Gut-muscle crosstalk: The effect of endurance training and probiotic supplementation on intestinal villus structure, postbiotics and VO2max in old male rats

Document Type : Original Article

Authors

Department of Exercise Physiology, Faculty of Sport Sciences, University of Guilan, Rasht, Guilan, Iran.

Abstract
The aim of this study was the effect of endurance exercise and probiotic supplement enriched with amino acid leucine and vitamin D on the gut-muscle axis in aged male rats. For this purpose, 25 male Wistar rats (5 rats in each group) in two age groups of 8 to 12 weeks (young) and 18 to 24 months (elderly) were randomly divided into 5 equal groups of old control (OC), young control (YC), endurance exercise (OE), supplement group (OS) and endurance exercise plus supplement (OES) were divided. The results showed that 8 weeks of endurance training (three times a week) and supplemental oral gavage (5 times a week) caused a significant change in postbiotics (decrease of indoxyl sulfate (IXS) and increase of Short-chain fatty acids (SCFAs)). The role of OS in reducing IXS was more prominent than OE and OES variables; of course, the synergistic effect of OES (P=0.000), caused a greater improvement in the amount of SCFA. Also, Administering the supplement alone and at rest (without exercise) could not cause a significant increase in VO2max (P=0.449). But, the effect of exercise on increasing VO2max index was more effective than OS and even OES. Eventually, the independent variables made a significant difference on the Villus height (VH) (except for the OS group) and number of goblet cells (GC) compared to the OC group (P<0.05).

What is already known on this subject?

Aging can cause inflammation by affecting gut function and gut microbiota composition, thereby leading to muscle dysfunction. Gut microbiota metabolites are key mediators influencing the gut-muscle axis. Probiotics, vitamin D, leucine amino acid and Endurance exercise, through changes in the intestinal microbiota, improving the intestinal epithelial barrier, inhibiting oxidative stress and reducing ROS production, lead to increasing the production of positive intestinal metabolites (SCFAs), reducing negative metabolites (IXS and LPS) and improve chronic and systemic inflammation, which will ultimately improve mitochondrial function and endurance exercise.

 

What this study adds?

The effect of OS in negative intestinal metabolites (IXS) was more effective than OE and OES; So that there was no significant difference with the OY control group.

The synergistic effect of OES in increasing positive intestinal metabolites (SCFAs), improving intestinal structure (GC and VH) was more effective than the separate effect of OS and OE; So that there was no significant difference with the OY control group.

The effect of exercise on increasing Vo2max index was more effective than OS and even OES; So that there was no significant difference with the OY control group.

Administering the supplement alone and at rest (without exercise) could not cause a significant increase in VO2max.

 

What this study adds?

The effect of OS in negative intestinal metabolites (IXS) was more effective than OE and OES; So that there was no significant difference with the OY control group.

The synergistic effect of OES in increasing positive intestinal metabolites (SCFAs), improving intestinal structure (GC and VH) was more effective than the separate effect of OS and OE; So that there was no significant difference with the OY control group.

The effect of exercise on increasing Vo2max index was more effective than OS and even OES; So that there was no significant difference with the OY control group.

Administering the supplement alone and at rest (without exercise) could not cause a significant increase in Vo2max.

Keywords

Subjects


Acknowledgements

The authors are grateful for the support and participation of the “Gene and Tissue Laboratory of Pasargad” during the laboratory stages.

Funding

None.

Compliance with ethical standards

The authors declare that they have no conflict of interest.

Ethical approval Animals had free access to standard food and water. All stages of keeping and slaughtering rats were carried out according to the rules of the Animal Ethics Committee of Guilan University, rasht, Guilan, Iran (ethical code: IR.GUILAN.REC.1402.085).

Informed consent Animal study.

Author contributions

Conceptualization: B.M., J.M., L.L.; Methodology: B.M., J.M., L.L.; Software: L.L.; Validation: L.L., Formal analysis; Investigation: B.M., J.M., L.L.; Resources: B.M., J.M.; Data curation: B.M., J.M., L.L.; Writing - original draft: L.L.; Writing – review & editing: B.M., J.M.; Visualization: L.L., B.M., J.M.; Supervision: B.M., J.M. Project administration: L.L.; Funding acquisition: B.M., J.M.

Abdul Kadir, N. A. A., Rahmat, A., & Jaafar, H. Z. (2015). Protective Effects of Tamarillo (Cyphomandra betacea) extract against High Fat Diet Induced Obesity in Sprague‐Dawley Rats. Journal of obesity, 2015(1), 846041. https:// doi. org/10.1155/ 2015/84604 1 (2015). https://doi.org/10.1155/2015/846041.
Bass, J. J., Nakhuda, A., Deane, C. S., Brook, M. S., Wilkinson, D. J., Phillips, B. E., ... & Atherton, P. J. (2020). Overexpression of the vitamin D receptor (VDR) induces skeletal muscle hypertrophy. Molecular metabolism, 42, 101059. https://doi.org/10.1016/j.molmet.2020.101059.
Bertuccioli, A., Zonzini, G. B., Cazzaniga, M., Cardinali, M., Di Pierro, F., Gregoretti, A., ... & Palazzi, C. M. (2024). Sports-Related Gastrointestinal Disorders: From the Microbiota to the Possible Role of Nutraceuticals, a Narrative Analysis. Microorganisms, 12(4), 804. https://doi.org/10.3390/microorganisms12040804.
Bilski, J., Pierzchalski, P., Szczepanik, M., Bonior, J., & Zoladz, J. A. (2022). Multifactorial mechanism of sarcopenia and sarcopenic obesity. Role of physical exercise, microbiota and myokines. Cells, 11(01), 160. https://doi.org/10.3390/cells11010160.
Boisseau, N., Barnich, N., & Koechlin-Ramonatxo, C. (2022). The nutrition-microbiota-physical activity triad: an inspiring new concept for health and sports performance. Nutrients, 14(5), 924. https://doi.org/10.3390/nu14050924.
Brzeziański, M., Migdalska-Sęk, M., Czechowska, A., Radzimiński, Ł., Jastrzębski, Z., Brzeziańska-Lasota, E., & Sewerynek, E. (2022). Correlation between the positive effect of vitamin D supplementation and physical performance in young male soccer players. International journal of environmental research and public health, 19(9), 5138. https://doi.org/10.3390/ijerph19095138.
Cataldi, S., Poli, L., Şahin, F. N., Patti, A., Santacroce, L., Bianco, A., ... & Fischetti, F. (2022). The effects of physical activity on the gut microbiota and the gut–brain axis in preclinical and human models: a narrative review. Nutrients, 14(16), 3293. https://doi.org/10.3390/nu14163293.
Caudal, D., Guinobert, I., Lafoux, A., Bardot, V., Cotte, C., Ripoche, I., & Huchet, C. (2018). Skeletal muscle relaxant effect of a standardized extract of Valeriana officinalis L. after acute administration in mice. Journal of traditional and complementary medicine, 8(2), 335-340. https://doi.org/10.1016/j.jtcme.2017.06.011.
Chaiyasut, C., Sivamaruthi, B. S., Lailerd, N., Sirilun, S., Khongtan, S., Fukngoen, P., & Sittiprapaporn, P. (2022). Probiotics supplementation improves intestinal permeability, obesity index and metabolic biomarkers in elderly Thai subjects: a randomized controlled trial. Foods, 11(3), 268. https://doi.org/10.3390/foods11030268.
Chen, L. H., Wang, M. F., Chang, C. C., Huang, S. Y., Pan, C. H., Yeh, Y. T., ... & Huang, H. Y. (2021). Lacticaseibacillus paracasei PS23 effectively modulates gut microbiota composition and improves gastrointestinal function in aged SAMP8 mice. Nutrients, 13(4), 1116. https://doi.org/10.3390/nu13041116.
Chinnappa, S., Tu, Y. K., Yeh, Y. C., Glorieux, G., Vanholder, R., & Mooney, A. (2018). Association between protein-bound uremic toxins and asymptomatic cardiac dysfunction in patients with chronic kidney disease. Toxins, 10(12), 520. https://doi.org/10.3390/toxins10120520.
de Marco Castro, E., Murphy, C. H., & Roche, H. M. (2021). Targeting the gut microbiota to improve dietary protein efficacy to mitigate sarcopenia. Frontiers in Nutrition, 8, 656730. https://doi.org/10.3389/fnut.2021.656730.
Díaz-Jiménez, J., Sánchez-Sánchez, E., Ordoñez, F. J., Rosety, I., Díaz, A. J., Rosety-Rodriguez, M., & Brenes, F. (2021). Impact of probiotics on the performance of endurance athletes: A systematic review. International Journal of Environmental Research and Public Health, 18(21), 11576. https://doi.org/10.3390/ijerph182111576.
Domínguez-Balmaseda, D., & García-Pérez-de-Sevilla, G. (2022). The Relationship between the Gut Microbiota and Exercise: A Narrative Review. Hygiene, 2(4), 152-162. https://doi.org/10.3390/hygiene2040014.
Dos Santos, G. B., de Oliveira, A. G., Ramos, L. A. F., Gomes‐Marcondes, M. C. C., & Areas, M. A. (2016). Long‐term leucine supplementation aggravates prolonged strenuous exercise‐induced cardiovascular changes in trained rats. Experimental physiology, 101(7), 811-820. https://doi.org/10.1113/EP085704.
Drozdowski, L., & Thomson, A. B. (2006). Aging and the intestine. World journal of gastroenterology: WJG, 12(47), 7578. doi: https://doi.org/10.3748/wjg.v12.i47.7578.
Ducray, H. A. G., Globa, L., Pustovyy, O., Roberts, M. D., Rudisill, M., Vodyanoy, V., & Sorokulova, I. (2020). Prevention of excessive exercise‐induced adverse effects in rats with Bacillus subtilis BSB3. Journal of Applied Microbiology, 128(4), 1163-1178. https://doi.org/10.1111/jam.14544.
Durk, R. P., Castillo, E., Márquez-Magaña, L., Grosicki, G. J., Bolter, N. D., Lee, C. M., & Bagley, J. R. (2019). Gut microbiota composition is related to cardiorespiratory fitness in healthy young adults. International journal of sport nutrition and exercise metabolism, 29(3), 249-253. DOI: https://doi.org/10.1123/ijsnem.2018-0024.
Endres, K., & Friedland, K. (2023). Talk to Me—Interplay between Mitochondria and Microbiota in Aging. International journal of molecular sciences, 24(13), 10818. 10.3390/ijms241310818. https://doi.org/10.3390/ijms241310818.
Fang, W. Y., Lin, C. L., Chang, W. H., Chang, C. H., Huang, Y. C., Tsai, Y. H., ... & Lo, Y. C. (2022). Protective Effects of the Chalcone-Based Derivative AN07 on Inflammation-Associated Myotube Atrophy Induced by Lipopolysaccharide. International Journal of Molecular Sciences, 23(21), 12929. https://doi.org/10.3390/ijms232112929.
Fusco, W., Lorenzo, M. B., Cintoni, M., Porcari, S., Rinninella, E., Kaitsas, F., ... & Ianiro, G. (2023). Short-chain fatty-acid-producing bacteria: key components of the human gut microbiota. Nutrients, 15(9), 2211. https://doi.org/10.3390/nu15092211.
Gao, Z., Yin, J., Zhang, J., Ward, R. E., Martin, R. J., Lefevre, M., ... & Ye, J. (2009). Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes, 58(7), 1509-1517. https://doi.org/10.2337/db08-1637
Ghaffar, T., Ubaldi, F., Volpini, V., Valeriani, F., & Romano Spica, V. (2024). The Role of Gut Microbiota in Different Types of Physical Activity and Their Intensity: Systematic Review and Meta-Analysis. Sports, 12(8), 221. https://doi.org/10.3390/sports12080221
Gregory, S. M., Parker, B. A., Capizzi, J. A., Grimaldi, A. S., Clarkson, P. M., Moeckel-Cole, S., ... & Thompson, P. D. (2013). Changes in vitamin D are not associated with changes in cardiorespiratory fitness. Age (years), 44, 16-4. doi: https://doi.org/10.11648/j.cmr.20130204.16.
Guimarães, A. G., Lopes, L. E., Capelassi, A. N., Araújo, A. C., Balbo, S. L., Blanc, H. N., ... & Bonfleur, M. L. (2021). Morphological alterations in gastrointestinal organs of western-diet obese rats submitted to vertical sleeve gastrectomy or Roux-en-Y gastric bypass. Anais da Academia Brasileira de Ciências, 93(4), e20200884. https://doi.org/10.1590/0001-3765202120200884.
Han, H., You, Y., Cha, S., Kim, T. R., Sohn, M., & Park, J. (2023). Multi-species probiotic strain mixture enhances intestinal barrier function by regulating inflammation and tight junctions in lipopolysaccharides stimulated caco-2 cells. Microorganisms, 11(3), 656. https://doi.org/10.3390/microorganisms11030656.
Hijová, E. (2023). Benefits of biotics for cardiovascular diseases. International Journal of Molecular Sciences, 24(7), 6292. https://doi.org/10.3390/sports12080221.
Huang, W. C., Hsu, Y. J., Huang, C. C., Liu, H. C., & Lee, M. C. (2020). Exercise training combined with Bifidobacterium longum OLP-01 supplementation improves exercise physiological adaption and performance. Nutrients, 12(4), 1145. https://doi.org/10.3390/nu12041145.
Huang, W. C., Lee, M. C., Lee, C. C., Ng, K. S., Hsu, Y. J., Tsai, T. Y., ... & Huang, C. C. (2019). Effect of Lactobacillus plantarum TWK10 on exercise physiological adaptation, performance, and body composition in healthy humans. Nutrients, 11(11), 2836. https://doi.org/10.3390/nu11112836.
Huang, W. C., Lee, M. C., Lee, C. C., Ng, K. S., Hsu, Y. J., Tsai, T. Y., ... & Huang, C. C. (2019). Effect of Lactobacillus plantarum TWK10 on exercise physiological adaptation, performance, and body composition in healthy humans. Nutrients, 11(11), 2836. 2836; https://doi.org/10.3390/nu11112836.
Huang, W. C., Pan, C. H., Wei, C. C., & Huang, H. Y. (2020). Lactobacillus plantarum PS128 improves physiological adaptation and performance in triathletes through gut microbiota modulation. Nutrients, 12(8), 2315. https://doi.org/10.3390/nu12082315.
Hussein, E. O., Ahmed, S. H., Abudabos, A. M., Aljumaah, M. R., Alkhlulaifi, M. M., Nassan, M. A., ... & Swelum, A. A. (2020). Effect of antibiotic, phytobiotic and probiotic supplementation on growth, blood indices and intestine health in broiler chicks challenged with Clostridium perfringens. Animals, 10(3), 507. https://doi.org/10.3390/ani10030507.
Iolascon, G., Moretti, A., Paoletta, M., Liguori, S., & Di Munno, O. (2021). Muscle regeneration and function in sports: a focus on vitamin D. Medicina, 57(10), 1015. https://doi.org/10.3390/medicina57101015
Iyer, N., & Corr, S. C. (2021). Gut microbial metabolite-mediated regulation of the intestinal barrier in the pathogenesis of inflammatory bowel disease. Nutrients, 13(12), 4259. https://doi.org/10.3390/nu13124259.
Kerksick, C. M., Moon, J. M., & Jäger, R. (2024). It’s Dead! Can Postbiotics Really Help Performance and Recovery? A Systematic Review. Nutrients, 16(5), 720. https://doi.org/10.3390/nu16050720.
Khailova, L., Dvorak, K., Arganbright, K. M., Halpern, M. D., Kinouchi, T., Yajima, M., & Dvorak, B. (2009). Bifidobacterium bifidum improves intestinal integrity in a rat model of necrotizing enterocolitis. American Journal of Physiology-Gastrointestinal and Liver Physiology, 297(5), G940-G949. https://doi.org/10.1152/ajpgi.00141.2009.
Kim, C. H., Wheatley, C. M., Behnia, M., & Johnson, B. D. (2016). The effect of aging on relationships between lean body mass and VO2max in rowers. PloS one, 11(8), e0160275. https://doi.org/10.1371/journal.pone.0160275.
Łagowska, K., Bajerska, J., Kamiński, S., & Del Bo’, C. (2022). Effects of probiotics supplementation on gastrointestinal symptoms in athletes: A systematic review of randomized controlled trials. Nutrients, 14(13), 2645. https://doi.org/10.3390/nu14132645.
Le Couteur, D. G., & Thillainadesan, J. (2022). What is an aging-related disease? An epidemiological perspective. The Journals of Gerontology: Series A, 77(11), 2168-2174. https://doi.org/10.1093/gerona/glac039.
Lee, M. C., Hsu, Y. J., Ho, C. S., Tsai, Y. S., Chen, C. C., & Huang, C. C. (2024). Supplementation with Lactiplantibacillus brevis GKEX Combined with Resistance Exercise Training Improves Muscle Mass, Strength Performance, and Body Fat Condition in Healthy Humans. Foods, 13(7), 1030. https://doi.org/10.3390/foods13071030.
Lee, M. C., Hsu, Y. J., Ho, H. H., Hsieh, S. H., Kuo, Y. W., Sung, H. C., & Huang, C. C. (2020). Lactobacillus salivarius subspecies salicinius SA-03 is a new probiotic capable of enhancing exercise performance and decreasing fatigue. Microorganisms, 8(4), 545. https://doi.org/10.3390/microorganisms8040545.
Lee, M. C., Tu, Y. T., Lee, C. C., Tsai, S. C., Hsu, H. Y., Tsai, T. Y., ... & Huang, C. C. (2021). Lactobacillus plantarum TWK10 improves muscle mass and functional performance in frail older adults: A randomized, double-blind clinical trial. Microorganisms, 9(7), 1466. https://doi.org/10.3390/microorganisms9071466.
Li, T., Rui, Z., Mao, L., Chang, Y., Shao, J., Chen, Y., & Wang, Q. (2023). Eight Weeks of Bifidobacterium lactis BL-99 Supplementation Improves Lipid Metabolism and Sports Performance through Short-Chain Fatty Acids in Cross-Country Skiers: A Preliminary Study. Nutrients, 15(21), 4554. https://doi.org/10.3390/nu15214554
Liu, S., Xiao, G., Wang, Q., Zhang, Q., Tian, J., Li, W., & Gong, L. (2023). Effects of dietary bacillus subtilis hc6 on growth performance, antioxidant capacity, immunity, and intestinal health in broilers. Animals, 13(18), 2915. https://doi.org/10.3390/ani13182915.
Lustgarten, M. S. (2019). The kidney–gut–muscle axis in end-stage renal disease is similarly represented in older adults. Nutrients, 12(1), 106. https://doi.org/10.3390/nu12010106.
Martínez-Arnau, F. M., Fonfría-Vivas, R., Buigues, C., Castillo, Y., Molina, P., Hoogland, A. J., & Cauli, O. (2020). Effects of leucine administration in sarcopenia: a randomized and placebo-controlled clinical trial. Nutrients, 12(4), 932. https://doi.org/10.3390/nu12040932.
Michalczyk, M. M., Gołaś, A., Maszczyk, A., Kaczka, P., & Zając, A. (2020). Influence of sunlight and oral D3 supplementation on serum 25 (OH) D concentration and exercise performance in elite soccer players. Nutrients, 12(5), 1311. https://doi.org/10.3390/nu12051311.
Miles, M. P., Wilson, S., & Yeoman, C. J. (2019). Physical activity and inflammation phenotype conversion. Journal of Clinical Exercise Physiology, 8(2), 64-73. https://doi.org/10.31189/2165-6193-8.2.64.
Mokarrami, A., Capacci, A., Trio, B., Della Morte Canosci, D., & Merra, G. (2024). Relationship between Gut-Microbiota and Sport Activity. Central European Journal of Sport Sciences and Medicine, 45, 25-53. DOI: https://doi.org/10.18276/cej.2024.1-03.
Nardone, O. M., de Sire, R., Petito, V., Testa, A., Villani, G., Scaldaferri, F., & Castiglione, F. (2021). Inflammatory bowel diseases and sarcopenia: the role of inflammation and gut microbiota in the development of muscle failure. Frontiers in Immunology, 12, 694217. https://doi.org/10.3389/fimmu.2021.694217.
Nicastro, H., Zanchi, N. E., da Luz, C. R., de Moraes, W. M., Ramona, P., de Siqueira Filho, M. A., ... & Lancha Jr, A. H. (2012). Effects of leucine supplementation and resistance exercise on dexamethasone-induced muscle atrophy and insulin resistance in rats. Nutrition, 28(4), 465-471. doi: https://doi.org/10.1016/j.nut.2011.08.008.
Ofori-Attah, E., Hashimoto, M., Oki, M., & Kadowaki, D. (2024). Therapeutic Effect of Natural Products and Dietary Supplements on Aflatoxin-Induced Nephropathy. International Journal of Molecular Sciences, 25(5), 2849. https://doi.org/10.3390/ijms25052849.
Olteanu, G., Ciucă-Pană, M. A., Busnatu, Ș. S., Lupuliasa, D., Neacșu, S. M., Mititelu, M., ... & Boroghină, S. C. (2024). Unraveling the Microbiome–Human Body Axis: A Comprehensive Examination of Therapeutic Strategies, Interactions and Implications. International Journal of Molecular Sciences, 25(10), 5561. https://doi.org/10.3390/ijms25105561.
Peng, K., Dong, W., Luo, T., Tang, H., Zhu, W., Huang, Y., & Yang, X. (2023). Butyrate and obesity: Current research status and future prospect. Frontiers in Endocrinology, 14, 1098881. https://doi.org/10.3389/fendo.2023.1098881.
Przewłócka, K., Folwarski, M., Kaźmierczak-Siedlecka, K., Skonieczna-Żydecka, K., & Kaczor, J. J. (2020). Gut-muscle axis exists and may affect skeletal muscle adaptation to training. Nutrients, 12(5), 1451. https://doi.org/10.3390/nu12051451.
Qaisrani, S. N., Hussain, A. I., Naveed, S., Bibi, F., Akram, C. A., Pasha, T. N., ... & Bilal, R. M. (2022). Effects of protein source, whole wheat and butyric acid on live performance, gut health and amino acid digestibility in broiler chickens. Metabolites, 12(10), 989. https://doi.org/10.3390/metabo12100989.
Qin, F., Dong, Y., Wang, S., Xu, M., Wang, Z., Qu, C., & Zhao, J. (2020). Maximum oxygen consumption and quantification of exercise intensity in untrained male Wistar rats. Scientific Reports, 10(1), 11520. https://doi.org/10.1038/s41598-020-68455-8.
Salarkia, N., Ghadamli, L., Zaeri, F., & Rad, L. S. (2013). Effects of probiotic yogurt on performance, respiratory and digestive systems of young adult female endurance swimmers: a randomized controlled trial. Medical Journal of the Islamic Republic of Iran, 27(3), 141. PMC3917487.
Salleh, R. M., Kuan, G., Aziz, M. N. A., Rahim, M. R. A., Rahayu, T., Sulaiman, S., ... & Appukutty, M. (2021). Effects of probiotics on anxiety, stress, mood and fitness of badminton players. Nutrients, 13(6), 1783. https://doi.org/10.3390/nu13061783.
Santibañez-Gutierrez, A., Fernández-Landa, J., Calleja-González, J., Delextrat, A., & Mielgo-Ayuso, J. (2022). Effects of probiotic supplementation on exercise with predominance of aerobic metabolism in trained population: A systematic review, meta-analysis and meta-regression. Nutrients, 14(3), 622. https://doi.org/10.3390/nu14030622.
Santilli, V., Bernetti, A., Mangone, M., & Paoloni, M. (2014). Clinical definition of sarcopenia. Clinical cases in mineral and bone metabolism, 11(3), 177. https://hdl.handle.net/11573/768514.
Savolainen, L., Timpmann, S., Mooses, M., Medijainen, L., Tõnutare, L., Ross, F., & Ööpik, V. (2022). Vitamin D Supplementation Has No Impact on Cardiorespiratory Fitness, but Improves Inflammatory Status in Vitamin D Deficient Young Men Engaged in Resistance Training. Nutrients, 14(24), 5302. https://doi.org/10.3390/nu14245302
Schilderink, R., Verseijden, C., & de Jonge, W. J. (2013). Dietary inhibitors of histone deacetylases in intestinal immunity and homeostasis. Frontiers in immunology, 4, 226. https://doi.org/10.3389/fimmu.2013.00226.
Schulze, A., & Busse, M. (2024). Sports diet and oral health in athletes: A comprehensive review. Medicina, 60(2), 319. https://doi.org/10.3390/medicina60020319.
Shah, A. M., Cai, Y., Zou, H., Zhang, X., Wang, L., Xue, B., ... & Peng, Q. (2019). Effects of supplementation of branches and leaves trimmed from tea plant on growth performance, rumen fermentation and meat composition of Nanjiang yellow goats. Animals, 9(9), 590. https://doi.org/10.3390/ani9090590
Smarkusz-Zarzecka, J., Ostrowska, L., Leszczyńska, J., Orywal, K., Cwalina, U., & Pogodziński, D. (2020). Analysis of the impact of a multi-strain probiotic on body composition and cardiorespiratory fitness in long-distance runners. Nutrients, 12(12), 3758. https://doi.org/10.3390/nu12123758
Smith, K. S., Morris, M. M., Morrow, C. D., Novak, J. R., Roberts, M. D., & Frugé, A. D. (2022). Associations between changes in fat-free mass, fecal microbe diversity, and mood disturbance in young adults after 10-weeks of resistance training. Microorganisms, 10(12), 2344. https://doi.org/10.3390/microorganisms10122344.
Soares, A. D. N., Wanner, S. P., Morais, E. S. S., Hudson, A. S. R., Martins, F. S., & Cardoso, V. N. (2019). Supplementation with Saccharomyces boulardii increases the maximal oxygen consumption and maximal aerobic speed attained by rats subjected to an incremental-speed exercise. Nutrients, 11(10), 2352. https://doi.org/10.3390/nu11102352.
Threadgold, T., Greenwood, E. C., & Van Wettere, W. (2021). Identifying suitable supplements to improve piglet survival during farrowing and lactation. Animals, 11(10), 2912. https://doi.org/10.3390/ani11102912.
Tieland, M., Trouwborst, I., & Clark, B. C. (2018). Skeletal muscle performance and ageing. Journal of cachexia, sarcopenia and muscle, 9(1), 3-19. https://doi.org/10.1002/jcsm.12238.
Toda, K., Yamauchi, Y., Tanaka, A., Kuhara, T., Odamaki, T., Yoshimoto, S., & Xiao, J. Z. (2020). Heat-killed bifidobacterium breve B-3 Enhances Muscle Functions: Possible involvement of increases in muscle mass and mitochondrial biogenesis. Nutrients, 12(1), 219. https://doi.org/10.3390/nu12010219.
Van Krimpen, S. J., Jansen, F. A., Ottenheim, V. L., Belzer, C., van Der Ende, M., & van Norren, K. (2021). The effects of pro-, pre-, and synbiotics on muscle wasting, a systematic review—Gut permeability as potential treatment target. Nutrients, 13(4), 1115. https://doi.org/10.3390/nu13041115.
Wang, H., Sun, Y., Xin, J., Zhang, T., Sun, N., Ni, X., & Bai, Y. (2020). Lactobacillus johnsonii BS15 prevents psychological stress–induced memory dysfunction in mice by modulating the gut–brain axis. Frontiers in Microbiology, 11, 1941. https://doi.org/10.3389/fmicb.2020.01941.
Waskiw-Ford, M., Hannaian, S., Duncan, J., Kato, H., Abou Sawan, S., Locke, M., & Moore, D. (2020). Leucine-enriched essential amino acids improve recovery from post-exercise muscle damage independent of increases in integrated myofibrillar protein synthesis in young men. Nutrients, 12(4), 1061. https://doi.org/10.3390/nu12041061.
Wu, G., Tawfeeq, H. R., Lackey, A. I., Zhou, Y., Sifnakis, Z., Zacharisen, S. M., ... & Storch, J. (2022). Gut microbiota and phenotypic changes induced by ablation of liver-and intestinal-type fatty acid-binding proteins. Nutrients, 14(9), 1762. https://doi.org/10.3390/nu14091762.
Yosi, F., & Metzler-Zebeli, B. U. (2023). Dietary Probiotics Modulate Gut Barrier and Immune-Related Gene Expression and Histomorphology in Broiler Chickens under Non-and Pathogen-Challenged Conditions: A Meta-Analysis. Animals, 13(12), 1970. https://doi.org/10.3390/ani13121970.
Yun, E. J., Imdad, S., Jang, J., Park, J., So, B., Kim, J. H., & Kang, C. (2022). Diet is a stronger covariate than exercise in determining gut microbial richness and diversity. Nutrients, 14(12), 2507. https://doi.org/10.3390/nu14122507.
Zhang, L., Liu, Y., Sun, Y., & Zhang, X. (2022). Combined physical exercise and diet: regulation of gut microbiota to prevent and treat of metabolic disease: a review. Nutrients, 14(22), 4774. https://doi.org/10.3390/nu14224774.
Zhang, L., Xiao, H., Zhao, L., Liu, Z., Chen, L., & Liu, C. (2023). Comparison of the effects of prebiotics and synbiotics supplementation on the immune function of male university football players. Nutrients, 15(5), 1158. https://doi.org/10.3390/nu15051158.
Zhou, H., Sun, J., Ge, L., Liu, Z., Chen, H., Yu, B., & Chen, D. (2020). Exogenous infusion of short-chain fatty acids can improve intestinal functions independently of the gut microbiota. Journal of animal science, 98(12), skaa371. https://doi.org/10.1093/jas/skaa371.
Zou, Y., Wang, J., Wang, Y., Peng, B., Liu, J., Zhang, B., ... & Wang, S. (2020). Protection of galacto-oligosaccharide against E. coli O157 colonization through enhancing gut barrier function and modulating gut microbiota. Foods, 9(11), 1710. https://doi.org/10.3390/foods9111710.
Volume 4, Issue 2
Spring 2024
Pages 86-98

  • Receive Date 25 March 2024
  • Revise Date 02 June 2024
  • Accept Date 08 June 2024