Assessment of Saccharomyces boulardii CNCM I-745-supplemented probiotic and synbiotic ice cream in mitigating trinitrobenzene sulfonic acid-induced colitis in rats
Main Article Content
Keywords
colitic albino rats; Saccharomyces boulardii CNCM I-745; synbiotic ice cream; tumor necrosis factor-alpha (TNF-α); TNBS
Abstract
Inflammatory bowel disease (IBD) refers to a pair of disorders, namely Crohn’s disease and ulcerative colitis (UC), which are distinguished by persistent gastrointestinal (GI) tract inflammation. Common manifestations include fever and inflammation of the colon, resulting in decreased absorption of nutrition and weight loss. The occur-rence of UC can be decreased by modulating the immune system via gut microflora with probiotics and prebiotics. This study aimed to create a rat model of colitis by utilizing trinitrobenzene sulfonic acid (TNBS) and to correlate intestinal anti-inflammatory activity, physical effects, and hepatoprotective properties of functional probiotic and synbiotic ice cream. In this study, probiotic, S. boulardii CNCM I-745, and prebiotic, inulin, which are proved to have beneficial effects on the gut, were used in the formulation of ice cream. The ice cream was then given to albino rats with TNBS-induced colitis. The effect of ice cream, which was based on probiotics and synbiotics, was assessed by comparing it with negative control and colitic mice. The evaluation focused on the effect of ice cream on physical and inflammatory indicators. Three treatment groups were administered probiotic and synbiotic ice cream based on their weight for a duration of 2 weeks. Prior to this, colitis was induced using TNBS. After consuming several functional ice cream formulations for 2 weeks, the levels of inflammatory markers, such as tumor necrosis factor-alpha and interleukin-6, exhibited a noticeable decline, indicating reduced inflammation. The ingestion of probiotic and synbiotic ice cream also led to enhanced weight gain. The serum levels of aspartate aminotransferase, alanine aminotransferase, and alkaline phosphatase, which are parameters for assessing hepatoprotective effects, also demonstrated that the treated groups had a faster recovery and reverted to their normal state. This could be attributed to the combination immunomodulatory action of probiotic and synbiotic ice cream formulations.
References
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Li, J., Chen, Y., Zhang, S., Zhao, Y., Gao, D., Xing, J, Xu, G. (2025). Purslane (Portulaca oleracea L.) polysaccharide attenuates carbon tetrachloride-induced acute liver injury by modulating the gut microbiota in mice. Genomics, 117(1), 110983. doi: https://doi.org/10.1016/j.ygeno.2024.110983
Ma, W., Li, W., Yu, S., Bian, H., Wang, Y., Jin, Y., et al. 2023. Immunomodulatory effects of complex probiotics on the immuno-suppressed mice induced by cyclophosphamide. Front Microbiol. 14:1055197. https://doi.org/10.3389/fmicb.2023.1055197
McFarland, L.V. 2010. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J Gastroenterol. 16(18):2202–2222. https://doi.org/10.3748/wjg.v16.i18.2202
Moazzam, S., Hussain, M.M. and Babar, A. 2013. Details about the yogurt starter culture and cell densities used. Response of hypothalamic-pituitary-adrenal axis and immune system to chronic restraint stress in male Sprague Dawley rats. Pak J Physiol. 9:29–31. https://doi.org/10.69656/pjp.v9i1.325
Mohammadi, R., Mortazavian, A.M., Khosrokhavar, R. et al. 2011. Probiotic ice cream: viability of probiotic bacteria and sensory properties. Ann Microbiol. 61:411–424. https://doi.org/10.1007/s13213-010-0188-z
Neurath, M.F. 2014. Cytokines in inflammatory bowel disease. Nature Rev Immunol. 14(5):329–342. https://doi.org/10.1038/nri3661
Öztürk, H.İ., Demirci, T. and Ak, N. 2018. Production of functional probiotic ice creams with white and dark blue fruits of Myrtus communis: the comparison of the prebiotic potentials on Lactobacillus casei 431 and functional characteristics. Food Sci Technol (LWT). 90(43):339–345. https://doi.org/10.1016/j.lwt.2017.12.049
Parhi, P., Liu, S.Q. and Choo, W.S. 2024. Synbiotics: effects of prebiotics on the growth and viability of probiotics in food matrices. Bioactive Carboh Diet Fibre. 32:100462. https://doi.org/10.1016/j.bcdf.2024.100462
Qin, Y.Q., Wang, L.Y., Yang, X.Y., Xu, Y.J., Fan, G., Fan, Y.G., Ren. J.N., An, Q. and Li, X. 2023. Inulin: properties and health benefits. Food Funct. 14(7):2948–2968. https://doi.org/10.1039/d2fo01096h
Rajendiran, V., Natarajan, V. and Devaraj, S.N. 2018. Anti-inflammatory activity of Alpinia officinarum hance on acute rat colon inflammation and tissue damage in DSS induced acute and chronic colitis models. Food Sci Human Wellness, 7(4):273–281. https://doi.org/10.1016/j.fshw.2018.10.004
Rodriguez, E. T., Flores, H. E. M., Lopez, J. O. R., Vega, R. Z., Garciglia, R. S., &Sanchez, R. E. P. (2017). Survival rate of Saccharomyces boulardii adapted to a functional freeze-dried yogurt: Experimental study related to processing, storage and digestion by Wistar rats. Functional Foods in Health & Disease, 7, 98–114.
https://doi.org/10.31989/ffhd.v7i2.319
Saddiqa, M., Umbreen, H., Zahoor, T., Bhatty, N. and Aftab, K. 2022. Immunomodulatory effect of yogurt enriched with garlic extract on ulcerative colitis induced rats. J Food Nutr Res. 10(5):377–385. https://doi.org/10.12691/jfnr-10-5-6
Samson, E.S., Olasunkanmi, A.K., Joel, J.S. and Alfred, E.F. 2012. Haematological and hepatotoxic potential of onion (Alliun cepa L.) and garlic (Allium sativum L.) extracts in rats. Eur J Med Plants. 2(4):290–307. https://doi.org/10.9734/EJMP/2012/1517
Sarwar, A., Aziz, T., Al-Dalali, S., Zhang, J., ud Din, J., Chen, C., Cao, Y., Fatima H. and Yang, Z. 2021. Characterization of synbiotic ice cream made with probiotic yeast Saccharomyces boulardii CNCM I-745 in combination with inulin. Food Sci Technol (LWT). 141:110910. https://doi.org/10.1016/j.lwt.2021.110910
Shao, X., Sun, C., Tang, X., Zhang, X., Han, D., Liang, S., Qu, R., Hui, X., Shan, Y., Hu, L., et al. 2020. Anti-inflammatory and intestinal microbiota modulation properties of Jinxiang garlic (Allium sativum L.) polysaccharides toward dextran sodium sulfate-induced colitis. J Agric Food Chem. 68:12295–12309. https://doi.org/10.1021/acs.jafc.0c04773
Shori, A.B., Aboulfazli, F. and Baba, A.S. 2018. Viability of probiotics in dairy products: a review focusing on yogurt, ice cream, and cheese. In: Advances in Biotechnology.
Tak, P.P. and Firestein, G.S. 2001. NF-κB: a key role in inflammatory diseases. J Clin Invest. 107(1):7–11. https://doi.org/10.1172/JCI11830
Tubesha, Z., Imam, M.U., Mahmud, R. and Ismail, M. 2013. Study on the potential toxicity of a thymoquinone-rich fraction nanoemulsion in Sprague Dawley rats. Molecules. 18(7):7460–7472. https://doi.org/10.3390/molecules18077460
Tung, J.M., Dolovich, L.R. and Lee, C.H. 2009. Prevention of Clostridium difficile infection with saccharomyces boulardii: a systematic review. Can J Gastroenterol. (12):817–821. https://doi.org/10.1155/2009/915847.
Umbreen, H., Arshad, M.U., Noreen, R. and Aftab, K. 2020. Ameliorative effects of apple and mango peels against hyperlipidemia and lipid peroxidation induced by hyperlipidemic diet. Sains Malaysiana. 49(6):1273–1282. https://doi.org/10.17576/jsm-2020-4906-05
Yang, N., Zhan, Y., Wan, J., Li, Y., Hu, X. and Liu, W. 2022. Effects of Lacidophilin tablets, yogurt, and bifid triple viable capsules on the gut microbiota of rats with antibiotic-associated diarrhea. Can J Infect Dis Med Microbiol. 2022:6521793. https://doi.org/10.1155/2022/6521793
Zeng, X., Li, X., Yue, Y., Wang, X., Chen, H., Gu, Y., Jia, H., He, Y., Yuan, Y. and Yue, T. 2022. Ameliorative effect of Saccharomyces cerevisiae JKSP39 on fusobacterium nucleatum and dextran sulfate sodium-induced colitis mouse model. J Agric Food Chem. 70(44):14179–14192. https://doi.org/10.1021/acs.jafc.2c05338
Zeng, A., Peng, M., Liu, H., Guo, Z., Xu, J., Wang, S., et al. 2019. Effects of debaryomyces hansenii treatment on intestinal mucosa microecology in mice with antibiotic-associated diarrhea. PLoS One, 14(11):e0224730. https://doi.org/10.1371/journal.pone.0224730
Zhao, N., Yang, Y., Chen, C., Jing, T., Hu, Y., Xu, H., Wang, S., He, Y., Liu, E. and Cui, J. 2022. Betaine supplementation alleviates dextran sulfate sodium-induced colitis via regulating the inflammatory response, enhancing the intestinal barrier, and altering gut microbiota. Food Funct. 13(24):12814–12826. https://doi.org/10.1039/d2fo02942a
Zhu, Z., Gu, Y., Zeng, C., Yang, M., Yu, H., Chen, H, Cai, H. (2022). Olanzapine-induced lipid disturbances: A potential mechanism through the gut microbiota-brain axis. Frontiers in pharmacology, 13, 897926. doi: 10.3389/fphar.2022.897926
Zhu, L., Gu, P. and Shen, H. (2019). Protective effects of berberine hydrochloride on DSS-induced ulcerative colitis in rats. Int Immunopharmacol. 68:242–251. https://doi.org/10.1016/j.intimp.2018.12.036
Bancroft, John D. and Gamble M. 2008. Theory and Practice of Histological Techniques, 6th edn. Churchill Livingstone Elsevier, Philadelphia, PA, 725 p.
Cencic, A. and Chingwaru, W. 2010. The role of functional foods, nutraceuticals, and food supplements in intestinal health. Nutrients. 2(6):611–625. https://doi.org/10.3390/nu2060611
Colombel J.F. and Mahadevan U. 2017. Inflammatory bowel disease: innovations and changing paradigms. Gastroenterology. 152:309–312. https://doi.org/10.1053/j.gastro.2016.12.004
Crobach, M.J., Dekkers, O.M., Wilcox, M.H. and Kuijper, E.J. 2016. European Society of Clinical Microbiology and Infectious Diseases (ESCMID): data review and recommendations for diagnosing Clostridium difficile-infection (CDI). Clin Microbiol Infect. 15(12):1053–1066. https://doi.org/10.1111/j.1469-0691.2009.03098.x
Crohn’s & Colitis Foundation of America. 2014, November. The facts about inflammatory bowel diseases. Updated December, 2023. https://www.crohnscolitisfoundation.org/sites/default/files/2019-02/Updated%20IBD%20Factbook.pdf. (Accessed on 10 March 2025).
Dong, L., Dong, F., Guo, P., Li, T., Fang, Y., Dong, Y, Zheng, Y. (2025). Gut microbiota as a new target for hyperuricemia: A perspective from natural plant products. Phytomedicine, 138, 156402. doi: https://doi.org/10.1016/j.phymed.2025.156402
Fan, J., Wang, L., Yang, T., Liu, J., Ge, W., Shen, J, Wang, L. (2024). Comparative analysis of gut microbiota in incident and prevalent peritoneal dialysis patients with peritoneal fibrosis, correlations with peritoneal equilibration test data in the peritoneal fibrosis cohort. Therapeutic Apheresis and Dialysis. doi: https://doi.org/10.1111/1744-9987.14226
Hamamoto, N., Maemura, K., Hirata, I., Murano, M., Sasaki, S and Katsu, K. 1999. Inhibition of dextran sulphate sodium (DSS)-induced colitis in mice by intracolonically administered antibodies against adhesion molecules (endothelial leucocyte adhesion molecule-1 [ELAM-1] orintercellular adhesion molecule-1 [ICAM-1]). Clin Exp Immunol. 117(3):462–468. https://doi.org/10.1046/j.1365-2249.1999.00985.x
Hempel, S., Newberry, S.J., Maher, A.R., Wang, Z., Miles, J.N., Shanman, R., ... and Shekelle, P.G. 2012. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis. JAMA. 307(18):1959–1969. https://doi.org/10.1001/jama.2012.3507
Hu, J.S., Huang, Y.Y., Kuang, J.H., Yu, J.J., Zhou, Q.Y. and Liu, D.M. 2020. Streptococcus thermophiles DMST-H2 promotes recovery in mice with antibiotic associated diarrhea. Microorganisms 8(11):1650. https://doi.org/10.3390/microorganisms8111650
Huth, P.J. and Park, K.M. 2012. Influence of dairy product and milk fat consumption on cardiovascular disease risk: a review of the evidence. Adv Nutr. 3(3):266–285. https://doi.org/10.3945/an.112.002030
Ikeda, M, Takeshima, F, Isomoto, H, Shikuwa, S., Mizuta, Y., Ozono, Y. and Kohno, S. 2008. Simvastatin attenuates trinitrobenzene sulfonic acid-induced colitis, but not oxazalone-induced colitis. Dig Dis Sci. 53(7):1869–1875. https://doi.org/10.1007/s10620-007-0102-0
Kanauchi, O., Serizawa, I., Araki, Y., Suzuki, A., Andoh, A. and Fujiyama, Y. 2003. Germinated barley foodstuff, a prebiotic product, ameliorates inflammation of colitis through modulation of the eneteric environment. J Gastroenterol. 38:134–141. https://doi.org/10.1007/s005350300022
Khalesi, M., Salami, M., Moslehishad, M., Winterburn, J. and Moosavi-Movahedi, A.A. 2017. Biomolecular content of camel milk: a traditional superfood towards future healthcare industry. Trends Food Sci Technol. 62:49–58. https://doi.org/10.1016/j.tifs.2017.02.004
Li, J., Chen, Y., Zhang, S., Zhao, Y., Gao, D., Xing, J, Xu, G. (2025). Purslane (Portulaca oleracea L.) polysaccharide attenuates carbon tetrachloride-induced acute liver injury by modulating the gut microbiota in mice. Genomics, 117(1), 110983. doi: https://doi.org/10.1016/j.ygeno.2024.110983
Ma, W., Li, W., Yu, S., Bian, H., Wang, Y., Jin, Y., et al. 2023. Immunomodulatory effects of complex probiotics on the immuno-suppressed mice induced by cyclophosphamide. Front Microbiol. 14:1055197. https://doi.org/10.3389/fmicb.2023.1055197
McFarland, L.V. 2010. Systematic review and meta-analysis of Saccharomyces boulardii in adult patients. World J Gastroenterol. 16(18):2202–2222. https://doi.org/10.3748/wjg.v16.i18.2202
Moazzam, S., Hussain, M.M. and Babar, A. 2013. Details about the yogurt starter culture and cell densities used. Response of hypothalamic-pituitary-adrenal axis and immune system to chronic restraint stress in male Sprague Dawley rats. Pak J Physiol. 9:29–31. https://doi.org/10.69656/pjp.v9i1.325
Mohammadi, R., Mortazavian, A.M., Khosrokhavar, R. et al. 2011. Probiotic ice cream: viability of probiotic bacteria and sensory properties. Ann Microbiol. 61:411–424. https://doi.org/10.1007/s13213-010-0188-z
Neurath, M.F. 2014. Cytokines in inflammatory bowel disease. Nature Rev Immunol. 14(5):329–342. https://doi.org/10.1038/nri3661
Öztürk, H.İ., Demirci, T. and Ak, N. 2018. Production of functional probiotic ice creams with white and dark blue fruits of Myrtus communis: the comparison of the prebiotic potentials on Lactobacillus casei 431 and functional characteristics. Food Sci Technol (LWT). 90(43):339–345. https://doi.org/10.1016/j.lwt.2017.12.049
Parhi, P., Liu, S.Q. and Choo, W.S. 2024. Synbiotics: effects of prebiotics on the growth and viability of probiotics in food matrices. Bioactive Carboh Diet Fibre. 32:100462. https://doi.org/10.1016/j.bcdf.2024.100462
Qin, Y.Q., Wang, L.Y., Yang, X.Y., Xu, Y.J., Fan, G., Fan, Y.G., Ren. J.N., An, Q. and Li, X. 2023. Inulin: properties and health benefits. Food Funct. 14(7):2948–2968. https://doi.org/10.1039/d2fo01096h
Rajendiran, V., Natarajan, V. and Devaraj, S.N. 2018. Anti-inflammatory activity of Alpinia officinarum hance on acute rat colon inflammation and tissue damage in DSS induced acute and chronic colitis models. Food Sci Human Wellness, 7(4):273–281. https://doi.org/10.1016/j.fshw.2018.10.004
Rodriguez, E. T., Flores, H. E. M., Lopez, J. O. R., Vega, R. Z., Garciglia, R. S., &Sanchez, R. E. P. (2017). Survival rate of Saccharomyces boulardii adapted to a functional freeze-dried yogurt: Experimental study related to processing, storage and digestion by Wistar rats. Functional Foods in Health & Disease, 7, 98–114.
https://doi.org/10.31989/ffhd.v7i2.319
Saddiqa, M., Umbreen, H., Zahoor, T., Bhatty, N. and Aftab, K. 2022. Immunomodulatory effect of yogurt enriched with garlic extract on ulcerative colitis induced rats. J Food Nutr Res. 10(5):377–385. https://doi.org/10.12691/jfnr-10-5-6
Samson, E.S., Olasunkanmi, A.K., Joel, J.S. and Alfred, E.F. 2012. Haematological and hepatotoxic potential of onion (Alliun cepa L.) and garlic (Allium sativum L.) extracts in rats. Eur J Med Plants. 2(4):290–307. https://doi.org/10.9734/EJMP/2012/1517
Sarwar, A., Aziz, T., Al-Dalali, S., Zhang, J., ud Din, J., Chen, C., Cao, Y., Fatima H. and Yang, Z. 2021. Characterization of synbiotic ice cream made with probiotic yeast Saccharomyces boulardii CNCM I-745 in combination with inulin. Food Sci Technol (LWT). 141:110910. https://doi.org/10.1016/j.lwt.2021.110910
Shao, X., Sun, C., Tang, X., Zhang, X., Han, D., Liang, S., Qu, R., Hui, X., Shan, Y., Hu, L., et al. 2020. Anti-inflammatory and intestinal microbiota modulation properties of Jinxiang garlic (Allium sativum L.) polysaccharides toward dextran sodium sulfate-induced colitis. J Agric Food Chem. 68:12295–12309. https://doi.org/10.1021/acs.jafc.0c04773
Shori, A.B., Aboulfazli, F. and Baba, A.S. 2018. Viability of probiotics in dairy products: a review focusing on yogurt, ice cream, and cheese. In: Advances in Biotechnology.
Tak, P.P. and Firestein, G.S. 2001. NF-κB: a key role in inflammatory diseases. J Clin Invest. 107(1):7–11. https://doi.org/10.1172/JCI11830
Tubesha, Z., Imam, M.U., Mahmud, R. and Ismail, M. 2013. Study on the potential toxicity of a thymoquinone-rich fraction nanoemulsion in Sprague Dawley rats. Molecules. 18(7):7460–7472. https://doi.org/10.3390/molecules18077460
Tung, J.M., Dolovich, L.R. and Lee, C.H. 2009. Prevention of Clostridium difficile infection with saccharomyces boulardii: a systematic review. Can J Gastroenterol. (12):817–821. https://doi.org/10.1155/2009/915847.
Umbreen, H., Arshad, M.U., Noreen, R. and Aftab, K. 2020. Ameliorative effects of apple and mango peels against hyperlipidemia and lipid peroxidation induced by hyperlipidemic diet. Sains Malaysiana. 49(6):1273–1282. https://doi.org/10.17576/jsm-2020-4906-05
Yang, N., Zhan, Y., Wan, J., Li, Y., Hu, X. and Liu, W. 2022. Effects of Lacidophilin tablets, yogurt, and bifid triple viable capsules on the gut microbiota of rats with antibiotic-associated diarrhea. Can J Infect Dis Med Microbiol. 2022:6521793. https://doi.org/10.1155/2022/6521793
Zeng, X., Li, X., Yue, Y., Wang, X., Chen, H., Gu, Y., Jia, H., He, Y., Yuan, Y. and Yue, T. 2022. Ameliorative effect of Saccharomyces cerevisiae JKSP39 on fusobacterium nucleatum and dextran sulfate sodium-induced colitis mouse model. J Agric Food Chem. 70(44):14179–14192. https://doi.org/10.1021/acs.jafc.2c05338
Zeng, A., Peng, M., Liu, H., Guo, Z., Xu, J., Wang, S., et al. 2019. Effects of debaryomyces hansenii treatment on intestinal mucosa microecology in mice with antibiotic-associated diarrhea. PLoS One, 14(11):e0224730. https://doi.org/10.1371/journal.pone.0224730
Zhao, N., Yang, Y., Chen, C., Jing, T., Hu, Y., Xu, H., Wang, S., He, Y., Liu, E. and Cui, J. 2022. Betaine supplementation alleviates dextran sulfate sodium-induced colitis via regulating the inflammatory response, enhancing the intestinal barrier, and altering gut microbiota. Food Funct. 13(24):12814–12826. https://doi.org/10.1039/d2fo02942a
Zhu, Z., Gu, Y., Zeng, C., Yang, M., Yu, H., Chen, H, Cai, H. (2022). Olanzapine-induced lipid disturbances: A potential mechanism through the gut microbiota-brain axis. Frontiers in pharmacology, 13, 897926. doi: 10.3389/fphar.2022.897926
Zhu, L., Gu, P. and Shen, H. (2019). Protective effects of berberine hydrochloride on DSS-induced ulcerative colitis in rats. Int Immunopharmacol. 68:242–251. https://doi.org/10.1016/j.intimp.2018.12.036
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Sarwar, A., Ullah, N., Yang, Z., Aziz, T., Alhomrani, M., Shami, A., Al-Asmari, F., Anajirih, N., ALsuhaymi, N., Baothman, B., Alhomrani, M., AlQadeeb, A., & Al-Joufi, F. (2025). Assessment of Saccharomyces boulardii CNCM I-745-supplemented probiotic and synbiotic ice cream in mitigating trinitrobenzene sulfonic acid-induced colitis in rats. Italian Journal of Food Science, 37(3), 245-254. https://doi.org/10.15586/ijfs.v37i3.2953
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Sarwar, A., Ullah, N., Yang, Z., Aziz, T., Alhomrani, M., Shami, A., Al-Asmari, F., Anajirih, N., ALsuhaymi, N., Baothman, B., Alhomrani, M., AlQadeeb, A., & Al-Joufi, F. (2025). Assessment of Saccharomyces boulardii CNCM I-745-supplemented probiotic and synbiotic ice cream in mitigating trinitrobenzene sulfonic acid-induced colitis in rats. Italian Journal of Food Science, 37(3), 245-254. https://doi.org/10.15586/ijfs.v37i3.2953