Research Article | Volume: 9, Supplement 1, March, 2019

A natural approach to control induced fumonisin B1-histopathological nephrotoxic and hepatotoxic changes in rats

Ashraf A Khalil Ashgan Abou Gabal Amira A Abdellatef Noha M Zahran Sahar F Deraz   

Open Access   

Published:  Mar 08, 2019

DOI:  10.7324/JAPS.2019.S103
Abstract

Among liver and kidney diseases, mycotoxin contamination of feed has become a major concern in animal feed science. A case control study was conducted to evaluate the recovery efficiency of lactic acid bacteria on serum lipid profile parameters and histopathological changes of nephrotoxic and hepatotoxic mycotoxin fumonisin B1 (FB1)- induced toxicity in kidney and liver of rats. Eighteen rats were randomly assigned to 12 experimental groups fed various doses of FB1 and/or co-administrated Lactobacillus delbrueckii subsp. lactis DSM 20076 (LL-DSM) and Pediococcus acidilactici NNRL B-5627 (PA-NNRL) for a period of 28 days. After 2 weeks, no significant signs of toxicity in rats fed FB1 alone or co-administrated with LAB were observed. Treatments of LL-DSM and/or PA-NNRL had no effect on organs weight, lipid profile, and histopathological examination of kidney and liver tissues along the experimental period. After 4 weeks, low-density lipoprotein-cholesterol, very low-density lipoprotein-cholesterol, triglycerides and total cholesterol were significantly increased, however the HDL-C, kidney and liver weights were significantly decreased in animals fed FB1 at doses tested. In the same line, the histopathological examination of livers and kidneys showed a series of morphological alterations in animals fed FB1, especially at the high dose (T200). Administration of LAB resulted in a significant improvement in all treatments tested as well as the histopathological patterns of liver and kidney tissues. Thus, using either LL-DSM or PA-NNRL strains could potentially expand another choice for safeguard application against immunotoxicities induced by fumonisins in many farm animal species that face inattentive exposition to this class of mycotoxins in their feedstuff.


Keyword:     Histopathology lipid profile hepatotoxicity nephrotoxicity fumonisins LAB detoxification.


Citation:

Khalil AA, Gabal AA, Abdellatef AA, Zahran NM, Deraz SF. A natural approach to control induced fumonisin B1- histopathological nephrotoxic and hepatotoxic changes in rats. J Appl Pharm Sci, 2019; 9(S1):017–029.

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Reference

Abdel-Wahhab M, Amer H, Hassan N, Hassan A, Naguib K. Effects of garlic and cabbage extracts on fuminisin-induced toxicity in rats. J Egypt Soc Toxicol, 2002; 26:1–12.

Abdel-Wahhab MA, Hassan AM, Amer HA, Naguib KM. Prevention of fumonisin-induced maternal and developmental toxicity in rats by certain plant extracts. J App Toxicol, 2004; 24:469–74. https://doi.org/10.1002/jat.1000

Aliabadi MA, Alikhani FE, Mohammadi M, Darsanaki RK. Biological control of aflatoxins. Eur J Exp Biol, 2013; 3:162–6.

Allain CC, Poon LS, Chan CS, Richmond W, Fu PC. Enzymatic determination of total serum cholesterol. Clin Chem, 1974; 20:470–5.

Ben Salah-Abbès J, Jebali R, Sharafi H, Noghabi KA, Oueslati R, Abbès S. Immuno-physiological alterations from AFB1 in rats counteracted by treatments with Lactobacillus paracasei BEJ01 and montmorillonite clay mixture. J Immunotoxicol, 2016; 13:628–37. https://doi.org/10.3109/1547691X.2016.1145157

Bennett J. Mycotoxins, mycotoxicoses, mycotoxicology and mycopathologia. Mycopathologia, 1987; 100:3–5. https://doi.org/10.1007/BF00769561

Bondy G, Barker M, Mueller R, Fernie S, Miller JD, Armstrong C, Hierlihy SL, Rowsell P, Suzuki C. Fumonisins B1 toxicity in male Sprague-Dawley rats. In: Jackson LS, De Vries JW, Bullerman LB (eds.). Fumonisins in food (advances in experimental medicine and biology). Plenum Press, New York, pp 251–64, . https://doi.org/10.1007/978-1-4899-1379-1_22

Bondy GS, Suzuki CAM, Mueller RW, Fernie SM, Armstrong CL, Hierlihy SL, Savard ME, Barker MG. Gavage administration of the fungal toxin fumonisin B1 to female Sprague-Dawley rats. J Toxicol Environ Health, 1998; 53:135–51. https://doi.org/10.1080/009841098159411

Bucolo G, David H. Quantitative determination of serum TGs by the use of enzymes. Clin Chem, 1973; 19:476–82.

Bulder AS, Arcella D, Bolger M, Carrington C, Kpodo K, Resnik S, Riley RT, Wolterink G, Wu F. Fumonisins (addendum). In: World Health Organization (ed.). Safety evaluation of certain food additives and contaminants, WHO Food Additives Series 65, WHO, Geneva, pp 325–794, 2012.

Burstein M, Samaille J. On a rapid determination of the cholesterol bound to the serum alpha-and beta-lipoproteins. Clin Chim Acta, 1960; 5:609 (in French). https://doi.org/10.1016/0009-8981(60)90075-9

Connerty HV, Briggs AR, Eaton Jr EH. Determination of serum, phospholipids, lipid phosphorous. In: Varley H (ed.). Practical clinical biochemistry, CBS Publishers, India, pp 319–20, 1961.

Dang HA, Zsolnai A, Kovacs M, Bors I, Bonal A, Bota B, Szabo-Fodor J. In vitro interaction between fumonisin B1 and the intestinal microflora of pigs. Pol J Microbiol, 2017; 66, 245–50. https://doi.org/10.5604/01.3001.0010.7858

Domijan AM, Peraica M, Vrdoljak AL, Radić B, Žlender V, Fuchs R. The involvement of oxidative stress in ochratoxin A and fumonisin B1 toxicity in rats. Mol Nutr Food Res, 2007; 51:1147–51. https://doi.org/10.1002/mnfr.200700079

Eknoyan G, Lameire N, Eckardt K, Kasiske B, Wheeler D, Levin A, Stevens P, Bilous R, Lamb E, Coresh J. Kidney disease: improving global outcomes (KDIGO) CKD work group. KDIGO 2012 clinical practice guideline for the evaluation and management of chronic kidney disease. Kidney Int, 2013; 3:5–14.

El-Nekeety AA, El-Kholy W, Abbas NF, Ebaid A, Amra HA, AbdelWahhab MA. Efficacy of royal jelly against the oxidative stress of fumonisin in rats. Toxicon, 2007; 50:256–69. https://doi.org/10.1016/j.toxicon.2007.03.017

El-Nezami H, Kankaanpää P, Salminen S, Ahokas J. Ability of dairy strains of lactic acid bacteria to bind a common food carcinogen, aflatoxin B1. Food Chem Toxicol, 1998; 36:321–6. https://doi.org/10.1016/S0278-6915(97)00160-9

El-Nezami H, Mykkanen H, Kankaanpaa P, Suomalainen T, Salminen S, Ahokas J. Ability of a mixture of Lactobacillus and Propionibacterium to influence the faecal aflatoxin content in healthy Egyptian volunteers: a pilot clinical study. Bioscience Microflora, 2000; 19:41–5.Enongene EN, Sharma RP, Bhandari N, Voss KA, Riley RT. Disruption of sphingolipid metabolism in small intestines, liver and kidney of mice dosed subcutaneously with fumonisin B1. Food Chem Toxicol, 2000; 38:793–9.

Fodor J, Meyer K, Gottschalk C, Mamet R, Kametler L, Bauer J, Horn P, Kovács F, Kovács M. In vitro microbial metabolism of fumonisin B1. Food Addit Contam, 2007; 24:416–20. https://doi.org/10.1080/02652030701216461

Fodor J, Meyer K, Riedlberger M, Bauer J, Pósa R, Horn P, Kovács F, Kovács M. Distribution and elimination of fumonisin analogues in weaned piglets after oral administration of Fusarium verticillioides fungal culture. Food Addit Contam, 2006; 23:492–501. https://doi.org/10.1080/02652030500544964

Forones N, Falcao J, Mattos D, Barone B. Cholesterolemia in colorectal cancer. Hepato-gastroenterol, 1997; 45:1531–4.

Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem, 1972; 18:499–502.

Gelderblom WC, Abel S, Smuts CM, Marnewick J, Marasas WF, Lemmer ER, Ramljak D. Fumonisin-induced hepatocarcinogenesis: mechanisms related to cancer initiation and promotion. Environ Health Perspect, 2001; 109:291–300.

Gelderblom WCA, Cawood ME, Snyman SD, Marasas WFO. Fumonisin B1 dosimetry in relation to cancer initiation in rat liver. Carcinogenesis, 1994; 15:209–14. https://doi.org/10.1093/carcin/15.2.209

Gelderblom WCA, Snyman SD, Lebepe-Mazur S, van der Westhuizen L, Kriek NPJ, Marasas WFO. The cancer-promoting potential of fumonisin B1 in rat liver using diethylnitrosamine as a cancer initiator. Cancer Lett, 1996; 109:101–8. https://doi.org/10.1016/S0304-3835(96)04431-X

Gratz S. Aflatoxin binding by probiotics. Experimental studies on intestinal aflatoxin transport, metabolism and toxicity. PhD Thesis, University of Kuopio, Finland, 2007.

Gratz S, Täubel M, Juvonen R, Viluksela M, Turner P, Mykkänen H, ElNezami H. Lactobacillus rhamnosus strain GG modulates intestinal absorption, fecal excretion, and toxicity of aflatoxin B1 in rats. App Environ Microbiol, 2006; 72:7398–400. https://doi.org/10.1128/AEM.01348-06

Halász A, Lásztity R, Abonyi T, Bata Á. Decontamination of mycotoxin-containing food and feed by biodegradation. Food Rev Int, 2009; 25:284–98. https://doi.org/10.1080/87559120903155750

Hard GC, Howard PC, Kovatch RM, Bucci TJ. Rat kidney pathology induced by chronic exposure to fumonisin B1 includes rare variants of renal tubule tumor. Toxicologic pathol, 2001; 29:379–86. https://doi.org/10.1080/019262301316905345

Haskard C, Binnion C, Ahokas J. Factors affecting the sequestration of aflatoxin by Lactobacillus rhamnosus strain GG. Chem Biol Interact, 2000; 128:39–49. https://doi.org/10.1016/S0009-2797(00)00186-1

Hathout AS, Mohamed SR, El-Nekeety AA, Hassan NS, Aly SE, Abdel-Wahhab MA. Ability of Lactobacillus casei and Lactobacillus reuteri to protect against oxidative stress in rats fed aflatoxins-contaminated diet. Toxicon, 2011; 58:179–86. https://doi.org/10.1016/j.toxicon.2011.05.015

Howard PC, Warbritton A, Voss KA, Lorentzen RJ, Thurman JD, Kovach RM, Bucci TJ. Compensatory regeneration as a mechanism for renal tubule carcinogenesis of fumonisin B1 in the F344/N/Nctr BR rat. Environ Health Perspect, 2001; 109:309–14. https://doi.org/10.1289/ehp.01109s2309

Juma KK, Fulakeza RMJ, Ngeranwa JN, Ngugi MP, Mburu ND. Evidence based phytopharmacological potential of herbal extracts in post-ingestion management of mycotoxins in animal models. J Clin Toxicol, 2015; 5:260–8.

Kankaanpää P, Tuomala E, El-Nezami H, Ahokas J, Salminen SJ. Binding of aflatoxin B1 alters the adhesion properties of Lactobacillus rhamnosus strain GG in a Caco-2 model. J Food Prot, 2000; 63:412–4. https://doi.org/10.4315/0362-028X-63.3.412

Karabela SP, Kairi CA, Magkouta S, Psallidas I, Moschos C, Stathopoulos I, Zakynthinos SG, Roussos C, Kalomenidis I, Stathopoulos GT. Neutralization of tumor necrosis factor bioactivity ameliorates urethaneinduced pulmonary oncogenesis in mice. Neoplasia, 2011; 13:1143–51. https://doi.org/10.1593/neo.111224

Khalil AA, Abou-Gabal AE, Abdellatef AA, Khalid AE. Protective role of probiotic lactic acid bacteria against dietary fumonisin B1-induced toxicity and DNA-fragmentation in sprague-dawley rats. Prep Biochem Biotechnol, 2015; 45:530–50. https://doi.org/10.1080/10826068.2014.940969

Khalil AA, Abou-Gabal AE, Elfaramawy AM, Khaled AE, Abdellatef AA. Lactic acid bacteria as antimycotic and antimycotoxins agents against toxigenic Fusarium species Associated to maize grains stored in Egyptian markets. J Pure App Microbiol, 2013; 7:93–105.

Kumar M, Verma V, Nagpal R, Kumar A, Behare PV, Singh B, Aggarwal PK. Anticarcinogenic effect of probiotic fermented milk and chlorophyllin on aflatoxin-B1-induced liver carcinogenesis in rats. Br J Nutr, 2012; 107:1006–16. https://doi.org/10.1017/S0007114511003953

Lillie R, Pasternack J, Gabe M. Techniques histologiques. Masson et Cie, Paris, p 249, 1968.

Long XD, Huang HD, Huang XY, Yao JG, Xia Q. XPC codon 939 poly-morphism is associated with susceptibility to DNA damage induced by AFB1 exposure. Int J Clin Exp Med, 2015; 8:1197–204.

Magan N, Olsen M. Mycotoxins in food: detection and control. Woodhead Publishing Limited, Sawston, UK, 2004.

Marasas WF, Riley RT, Hendricks KA, Stevens VL, Sadler TW, Gelineau-van Waes J, Missmer SA, Cabrera J, Torres O, Gelderblom WC, Allegood J, Martinez C, Maddox J, Miller JD, Starr L, Sullards MC, Roman AV, Voss KA, Wang E, Merrill Jr AH. Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr, 2004; 134:711–6. https://doi.org/10.1093/jn/134.4.711

Marin S, Ramos A, Cano-Sancho G, Sanchis V. Mycotoxins: occurrence, toxicology, and exposure assessment. Food Chem Toxicol, 2013; 60:218–37. https://doi.org/10.1016/j.fct.2013.07.047

Merrill AH, Jr Schmelz EM, Dillehay DL, Spiegel S, Shayman JA, Schroeder JJ, Riley RT, Voss KA, Wang E. Sphingolipids — the enigmatic lipid class: biochemistry, physiology, and pathophysiology. Toxicol Appl Pharmacol, 1997; 42:208–25. https://doi.org/10.1006/taap.1996.8029

Merrill AH, Jr Sullards MC, Wang E, Voss KA, Riley RT. Sphingolipid metabolism: roles in signal transduction and disruption by fumonisins. Environ Health Perspect, 2001; 109:283–9.

Mouline B, Ollier S, Olmer M. Disturbances of lipid metabolism during nephrotic syndrome. Nephrol, 1992; 13:193–9.

Müller S, Dekant W, Mally A. Fumonisin B1 and the kidney: modes of action for renal tumor formation by fumonisin B1 in rodents. Food Chem Toxicol, 2012; 50:3833–46. https://doi.org/10.1016/j.fct.2012.06.053

Nada S, Amra H, Deabes M, Omara E. Saccharomyces Cerevisiae and probiotic bacteria potentially inhibit aflatoxins production in vitro and in vivo studies. Int J Toxicol, 2010; 8:32.

Niderkorn V, Boudra H, Morgavi D. Binding of Fusarium mycotoxins by fermentative bacteria in vitro. J App Microbiol, 2006; 101:849–56. https://doi.org/10.1111/j.1365-2672.2006.02958.x

Niderkorn V, Morgavi DP, Aboab B, Lemaire M, Boudra H. Cell wall component and mycotoxin moieties involved in the binding of fumonisin B1 and B2 by lactic acid bacteria. J Appl Microbiol, 2009; 106:977–85. https://doi.org/10.1111/j.1365-2672.2008.04065.x

NTP. Toxicology and carcinogenesis studies of fumonisin B1 (CAS No. 116355-83-0) in F344/N rats and B6C3F1 mice (Feed Studies). Natl Toxicol Program Tech Rep Ser, 2001; 496:1–352.

Oatley JT, Rarick MD, Ji GE, Linz JE. Binding of aflatoxin B1 to Bifidobacteria in vitro. J Food Prot, 2000; 63:1133–6. https://doi.org/10.4315/0362-028X-63.8.1133

Pereira P, Nesci A, Etcheverry M. Effects of biocontrol agents on Fusarium verticillioides count and fumonisin content in the maize agroecosystem: impact on rhizospheric bacterial and fungal groups. Biol control, 2007; 42:281–7. https://doi.org/10.1016/j.biocontrol.2007.05.015

Pizzolitto R, Armando M, Salvano M, Dalcero A, Rosa C. Evaluation of Saccharomyces cerevisiae as an antiaflatoxicogenic agent in broiler feedstuffs. Poult sci, 2013; 92:1655–63. https://doi.org/10.3382/ps.2012-02846

Placinta C, D'mello J, Macdonald AA. Review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins. Anim feed sci technol, 1999; 78:21–37. https://doi.org/10.1016/S0377-8401(98)00278-8

Ramesh G. Symptoms, diagnosis, and pathophysiology of mycotoxin exposure. Murray State University, Hopkinsville, Kentucky, 2012.

Reddy K, Farhana N, Salleh B, Oliveira C. Microbiological control of mycotoxins: present status and future concerns. Cur Res Technol Edu Topics App Microbiol Microbial Biotechnol, 2010; 2:1078–86.

Richmond W. Preparation and properties of a cholesterol oxidase from Nocardia sp. and its application to the enzymatic assay of total cholesterol in serum. Clin Chem, 1973; 19:1350–6.

Riley RT, Enongene E, Voss KA, Norred WP, Meredith FI, Sharma RP, Spitsbergen J, Williams DE, Carlson DB, Merrill Jr AH. Sphingolipid perturbations as mechanisms for fumonisin carcinogenesis. Environ Health Perspect, 2001; 109:301–8.

Riley RT, Hinton DM, Chamberlain WJ, Bacon CW, Wang E, Merrill Jr AH, Voss KA. Dietary fumonisin B1 induces disruption of sphingolipid metabolism in Sprague–Dawley rats: a new mechanism of nephrotoxicity. J Nutr, 1994; 124:594–603. https://doi.org/10.1093/jn/124.4.594

Sartori M, Nesci A, Castillo C, Etcheverry M. Biological control of fumonisins production in maize at field level. Int J Agric Policy Res, 2013; 1:188–96.

Sezer C, Guven A, Bilge Oral N, Vatansever L. Detoxification of aflatoxin B1 by bacteriocins and bacteriocinogenic lactic acid bacteria. Turk J Vet Anim Sci, 2013; 37:594–601. https://doi.org/10.3906/vet-1301-31

Sharma RP, Dugyala RR, Voss KA. Demonstration of in-situ apoptosis in mouse liver and kidney after short-term repeated exposure to fumonisin B1. J comp Pathol, 1997; 117:371–81. https://doi.org/10.1016/S0021-9975(97)80084-9

Shephard GS, Thiel PG, Sydenham EW, Savard ME. Fate of a single dose of 14C labelled fumonisin B1 in vervet monkeys. Nat Toxins, 1995; 3:145–50. https://doi.org/10.1002/nt.2620030305

Shephard GS, Thiel PG, Sydenham EW, Vleggaar R, Alberts JF. Determination of the mycotoxin fumonisin B1 and identification of its partially hydrolysed metabolites in the faeces of non-human primates. Food Chem Toxicol, 1994; 32:23–9. https://doi.org/10.1016/0278-6915(84)90032-2

Shetty PH, Jespersen L. Saccharomyces cerevisiae and lactic acid bacteria as potential mycotoxin decontaminating agents. Trends Food Sci Technol, 2006; 17:48–55. https://doi.org/10.1016/j.tifs.2005.10.004

Stiles J, Bullerman L. Inhibition of Fusarium species and mycotoxin production by Bacillus pumilus NEB1 and Lactobacillus rhamnosus VT1. 13th International Reinhardsbrunn Symposium, Modern Fungicides and Antifungal Compounds III Agro Concept GmbH, Germany, 2002.

Tsitsigiannis DI, Dimakopoulou M, Antoniou PP, Tjamos EC. Biological control strategies of mycotoxigenic fungi and associated mycotoxins in Mediterranean basin crops. Phytopathol Mediterr, 2012; 51:158–74.

Tsunoda M, Shanna RP, Riley RT. Early fumonisin B1, toxicity in relation to disrupted sphingolipid metabolism in male BALB/c mice. J Biochem Mol Toxicol, 1998; 12:281–9. https://doi.org/10.1002/(SICI)1099-0461(1998)12:5<281::AID-JBT4>3.0.CO;2-H

Vinderola G, Ritieni A. Role of probiotics against mycotoxins and their deleterious effects. J Food Res, 2014; 4:10–21. https://doi.org/10.5539/jfr.v4n1p10

Voss K, Smith G, Haschek W. Fumonisins: toxicokinetics, mechanism of action and toxicity. Anim Feed Sci Technol, 2007; 137:299–325. https://doi.org/10.1016/j.anifeedsci.2007.06.007

Voss KA, Chamberlain WJ, Bacon CW, Herbert RA, Walters DB, Norred WP. Subchronic feeding study of the mycotoxin fumonisin B1 in B6C3F1 mice and Fischer 344 rats. Fundam App Toxicol, 1995; 24:102–10. https://doi.org/10.1006/faat.1995.1012

Voss KA, Riley RT, Norred WP, Bacon CW, Meredith FI, Howard PC, Plattner RD, Collins TF, Hansen DK, Porter JK. An overview of rodent toxicities: liver and kidney effects of fumonisins and Fusarium moniliforme. Environ Health Perspect, 2001; 109:259–66.

WHO. Fumonisin B1, environmental health criteria 219. International Programme on Chemical Safety, World Health Organization, Geneva, 2000.

WHO. Evaluation of certain mycotoxins in food. WHO technical report series No. 906, Fifty-sixth Report of the Joint FAO/WHO Expert Committee on Food Additives, World Health Organization, Geneva, 2002.

Williams JH, Phillips TD, Jolly PE, Stiles JK, Jolly CM, Aggarwal D. Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions. Am J Clin Nutr, 2004; 80:1106–22. https://doi.org/10.1093/ajcn/80.5.1106

Wu F, Munkvold GP. Mycotoxins in ethanol co-products: modeling economic impacts on the livestock industry and management strategies. J Agric Food Chem, 2008; 56:3900–11. https://doi.org/10.1021/jf072697e

Yang YS, Ahn TH, Lee JC, Moon CJ, Kim SH, Jun W, Park SC, Kim HC, Kim JC. Protective effects of Pycnogenol on carbon tetrachloride-induced hepatotoxicity in Sprague–Dawley rats. Food Chem Toxicol, 2008; 46:380–7.

Yin YN, Yan LY, Jiang JH, Ma ZH. Biological control of aflatoxin contamination of crops. J Zhejiang Univ Sci B, 2008; 9:787–92.

Zhang M, Fan X, Fang B, Zhu C, Zhu J, Ren F. Effects of Lactobacillus salivarius Ren on cancer prevention and intestinal microbiota in 1,2-dimethylhydrazine-induced rat model. J Microbiol, 2015; 53:398–405.

Zhang Y, Caupert J. A survey of mycotoxins in US distiller’s dried grains with solubles from 2009 to 2011. J Agric Food Chem, 2012; 60:539–43.

Zoghi A, Khosravi-Darani K, Sohrabvandi S. Surface binding of toxins and heavy metals by probiotics. Mini Rev Med Chem, 2014; 14:84–98.

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