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Effect of lactic acid bacteria isolated from some fermented dairy products on carbon tetrachloride-induced hepatotoxicity and nephrotoxicity of albino rats

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Abstract

The current research was performed to evaluate the potential protective effect of Lactobacillus paracasei ssp. paracasei, Pediococcus acidilactici, Lactococcus lactis ssp. lactis, and silymarin in the alleviation of health (hepatic and renal) complications caused by carbon tetrachloride (CCl4) in rats. Healthy sixty albino rats were divided into six groups, the first group was control (negative), the second group (control positive) was injected CCl4 (1 ml/kg, 1:1 v/v paraffin oil mixture, i.p. every third day for 8 weeks), the third group (CCl4 + silymarin group) receiving both CCl4 and daily silymarin therapy (50 mg/kg, oral), and the fourth group: CCl4 + Lactobacillus paracasei (1 ml orally). The fifth group (CCl4 + Pediococcus acidilactici 1 ml orally) and the sixth group (CCl4 + Lactococcus lactis 1 ml orally) for 8 weeks per day. Biochemical markers were tested for blood, liver, and kidney tissue. Histopathological examination of the liver and kidney tissues was performed. The findings obtained have shown that Lactobacillus paracasei ssp. paracasei, Pediococcus acidilactici, and Lactococcus lactis ssp. lactis improved the disrupted biochemical parameters caused by CCl4 therapy. Besides, the findings of the histopathology are in consistent with biochemical parameters and the protective ability of lactic acid bacteria suggesting that the best lactic acid bacteria were Pediococcus acidilactici that helped strengthen liver fibrosis caused by CCl4 therapy, while the best bacterium for improving renal damage was Lactococcus lactis.

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References

  • Abdel Salam OM, Sleem AA, Omara EA, Hassan NS (2007) Effect of ribavirin alone or combined with silymarin on carbon tetrachloride induced hepatic damage in rats. Drug Target Insights 2:19–27

    Google Scholar 

  • Abdel-Daim MM, Abuzead SMM, Halawa SM (2013) Protective role of Spirulina platensis against acute deltamethrin-induced toxicity in rats. PLoS One 8:e72991

    CAS  Google Scholar 

  • Abdel-Daim MM, Farouk SM, Madkour FF, AZAB SS (2015) Antiinflammatory and immunomodulatory effects of Spirulina platensis in comparison to Dunaliella salina in acetic acid-induced rat experimental colitis. Immunopharmacol Immunotoxicol 37:126–139

    CAS  Google Scholar 

  • Abdo W, Hirata A, Shukry M, Kamal T, Abdel-Sattar E, Mahrous E, Yanai T (2015)Calligonum comosum extract inhibits diethylnitrosamine-induced hepatocarcinogenesis in rats. Oncol Lett 10(2):716–722

    CAS  Google Scholar 

  • Al-Hariri M (2011) Propolis and its direct and indirect hypoglycemic effect. J Fam Community Med 18(3):152–154. https://doi.org/10.4103/2230-8229.90015

    Article  Google Scholar 

  • Al-Sayed E, Abdel-Daim MM, Kilany OE, Karonen M, Sinkkonen J (2015) Protective role of polyphenols from Bauhinia hookeri against carbon tetrachloride-induced hepato- and nephrotoxicity in mice. Ren Fail 37(7):1198–1207

    CAS  Google Scholar 

  • Asuquo OR, Ekanem TB, Eluwa MAm, Oko OO, Ikpi DE (2012) Evaluation of toxicological effects of Spondias mombin in adult male Wistar rats. J Nat Sci Res 2:144–151

    Google Scholar 

  • Bancroft JD, Stevens A, Turner DR (1996) Theory and practice of histological techniques, Fourth edn. Churchil Livingstone, New York, London, San Francisco, Tokyo

  • Bergey’s Manual of Systemic Bacteriology (1984) Krieg, N.R. and Holt, J.G., Eds., Baltimore: Williams and Wilkins

  • Bhattacharya T, Maishu PS, Akter R, Rahman HM, Akhtar MF, Saleem A, Jumah MB, Kamel M, Abdel-Latif MA, Abdel-Daim MM (2021) A review on natural sources derived protein nanoparticles as anticancer agents. Curr Top Med Chem 21(1)

  • Bikheet MM, Darwish AM, Hassanein KA, Shalaby SI (2015) Lactic acid bacteria with potential to eliminate fungal spoilage in cheeses. Proceeding the 2nd Minia international conference “Agriculture and Irrigation in Nile Basin Countries” 32–25 March, Minia, Egypt, pp312–317

  • Bikheet MM, Mahmoud ME, Hassan HM, Yassien EE (2021) The effect of two strains of LAB (P. acidilactaci and L. lactis) in laboratory rats. Scientific Journal of Agricultural Sciences 3(1):137–143. https://doi.org/10.21608/sjas.2021.73876.1093

  • Bin-Jumah MN, AL-Huqail AA, Abdelnaeim N, Kamel M, Fouda MMA, Abulmeaty MMA, Saadeldin IM, Abdel-Daim MM (2021) Potential protective effects of Spirulina platensis on liver, kidney, and brain acrylamide toxicity in rats. Environ Sci Pollut Res Int 28:26653–26663

  • Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ (2015) Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis 26:3854

    Google Scholar 

  • Carlin MR, Kazemi SK, Sangwan N, Cano RDJ (2018). Probiotics and methods of use. The Biocollective LLC, assignee. US Pat. 62/594,201

  • Chlopcikova S, Psotova J, Miketova P, Simanek V (2004) Chemoprotective effect of plant phenolics against anthracyclin-induced toxicity on rats cardiomyocytes part I. Silymarin and its flavonolignans. Phytother Res 18:107–110

    CAS  Google Scholar 

  • Corthier G, Renault P (1999) Future directions for research on biotherapeutic agents: contribution of genetic approaches on lactic acid bacteria. In: Elmer GW (ed) Biotherapeutic agents and infectious diseases. Humana Press Inc., Totowa, N.J, pp 269–304

    Google Scholar 

  • Dacie JV, Lewis SM (1991) Practical haematology, 7th edn. Churchil Livingstone, Edinburgh, pp 54–79

    Google Scholar 

  • DeGruttola AK, Low D, Mizoguchi A, Mizoguchi E (2016) Current understanding of dysbiosis in disease in human and animal models. Inflamm Bowel Dis 22:1137–1150

    Google Scholar 

  • Dubey V, Mishra AK, Ghosh AR, Mandal BK (2019) Probiotic Pediococcus pentosaceus GS4 shields brush border membrane and alleviates liver toxicity imposed by chronic cadmium exposure in Swiss albino mice. J Appl Microbiol 126:1233–1244

    CAS  Google Scholar 

  • Elmer GW, Surawicz CM, McFarland LV (1996) Biotherapeutic agents. A neglected modality for the treatment and prevention of selected intestinal and vaginal infection. JAMA 275:870–876

    CAS  Google Scholar 

  • El-Sayed A, Kamel M (2021) Bovine mastitis prevention and control in the post-antibiotic era. Trop Anim Health Prod 53:236

    Google Scholar 

  • Eric E U, Adolphus E (2020) Ameliorative effects of turmeric extract against CCl4 induced liver and kidney injury in adult Wistar rat. Asian Journal of Immunology 3(4):36–42

    Google Scholar 

  • Fahmy NM, Al-Sayed E, Abdel-Daim MM, Karonen M, Singab AN (2016) Protective effect of Terminalia muelleri against carbon tetrachloride induced hepato and nephro-toxicity in mice and characterization of its bioactive constituents. Pharm Biol 54(2):303–313

    CAS  Google Scholar 

  • Hassanein KMA (2014) Immunohistochemical and ultrastructural studies on oval cells during hepatic carcinogenesis and fibrosis in rats. Glob Vet 13(6):1029–1036

    Google Scholar 

  • Hassanein KMA, Al-Emam A, Raded K (2016) Prophylactic effects of thymoquinone against carbon tetrachloride-induced hepatic damage in Sprague-Dawley rats. J Appl Pharm Sci 6(02):167–171

    CAS  Google Scholar 

  • Heeba GH, Mahmoud ME (2014) Therapeutic potential of morin against liver fibrosis in rats: modulation of oxidative stress, cytokine production and nuclear factor kappa B. Environ Toxicol Pharmacol 37:662–671

    CAS  Google Scholar 

  • Hoeney M (1985) Introduction to clinical immunology. Butterworth, London, pp3

  • Ilhan N, Seckin D (2005) Protective effect of Nigella sativa seeds on CCl4-induced hepatotoxicity. F U Saglik Bil Gergisi 19(3):175–179

    Google Scholar 

  • Jain NC (1986) In: Jain NC (ed) Schalm’s veterinary haematology, 4th edn. Lea and Febiger, Philadelphia, p 1221

    Google Scholar 

  • Jantararussamee C, Rodniem S, Taweechotipatr M, Showpittapornchai U, Pradidarcheep W (2020) Hepatoprotective effect of probiotic lactic acid bacteria on thioacetamide-induced liver fibrosis in rats. Probiotics Antimicrob Proteins 13:40–50. https://doi.org/10.1007/s12602-020-09663-6

    Article  CAS  Google Scholar 

  • Joint Food and Agriculture Organization and World Health Organization (FAO/WHO) (2002) Working group report on drafting guidelines for the evaluation of probiotics in food. London, Ontario, Canada, pp 1–11

  • Joseph G, Ionchin S, Ramachandran J (2006) Efficacy of silymarin and curcumin on dimethyl nitrosamine induced liver fibrosis in rats. Biomedicine 26:18–26

    Google Scholar 

  • Kaizu H, Sasaki M, Nakajima H (1993) Effect of antioxidative lactic acid bacteria on rats fed a diet deficient in vitamin E. J Dairy Sci 76:2493–2499

    CAS  Google Scholar 

  • Kashinath RT (1990) Hypolipidemic effect of disulphide in rats fed with high lipids diets and/or ethanol. Ph.D. Thesis University of Bangalore, 221–225

  • Kim J-E, Kim JY, Lee KW, Lee HJ (2007) Cancer chemopreventive effects of lactic acid bacteria. J Microbiol Biotechnol 17(8):1227–1235

    Google Scholar 

  • Krinsky NI (1992) Mechanism of action of biological antioxidants. Proc Soc Exp Biol Med 200:248–254

    CAS  Google Scholar 

  • Kris-Etherton PM, Fleming JA (2015) Emerging nutrition science on fatty acids and cardiovascular disease: nutritionists’ perspectives. Adv Nutr 6:326S–337S

    CAS  Google Scholar 

  • Lata J, Jurankova J, Kopacova M, Vitek P (2011) Probiotics in hepatology. World J Gastroenterol 17(24):2890–2896

    Google Scholar 

  • LeBlanc JG, Burgess C, Sesma F, Savoy de Giori G, van Sinderen D (2005)Lactococcus lactis is capable of improving the riboflavin status in deficient rats. Br J Nutr 94:262–267. https://doi.org/10.1079/BJN20051473

    Article  CAS  Google Scholar 

  • Line MY, Yen CL (1999) Antioxidative ability of lactic acid bacteria. J Agric Food Chem 47:1460–1466

    Google Scholar 

  • Mandour AS, Samir H, El-Beltagy MA, Abdel-Daim MM, Izumi W, Ma D, Matsuura K, Tanaka R, Watanabe G (2020) Effect of supra-nutritional selenium-enriched probiotics on hematobiochemical, hormonal, and Doppler hemodynamic changes in male goats. Environ Sci Pollut Res Int 27(16):19447–19460

    CAS  Google Scholar 

  • Marsillach J, Camps J, Ferre N, Beltran R, Rul A, Mackness B, Mackness M, Joven J (2009)Paraoxonase-1 is related to inflammation, fibrosis and PPAR delta in experimental liver disease. BMC Gastroenterol 9(3):1–13

    Google Scholar 

  • Maurice CF, Haiser HJ, Turnbaugh PJ (2013) Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 152:39–50

    CAS  Google Scholar 

  • Mohamed NZ, Aly HF, El-Mezayen H, El-Salamony HE (2016) Bee honey modulates the oxidant-antioxidant imbalance in diethylnitrosamine-initiated rat hepatocellular carcinoma. Int J Appl Pharm Sci Res 6:156–163

    CAS  Google Scholar 

  • Motulsky HJ (1999) Analyzing data with GraphPad Prism. GraphPad Software Inc., San Diego CA www.graphpad.com

    Google Scholar 

  • Naima Z, Howaida I, Hanan FA, Mantawi NI (2014) CCL4-induced hepato nephrotoxicity: protective effect nutraceuticals on inflammatory factors and antioxidant status in rats. J Appl Pharm Sci 4(2):87–90

    Google Scholar 

  • Nema AK, Abhinav A, Varsha K (2011) Hepatoprotective activity of Leptadenia reticulata stems against carbon tetrachloride-induced hepatotoxicity in rats. Indian J Pharm 43:254–257

    Google Scholar 

  • Olajugbagbe ET, Odukoya ASO, Omafuvbel BO (2020) Evaluation of the effects of Pediococcus acidilactici isolated from Wara, a Nigerian milk product, in the prevention of diarrhea and the modulation of intestinal microflora in Wistar rats. Asian J Med Health 18(9):94–106

    Google Scholar 

  • Oumeddour A, Zaroure D, Haroun R, Zaimeche R, Riane K, Sifour M, Tahraou (2019) Protective effects of propolis and probiotic Lactobacillus acidophilus against carbon tetrachloride-induced hepatotoxicity in rats. Pharm Sci 25(3):190–197. https://doi.org/10.15171/PS.2019.36

    Article  Google Scholar 

  • Park SW, Lee CH, Kim YS et al (2008) Protective effect of baicalin against carbon tetrachloride-induced acute hepatic injury in mice. J Pharmacol Sci 106:136–143

    CAS  Google Scholar 

  • Pezzilli R (2009) Chronic pancreatitis: maldigestion, intestinal ecology and intestinal inflammation. World J Gastroenterol 15:1673–1676

    CAS  Google Scholar 

  • Plaa GL (2000) Chlorinated methanes and liver injury: highlights of the past 50 years. Annu Rev Pharmacol Toxicol 40:42–65

    CAS  Google Scholar 

  • Pradhan SC, Griish C (2006) Hepatoprotective herbal drug, silymarin from experimental pharmacology to clinical medicine. Indian J Med Res 124:491–504

    CAS  Google Scholar 

  • Rahmat AA, Dar FA, Choudhary IM (2014) Protection of CCl4-induced liver and kidney damage by phenolic compounds in leaf extracts of Cnestis ferruginea (de Candolle). Pharm Res 6:19–28

    Google Scholar 

  • Salatin SM, Marghani BH, El-Adl M, Salama MF (2019) Effect of diethyl nitrosamine and carbon tetrachloride induced hepatotoxicity in obese rats. Alex J Vet Sci 63(2):132–141

    Google Scholar 

  • Salvemini D, Botting R (1993) Modulation of platelet function by free radicals and free radical scavengers. TIPS 14:36–42

    CAS  Google Scholar 

  • Schermer S (1967) In: Davis FA (ed) The blood morphology of laboratory animals, third edn. Davis Co. Pub, Philadelphia, pp 10–42

  • Scholten D, Trebicka J, Liedtke C, Weiskirchen R (2015) The carbon tetrachloride model in mice. Lab Anim 49(S1):4–11

    CAS  Google Scholar 

  • Searle AJ, Wilson RL (1980) Glutathione peroxidase: effect of superoxide, hydroxyl and bromine free radicals on enzymic activity. Int J Radiat Biol 37:213

    CAS  Google Scholar 

  • Sharpe ME (1979) Identification of lactic acid bacteria. In: Skinner FA, Lovelock DW (eds) Identification methods for microbiologists. Academic Press, London

    Google Scholar 

  • Södergren E, Cederberg J, Vessby B, Basum S (2001) Vitamin E reduces lipid peroxidation in experimental hepatotoxicity in rats. Eur J Nutr 40(1):10–16. https://doi.org/10.1007/pl00007381

    Article  Google Scholar 

  • Tezel BU (2019) Preliminary in-vitro evaluation of the probiotic potential of the bacteriocinogenic strain Enterococcus lactis PMD74 isolated from ezine cheese. J Food Qual 1–12

  • Thompson M, Jaiswal Y, Wang I, Williams L (2017) Hepatotoxicity: treatment, causes and applications of medicinal plants as therapeutic agents. J.Phytopharmacol. 6(3):186–193

    Google Scholar 

  • Tilak KS, Veeraiah K, Reju MP (2007) Effects of ammonia, nitrite, and nitrate on hemoglobin content oxygen consumption of freshwater fish, Cyprinuscarplo (Linnaeus). J Envron Biol 28(1):45–47

    CAS  Google Scholar 

  • Van Bezooijen CF, Grell T, Knook DL (1977) The effect of age on protein synthesis by isolated liver parenchymal cells. Mech Ageing Dev 6:293–304

    Google Scholar 

  • Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Wang Y, Li W (2017) Antioxidant properties of probiotic bacteria. Nutrients 9:521

    Google Scholar 

  • Weber LW, Boll M, Stampfl A (2003) Hepatotoxicity and mechanism of action of halokanes: carbon tetrachloride as a toxicological model. Crit Rev Toxicol 33(2):105–136

    CAS  Google Scholar 

  • Williamson EM, Okpako DT, Evans FJ (1996) Pharmacological methods in phytotherapy research: selection, preparation and pharmacological evaluation of plant material, vol 1. JohnWiley & Sons, Chichester

    Google Scholar 

  • Wong F, Salerno F (2010)Beta-blockers in cirrhosis: friend and foe. Hepatology 52:811–813

    Google Scholar 

  • Yan H, Harhding JJ (1997)Glycation-induced inactivation and loss of antigenicity of catalase and superoxide dismutase. Biochem J 328(Pt 2):599–605. https://doi.org/10.1042/bj3280599

    Article  CAS  Google Scholar 

  • Yeung AW K, Tzvetkov NT, El-Tawil OS, Bungǎu SG, Abdel-Daim MM, Atanasov AG (2019) Antioxidants: scientific literature landscape analysis. Oxidative Med Cell Longev 8278454:1–11

  • Youssef EA, Amin AM, Kazem AH, Hassan SM, Khalil EM (2010) Effect of silymarin on liver injury induced by carbon tetrachloride in rats: histopathological and immunohistochemical studies. Egypt J Exp Biol (Zool) 6(1):107–115

    Google Scholar 

  • Zagato E, Milet E, Massimiliano L, Fasano F, Budelli A, Penna G, Rescigno M (2014)Lactobacillus paracasei CBA L74: metabolic products and fermented milk for infant formula have anti-inflammatory activity on dendritic cells in vitro and protective effects against colitis and an enteric pathogen in vivo. PLoS One 9:1–14

    Google Scholar 

  • Zerin M, Karakilcik AZ, Nazligul Y, Bitiren M, Ozardali HI, Musa D (2004) Protective role of Nigella sativa oil on experimental liver injury in rats. Turkiye Klinikleri J Med Sci 24:598–602

    CAS  Google Scholar 

  • Zhang S, Li D, Tian K, Bai Y, Zhang H, Song C, Qiao M, Kong D, Yu Y (2009) Development of a recombinant ureolytic Lactococcus lactis for urea removal. Artif Cells Blood Substit Immobil Biotechnol 37:227–234

    CAS  Google Scholar 

  • Zhao XY, Wang BE, Wang TL (2006) Inhibitory effect of silymarin on hepatic fibrosis induced by dimethylnitrosamine: experimental with rats. Zhonghua Yi Xue Za Zhi NCBI J 86(36):2563–2566

    CAS  Google Scholar 

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Acknowledgements

We thank Dr. Khaled M. A. Hassanein Prof of Pathology and Clinical Pathology, Faculty of Vet. Med. Director of Electron Microscope Unit, Assiut University, where he helped us in the histopathological examination, lesion scoring, writing, and photographed the histopathology.

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Authors and Affiliations

  1. Department of Dairy Science, Faculty of Agriculture, Minia University, El-Minia, Egypt

    Maha M. Bikheet

  2. Department of Agricultural Chemistry, Faculty of Agriculture, Minia University, El-Minia, Egypt

    Magda E. Mahmoud, Eman E. Yassien & Hanaa M. Hassan

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  1. Maha M. Bikheet
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  2. Magda E. Mahmoud
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  3. Eman E. Yassien
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  4. Hanaa M. Hassan
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Contributions

Maha M. Bikheet: data curation, writing—original draft preparation, and methodology; Magda E. Mahmoud: visualization, software, data curation, methodology, and investigation; Eman E. Yassien: methodology, software, and validation; Hanaa M. Hassan: conceptualization, investigation, methodology, formal analysis, data curation, writing (original draft preparation), writing (review and editing), and visualization.

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Correspondence to Hanaa M. Hassan.

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Bikheet, .M., Mahmoud, M.E., Yassien, E.E. et al. Effect of lactic acid bacteria isolated from some fermented dairy products on carbon tetrachloride-induced hepatotoxicity and nephrotoxicity of albino rats. Environ Sci Pollut Res 29, 11790–11800 (2022). https://doi.org/10.1007/s11356-021-16524-4

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