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Original Communication

Oral administration of Lactobacillus casei Shirota can ameliorate the adverse effect of an acute aflatoxin exposure in Sprague Dawley rats

Published Online:https://doi.org/10.1024/0300-9831/a000513

Abstract. Aflatoxin B1(AFB1) is a toxic compound commonly found in some crops with an adverse health effect on human and animals. Some beneficial microorganisms (or probiotics) such as lactic acid bacteria have shown the ability to reduce the bioavailability of aflatoxins and its intestinal absorption. However, the dose and duration of aflatoxins exposure and probiotic treatment can influence the ability of probiotics to remove aflatoxins. Therefore, this research aimed to investigate the efficacy of oral probiotic Lactobacillus casei Shirota strain (LcS) induction in an acute exposure to AFB1 in rats. Experimentally, Sprague Dawley rats were divided into three groups: AFB1 only (n = 9); AFB1 treated with LcS (n = 9); and control (no AFB1 exposure) (n = 6) groups. The blood AFB1 level of rats treated with LcS was slightly lower than the untreated AFB1 induced rats (11.12 ± 0.71 vs 10.93 ± 0.69 ng g–1). Also, LcS treatment slightly moderated the liver and kidney biomarkers in AFB1 induced rats. However, a trend for a significant difference was only observed in ALT of AFB1 induced rats treated with LcS compared to their counterparts (126.11 ± 36.90 vs 157.36 ± 15.46, p = 0.06). Rats’ body weight decreased in all animals force-fed with AFB1 with no significant difference between LcS treatment compared to the counterpart. In conclusion, this experiment indicated that probiotic LsC was able to slightly ameliorate the adverse effect of an acute exposure to AFB1 in rats. However, future studies with longer probiotics treatment or higher probiotics dose is required to confirm these findings.

Literature

  • Bennett JW, Klich M. (2003) Mycotoxins. Clin Microbiol Rev.16, 497–516. First citation in articleCrossrefGoogle Scholar

  • Peraica M, Richter D, Rasic D. (2014) Mycotoxicoses in children. Arh Hig Rada.65, 347–63. First citation in articleCrossrefGoogle Scholar

  • Lehmann L, Wagner J, Metzler M. (2006) Estrogenic and clastogenic potential of the mycotoxin alternariol in cultured mammalian cells. Food Chem Toxicol.44, 398–408. First citation in articleCrossrefGoogle Scholar

  • Creppy EE. (2002) Update of survey, regulation and toxic effects of mycotoxins in Europe. Toxicol Lett.127, 19–28. First citation in articleGoogle Scholar

  • Robbins CA, Swenson LJ, Nealley ML, Kelman BJ, Gots RE. (2000) Health effects of mycotoxins in indoor air: a critical review. Appl Occup Environ Hyg.15, 773–84. First citation in articleCrossrefGoogle Scholar

  • Williams JH, Phillips TD, Jolly PE, Stiles JK, Jolly CM, Aggarwal D. (2004) Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions. Am J Clin Nutr.80, 1106–22. First citation in articleCrossrefGoogle Scholar

  • Pitt J. (2000) Toxigenic fungi and mycotoxins. Br Med Bull.56, 184–92. First citation in articleCrossrefGoogle Scholar

  • International Agency for Research on Cancer. (2002) IARC Working Group on the Evaluation of Carcinogenic Risks to Humans: Some traditional herbal medicines, some mycotoxins, naphthalene and styrene: World Health Organization. First citation in articleGoogle Scholar

  • Azziz-Baumgartner E, Lindblade K, Gieseker K, Rogers HS, Kieszak S, Njapau H, et al. (2005) Case–control study of an acute aflatoxicosis outbreak, Kenya, 2004. Environ Health Perspect.113, 1779. First citation in articleCrossrefGoogle Scholar

  • Chao TC, Maxwell SM, Wong SY. (1991) An outbreak of aflatoxicosis and boric acid poisoning in Malaysia: a clinicopathological study. J Pathol.164, 225–33. First citation in articleCrossrefGoogle Scholar

  • Arzandeh S, Selamat J, Lioe H. (2010) Aflatoxin in raw peanut kernels marketed in Malaysia. J Food Drug Anal.18. First citation in articleGoogle Scholar

  • Leong Y-H, Rosma A, Latiff AA, Ahmad NI. (2011) Exposure assessment and risk characterization of aflatoxin B1 in Malaysia. Mycotoxin Res.27, 207–14. First citation in articleGoogle Scholar

  • Phillips T, Afriyie-Gyawu E, Williams J, Huebner H, Ankrah N-A, Ofori-Adjei D, et al. (2008) Reducing human exposure to aflatoxin through the use of clay: a review. Food Addit Contam.25, 134–45. First citation in articleCrossrefGoogle Scholar

  • Kabak B, Ozbey F. (2012) Aflatoxin M 1 in UHT milk consumed in Turkey and first assessment of its bioaccessibility using an in vitro digestion model. Food Control.28, 338–44. First citation in articleCrossrefGoogle Scholar

  • Armando M, Dogi C, Poloni V, Rosa C, Dalcero A, Cavaglieri L. (2013) In vitro study on the effect of Saccharomyces cerevisiae strains on growth and mycotoxin production by Aspergillus carbonarius and Fusarium graminearum. Int J Food Microbiol 161, 182–8. First citation in articleCrossrefGoogle Scholar

  • Gratz S, Mykkänen H, El-Nezami H. (2005) Aflatoxin B1 binding by a mixture of Lactobacillus and Propionibacterium: in vitro versus ex vivo. J Food Prot.68, 2470–4. First citation in articleCrossrefGoogle Scholar

  • Ferrer M, Manyes L, Manes J, Meca G. (2015) Influence of prebiotics, probiotics and protein ingredients on mycotoxin bioaccessibility. Food & function.6, 987–94. First citation in articleCrossrefGoogle Scholar

  • Kabak B, Brandon EF, Var I, Blokland M, Sips AJ. (2009) Effects of probiotic bacteria on the bioaccessibility of aflatoxin B(1) and ochratoxin A using an in vitro digestion model under fed conditions. Journal of environmental science and health Part B, Pesticides, food contaminants, and agricultural wastes.44, 472–80. First citation in articleGoogle Scholar

  • FAO/WHO, Guidelines for the Evaluation of Probiotics in Food. London, Ontario, Canada2002. First citation in articleGoogle Scholar

  • Irwin C, Khalesi S, Cox AJ, Grant G, Davey AK, Bulmer AC, et al. (2017) Effect of 8-Weeks Prebiotics/Probiotics Supplementation on Alcohol Metabolism and Blood Biomarkers of Healthy Adults: A Pilot Study. European journal of nutrition. First citation in articleCrossrefGoogle Scholar

  • Khalesi S, Sun J, Buys N, Jayasinghe R. (2014) Effect of Probiotics on Blood Pressure A Systematic Review and Meta-Analysis of Randomized, Controlled Trials. Hypertension.64, 897–903. First citation in articleCrossrefGoogle Scholar

  • Nikbakht E, Khalesi S, Singh I, Williams LT, West NP, Colson N. (2016) Effect of probiotics and synbiotics on blood glucose: a systematic review and meta-analysis of controlled trials. European journal of nutrition. First citation in articleCrossrefGoogle Scholar

  • Stanley D, Hughes RJ, Geier MS, Moore RJ. (2016) Bacteria within the Gastrointestinal Tract Microbiota Correlated with Improved Growth and Feed Conversion: Challenges Presented for the Identification of Performance Enhancing Probiotic Bacteria. Frontiers in microbiology.7, 187. First citation in articleCrossrefGoogle Scholar

  • Takada M, Nishida K, Kataoka-Kato A, Gondo Y, Ishikawa H, Suda K, et al. (2016) Probiotic Lactobacillus casei strain Shirota relieves stress-associated symptoms by modulating the gut-brain interaction in human and animal models. Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.28, 1027–36. First citation in articleCrossrefGoogle Scholar

  • El-Nezami H, Chrevatidis A, Auriola S, Salminen S, Mykkänen H. (2002) Removal of common Fusarium toxins in vitro by strains of Lactobacillus and Propionibacterium. Food Addit Contam.19, 680–6. First citation in articleCrossrefGoogle Scholar

  • Styriak I, Conková E. (2002) Microbial binding and biodegradation of mycotoxins. Vet Hum Toxicol.44, 358–61. First citation in articleGoogle Scholar

  • Mohd Redzwan S, Abd Mutalib MS, Wang JS, Ahmad Z, Kang MS, Abdul Rahman N, et al. (2016) Effect of supplementation of fermented milk drink containing probiotic Lactobacillus casei Shirota on the concentrations of aflatoxin biomarkers among employees of Universiti Putra Malaysia: a randomised, double-blind, cross-over, placebo-controlled study. Br J Nutr.115, 39–54. First citation in articleCrossrefGoogle Scholar

  • Hernandez-Mendoza A, González-Córdova AF, Vallejo-Cordoba B, Garcia HS. (2011) Effect of oral supplementation of Lactobacillus reuteri in reduction of intestinal absorption of aflatoxin B1 in rats. J Basic Microbiol.51, 263–8. First citation in articleCrossrefGoogle Scholar

  • Nikbakht Nasrabadi E, Jamaluddin R, Mutalib A, Khaza’ai H, Khalesi S, Mohd Redzwan S. (2013) Reduction of aflatoxin level in aflatoxin-induced rats by the activity of probiotic Lactobacillus casei strain Shirota. J Appl Microbiol.114, 1507–15. First citation in articleCrossrefGoogle Scholar

  • Lee YK, Salminen S. (2009) Handbook of probiotics and prebiotics: John Wiley & Sons. First citation in articleCrossrefGoogle Scholar

  • Firmin S, Gandia P, Morgavi DP, Houin G, Jouany J, Bertin G, et al. (2010) Modification of aflatoxin B1 and ochratoxin A toxicokinetics in rats administered a yeast cell wall preparation. Food Addit Contam.27, 1153–60. First citation in articleCrossrefGoogle Scholar

  • Verna EC, Lucak S. (2010) Use of probiotics in gastrointestinal disorders: what to recommend? Therapeutic Advances in Gastroenterology.3, 307–19. First citation in articleGoogle Scholar

  • Karimi G, Jamaluddin R, Mohtarrudin N, Ahmad Z, Khazaai H, Parvaneh M. (2017) Single-species versus dual-species probiotic supplementation as an emerging therapeutic strategy for obesity. Nutrition, metabolism, and cardiovascular diseases : NMCD.27, 910–8. First citation in articleCrossrefGoogle Scholar

  • Leong Y-H, Rosma A, Latiff AA, Izzah AN. (2012) Associations of serum aflatoxin B 1–lysine adduct level with socio-demographic factors and aflatoxins intake from nuts and related nut products in Malaysia. Int J Hyg Environ Health.215, 368–72. First citation in articleGoogle Scholar

  • Redzwan SM, Rosita J, Sokhini AMM, Aqilah ARN. (2012) Association between aflatoxin M1 excreted in human urine samples with the consumption of milk and dairy products. Bull Environ Contam Toxicol.89, 1115–9. First citation in articleCrossrefGoogle Scholar

  • Mykkänen H, Zhu H, Salminen E, Juvonen RO, Ling W, Ma J, et al. (2005) Fecal and urinary excretion of aflatoxin B1 metabolites (AFQ1, AFM1 and AFB-N7-guanine) in young Chinese males. Int J Cancer.115, 879–84. First citation in articleCrossrefGoogle Scholar

  • Polychronaki N, Wild CP, Mykkänen H, Amra H, Abdel-Wahhab M, Sylla A, et al. (2008) Urinary biomarkers of aflatoxin exposure in young children from Egypt and Guinea. Food Chem Toxicol.46, 519–26. First citation in articleCrossrefGoogle Scholar

  • Sabran MR, Jamaluddin R, Mutalib MSA. (2012) Screening of aflatoxin M 1, a metabolite of aflatoxin B 1 in human urine samples in Malaysia: a preliminary study. Food Control.28, 55–8. First citation in articleCrossrefGoogle Scholar

  • Aoki T, Asahara T, Matsumoto K, Takada T, Chonan O, Nakamori K, et al. (2014) Effects of the continuous intake of a milk drink containing Lactobacillus casei strain Shirota on abdominal symptoms, fecal microbiota, and metabolites in gastrectomized subjects. Scandinavian journal of gastroenterology.49, 552–63. First citation in articleCrossrefGoogle Scholar

  • Reale M, Boscolo P, Bellante V, Tarantelli C, Di Nicola M, Forcella L, et al. (2012) Daily intake of Lactobacillus casei Shirota increases natural killer cell activity in smokers. Br J Nutr.108, 308–14. First citation in articleCrossrefGoogle Scholar

  • Wong S, Jamous A, O’Driscoll J, Sekhar R, Weldon M, Yau CY, et al. (2014) A Lactobacillus casei Shirota probiotic drink reduces antibiotic-associated diarrhoea in patients with spinal cord injuries: a randomised controlled trial. Br J Nutr.111, 672–8. First citation in articleCrossrefGoogle Scholar

  • Maxuitenko YY, North WG, Roebuck B. (1997) Urinary taurine as a non-invasive marker of aflatoxin B1-induced hepatotoxicity: success and failure. Toxicology.118, 159–69. First citation in articleCrossrefGoogle Scholar

  • Abdel-Wahhab MA, Ahmed H, Hagazi MM. (2006) Prevention of aflatoxin B1-initiated hepatotoxicity in rat by marine algae extracts. J Appl Toxicol.26, 229–38. First citation in articleCrossrefGoogle Scholar

  • Barber M, McMillan D, Wallace A, Ross J, Preston T, Fearon K. (2004) The response of leptin, interleukin–6 and fat oxidation to feeding in weight-losing patients with pancreatic cancer. Br J Cancer.90, 1129. First citation in articleCrossrefGoogle Scholar

  • Gratz S. (2007) Aflatoxin binding by probiotics: experimental studies on intestinal aflatoxin transport, metabolism and toxicity: University of Kuopio, Finland. First citation in articleGoogle Scholar

  • Million M, Angelakis E, Paul M, Armougom F, Leibovici L, Raoult D. (2012) Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb Pathog.53, 100–8. First citation in articleCrossrefGoogle Scholar

  • Lu H, Li Y. (2002) Effects of dimethyl diphenyl bicarboxylate on the metabolism and hepatotoxicity of aflatoxin B1 in rats. Yao xue xue bao = Acta pharmaceutica Sinica.37, 753–7. First citation in articleGoogle Scholar

  • Abdel-Wahhab MA, Abdel-Azim SH, El-Nekeety AA. (2008) Inula crithmoides extract protects against ochratoxin A-induced oxidative stress, clastogenic and mutagenic alterations in male rats. Toxicon.52, 566–73. First citation in articleCrossrefGoogle Scholar

  • Khalesi S, Johnson DW, Campbell K, Williams S, Fenning A, Saluja S, et al. (2017. https://doi.org/10.1007/s00394-017-1568-y) Effect of probiotics and synbiotics consumption on serum concentrations of liver function test enzymes: a systematic review and meta-analysis. European Journal of Nutrition. First citation in articleCrossrefGoogle Scholar

  • Martinez-de-Anda A, Valdivia AG, Jaramillo-Juarez F, Reyes JL, Ortiz R, Quezada T, et al. (2010) Effects of aflatoxin chronic intoxication in renal function of laying hens. Poultry science.89, 1622–8. First citation in articleCrossrefGoogle Scholar

  • Abdel-Wahhab MA, Omara EA, Abdel-Galil MM, Hassan NS, Nada SA, Saeed A, et al. (2007) Zizyphus spina-christi extract protects against aflatoxin B1-intitiated hepatic carcinogenicity. Afr J Tradit Complement Altern Med.4, 248. First citation in articleGoogle Scholar

  • Miller DM, Wilson DM. (1994) Veterinary Diseases. First citation in articleGoogle Scholar

  • Sherif SO, Salama EE, Abdel-Wahhab MA. (2009) Mycotoxins and child health: The need for health risk assessment. Int J Hyg Environ Health.212, 347–68. First citation in articleCrossrefGoogle Scholar

  • Hathout AS, Mohamed SR, El-Nekeety AA, Hassan NS, Aly SE, Abdel-Wahhab MA. (2011) Ability of Lactobacillus casei and Lactobacillus reuteri to protect against oxidative stress in rats fed aflatoxins-contaminated diet. Toxicon.58, 179–86. First citation in articleCrossrefGoogle Scholar