In-vivo evaluation of the adverse effects of ochratoxin A on broiler chicken health and adsorption efficacy of indigenous and commercial clay of Balochistan, Pakistan

References

• Abdelrahman RE, Khalaf AAA, Elhady MA, Ibrahim MA, Hassanen EI, Noshy PA. 2022. Antioxidant and antiapoptotic effects of quercetin against ochratoxin A-induced nephrotoxicity in broiler chickens. Environ Toxico Pharma. 96:103982. doi: 10.1016/j.etap.2022.103982.
   PubMed Web of Science ®Google Scholar
• Abro MR. Rashid N, Khanoranga, Soomro RN, Siddique Z. 2024. Comparative Assessment of Thermal Treatment for Mycotoxins Adsorption Potential of Indigenous Clay from Balochistan, Pakistan. Pak. J. Anal. Chem. 25(1). 2. doi: 10.21743/pjaec/2024.06.03.
   Google Scholar
• Ali AEMA, Refat NA, Mowafy RE, Gaheen SA. 2017. Experimental pathological studies on ochratoxicosis in broiler chickens. Zagazig Vet J. 45:155–164. doi: 10.21608/zvjz.2019.28660.
   Google Scholar
• Ahmad MFUD, Saleemi MK, Khan MZ, Muhammad F, Khatoon A, Bhatti SA, Ahmed I. 2012. Effects of Ochratoxin A feeding in white leghorn cockerels on hematological and serum biochemical parameters and its amelioration with silymarin and vitamin E. Pak Vet J. 32(4).
   Web of Science ®Google Scholar
• Alford R, Mishael YG. 2023. Bi-functional clay-based sorbent for Ochratoxin A removal and wine fining. Food Chem. 416:135827. doi: 10.1016/j.foodchem.2023.135827.
   PubMed Web of Science ®Google Scholar
• Aloui A, Ben Salah-Abbes J, Zinedine A, Riba A, Durand N, Meile JC, Abbes S. 2023. Prevention and detoxification of mycotoxins in human food and animal feed using bio-resources from South Mediterranean countries: a critical review. Crit Rev Toxico. 1–14.
   PubMed Web of Science ®Google Scholar
• Aloui A, Ben Salah-Abbès J, Zinedine A, Riba A, Durand N, Meile JC, Montet D, Brabet C, Abbès S. 2023. Prevention and detoxification of mycotoxins in human food and animal feed using bio-resources from South Mediterranean countries: a critical review. Crit Rev Toxicol. 53(2):117–130. doi: 10.1080/10408444.2023.2211178.
   PubMed Web of Science ®Google Scholar
• Assunção R, Silva MJ, Alvito P. 2016. Challenges in risk assessment of multiple mycotoxins in food. WMJ. 9(5):791–812. doi: 10.3920/WMJ2016.2039.
   Google Scholar
• Battacone G, Nudda A, Pulina G. 2010. Effects of Ochratoxin A on livestock production. Toxins. 2(7):1796–1824. doi: 10.3390/toxins2071796.
   PubMed Web of Science ®Google Scholar
• Bisi-Johnson MA, Obi CL, Ekosse GE. 2010. Microbiological and health related perspectives of geophagia: an overview. Afr J Biotech. 9(36):5784.
   Google Scholar
• Bryła M, Pierzgalski A, Zapaśnik A, Uwineza PA, Ksieniewicz-Woźniak E, Modrzewska M, Waśkiewicz A. 2022. Recent research on Fusarium mycotoxins in maize—a review. Foods. 11(21):3465. doi: 10.3390/foods11213465.
   PubMed Web of Science ®Google Scholar
• Bryden WL. 2007. Mycotoxins in the food chain: human health implications. Asia Pac J Clin Nutr. 16(S1):95–101.
   PubMedGoogle Scholar
• Chen C, Cao J, Wang X, Chai Q, Zhang Y, Chen H, Zhu X, Pan Y, Liu J. 2022. A novel dual-flux immune chromatographic test strip based on luminescence resonance energy transfer for simultaneous detection of ochratoxin A and deoxynivalenol. Mikrochim Acta. 189(12):466. doi: 10.1007/s00604-022-05561-6.
   PubMed Web of Science ®Google Scholar
• Chilaka CA, Obidiegwu JE, Chilaka AC, Atanda OO, Mally A. 2022. Mycotoxin regulatory status in Africa: a decade of weak institutional efforts. Toxins (Basel). 14(7):442. doi: 10.3390/toxins14070442.
   PubMed Web of Science ®Google Scholar
• Chkuaseli A, Khutsishvili-Maisuradze M, Chagelishvili A, Natsvaladze K, Lashkarashvili T, Chagelishvili G, Maisuradze N. 2016. Application of new mycotoxin adsorbent-bentonite clay “Askangel” in poultry feed. Ann Agrar Sci. 14(4):295–298. doi: 10.1016/j.aasci.2016.09.004.
   Google Scholar
• Del Bianchi M, Oliveira CAFD, Albuquerque RD, Guerra JL, Correa B. 2005. Effects of prolonged oral administration of aflatoxin B1 and fumonisin B1 in broiler chickens. Poult Sci. 84(12):1835–1840. doi: 10.1093/ps/84.12.1835.
   PubMed Web of Science ®Google Scholar
• Ding L, Han M, Wang X, Guo Y. 2023. Ochratoxin A: overview of prevention, removal, and detoxification methods. Toxins (Basel). 15(9):565. doi: 10.3390/toxins15090565.
   PubMed Web of Science ®Google Scholar
• Daou R, Hoteit M, Bookari K, Joubrane K, Khabbaz LR, Ismail A, Maroun RG, El Khoury A. 2022. Public health risk associated with the co-occurrence of aflatoxin B1 and ochratoxin A in spices, herbs, and nuts in Lebanon. Front Public Health. 10:1072727. doi: 10.3389/fpubh.2022.1072727.
   PubMed Web of Science ®Google Scholar
• Elsaidy N, Mohamed RA, Abouelenien F. 2015. Assessment of variable drinking water sources used in Egypt on broiler health and welfare. Vet World. 8(7):855–864. doi: 10.14202/vetworld.2015.855-864.
   PubMedGoogle Scholar
• El-Nabarawy AM, Madian K, Shaheed IB, El-Ghany A. 2020. Comparative evaluation of different antimycotoxins for controlling mycotoxicosis in broiler chickens. JWPR. 10(2s):223–234. doi: 10.36380/jwpr.2020.28.
   Google Scholar
• El-Barkouky EM, Mohamed FR, Atta AM, Abu Taleb AM, El Menawey MA, Hatab MH. 2010. Effect of Saccharomyces cerevisiae and vitamin C supplementation on performance of broilers subjected to ochratoxin A contamination. Egyptian Poul Sci. 30(1):89–113.
   Google Scholar
• Elliott CT, Connolly L, Kolawole O. 2020. Potential adverse effects on animal health and performance caused by the addition of mineral adsorbents to feeds to reduce mycotoxin exposure. Mycotoxin Res. 36(1):115–126. doi: 10.1007/s12550-019-00375-7.
   PubMed Web of Science ®Google Scholar
• Feng S, Hua MZ, Roopesh MS, Lu X. 2023. Rapid detection of three mycotoxins in animal feed materials using competitive ELISA-based origami microfluidic paper analytical device. Anal Bioanal Chem. 415(10):1943–1951. doi: 10.1007/s00216-023-04612-y.
   PubMedGoogle Scholar
• Frangiamone M, Cimbalo A, Alonso-Garrido M, Vila-Donat P, Manyes L. 2022. In vitro and in vivo evaluation of AFB1 and OTA-toxicity through immunofluorescence and flow cytometry techniques: a systematic review. Food Chem Toxicol. 160:112798. doi: 10.1016/j.fct.2021.112798.
   PubMed Web of Science ®Google Scholar
• Gul A, Jahangeer M, Murtaza B, Ahmed J, Nadeem AA, Yongping X, Mehmood M. 2023. Different molds and their toxins: as contaminants in one health perspective. Vol. 2. FaisalabCad, Pakistan: One Health Triad, Unique Scientific Publishers; p. 231–241.
   Google Scholar
• Gillani S, Sadef Y, Imran M, Raza HMF, Ghani A, Anwar S, Hussain S. 2022. Determination and detoxification of aflatoxin and ochratoxin in maize from different regions of Pakistan. Environ Monitoring Assess. 194(9):613.
   PubMed Web of Science ®Google Scholar
• González-Curbelo MÁ, Kabak B. 2023. Occurrence of mycotoxins in dried fruits worldwide, with a focus on aflatoxins and ochratoxin a: a review. Toxins (Basel). 15(9):576. doi: 10.3390/toxins15090576.
   PubMed Web of Science ®Google Scholar
• Hamad GM, El-Makarem HSA, Allam MG, El Okle OS, El-Toukhy MI, Mehany T, El-Halmouch Y, Abushaala MMF, Saad MS, Korma SA, et al. 2023. Evaluation of the adsorption efficacy of bentonite on aflatoxin M1 levels in contaminated milk. Toxins (Basel). 15(2):107. doi: 10.3390/toxins15020107.
   PubMed Web of Science ®Google Scholar
• Hamed D, Elhalous D, Mohamed O, Elfeil W. 2023. Pathological studies on the effect of prebiotic and probiotic on aflatoxicosis in broiler chickens. Suez Canal Vet Medical J. 28(1):223–241. doi: 10.21608/scvmj.2023.307794.
   Google Scholar
• Hamad GM, Mehany T, Simal-Gandara J, Abou-Alella S, Esua OJ, Abdel-Wahhab MA, Hafez EE. 2023. A review of recent innovative strategies for controlling mycotoxins in foods. Food Control. 144:109350. doi: 10.1016/j.foodcont.2022.109350.
   Web of Science ®Google Scholar
• Huff WE, Wyatt RD, Hamilton PB. 1975. Nephrotoxicity of dietary ochratoxin A in broiler chikens. Appl Microbiol. 30(1):48–51. doi: 10.1128/am.30.1.48-51.1975.
   PubMedGoogle Scholar
• Imran M, Cao S, Wan SF, Chen Z, Saleemi MK, Wang N, Munawar J. 2020. Mycotoxins–a global one health concern: a review. Agrobiol Records. 2:1–16. doi: 10.47278/journal.abr/2020.006.
   Google Scholar
• Jalilzadeh-Amin G, Dalir-Naghadeh B, Ahmadnejad-Asl-Gavgani M, Fallah AA, Mousavi Khaneghah A. 2023. Prevalence and concentration of mycotoxins in animal feed in the Middle East and North Africa (MENA): a systematic review and meta-analysis. Toxins (Basel). 15(3):214. doi: 10.3390/toxins15030214.
   PubMed Web of Science ®Google Scholar
• Juraschek LM, Kappenberg A, Amelung W. 2022. Mycotoxins in soil and environment. Sci Total Environ. 814:152425. doi: 10.1016/j.scitotenv.2021.152425.
   PubMed Web of Science ®Google Scholar
• Khan SA, Awan K, Urooj A, Itano EN. 2023. Ochratoxin-A induced pathological changes in broiler chicks. PAB.), 12(4):1608–1616. doi: 10.19045/bspab.2023.120162.
   Google Scholar
• Khatoon A, Khan MZ, Khan A, Javed I. 2016. Toxicopathological and serum biochemical alterations induced by ochratoxin A in broiler chicks and their amelioration by locally available bentonite clay. Pakistan j of Agri Sci. 53(4).
   Web of Science ®Google Scholar
• Kihal A, Rodríguez-Prado M, Calsamiglia S. 2022. The efficacy of mycotoxin binders to control mycotoxins in feeds and the potential risk of interactions with nutrient: a review. J Ani Sci. 100(11):skac328.
   PubMed Web of Science ®Google Scholar
• Kőszegi T, Poór M. 2016. Ochratoxin A: molecular interactions, mechanisms of toxicity and prevention at the molecular level. Toxins. 8(4):111. doi: 10.3390/toxins8040111.
   PubMed Web of Science ®Google Scholar
• Koynarski V, Stoev S, Grozeva N, Mirtcheva T, Daskalov H, Mitev J, Mantle P. 2007. Experimental coccidiosis provoked by Eimeria acervulina in chicks simultaneously fed on ochratoxin A contaminated diet. Res Vet Sci. 82(2):225–231. doi: 10.1016/j.rvsc.2006.07.004.
   PubMed Web of Science ®Google Scholar
• Kumar P, KamLe M, Mahato DK. 2023. Mycotoxins in food and feed: detection and management strategies. Boca Raton: CRC Press.
   Google Scholar
• Lauwers M, Croubels S, Letor B, Gougoulias C, Devreese M. 2019. Biomarkers for exposure as a tool for efficacy testing of a mycotoxin detoxifier in broiler chickens and pigs. Toxins (Basel). 11(4):187. doi: 10.3390/toxins11040187.
   PubMed Web of Science ®Google Scholar
• Li XK, Wang JZ, Wang CQ, Zhang CH, Li X, Tang CH, Wei XL. 2016. Effect of dietary phosphorus levels on meat quality and lipid metabolism in broiler chickens. Food Chem. 205:289–296. doi: 10.1016/j.foodchem.2016.02.133.
   PubMed Web of Science ®Google Scholar
• Li Y, Tian G, Dong G, Bai S, Han X, Liang J, Meng J, Zhang H. 2018. Research progress on the raw and modified montmorillonites as adsorbents for mycotoxins: a review. Applied Clay Sci. 163:299–311. doi: 10.1016/j.clay.2018.07.032.
   Web of Science ®Google Scholar
• Lopes P, Sobral MMC, Lopes GR, Martins ZE, Passos CP, Petronilho S, Ferreira IM. 2023. Mycotoxins’ prevalence in food industry by-products: a systematic review. Toxins (Basel). 15(4):249. doi: 10.3390/toxins15040249.
   PubMed Web of Science ®Google Scholar
• Malekinezhad P, Ellestad L E, AfzaliN, Farhangfar SH, Omidi A, Mohammadi A 2021. Evaluation of berberine efficacy in reducing the effects of aflatoxin B1 and ochratoxin A added to male broiler rations. Poul Sci. 100(2), 797–809. doi: 10.1016/j.psj.2020.10.040.
   Google Scholar
• Marasas WF, Gelderblom WC, Shephard S, Vismer HF. 2008. Mycotoxins: a global problem. In: Mycotoxins: detection methods, management, public health and agricultural trade. Wallingford (UK): CABI; p. 29–39.
   Google Scholar
• Marc RA. 2022. Implications of mycotoxins in food safety. In: Mycotoxins and food safety-recent advances. Intech Open.
   Google Scholar
• Mukhtar K, Nabi BG, Ansar S, Bhat ZF, Aadil RM, Khaneghah AM. 2023. Mycotoxins and consumers’ awareness: recent progress and future challenges. Toxicon. 232:107227. doi: 10.1016/j.toxicon.2023.107227.
   PubMed Web of Science ®Google Scholar
• Nazarizadeh H, Mohammad Hosseini S, Pourreza J. 2019. Effect of plant extracts derived from thyme and chamomile on the growth performance, gut morphology and immune system of broilers fed aflatoxin B1 and ochratoxin A contaminated diets. Italian J of Ani Sci. 18(1):1073–1081. doi: 10.1080/1828051X.2019.1615851.
   Web of Science ®Google Scholar
• Nedeljković-Trailović J, Trailović S, Resanović R, Milićević D, Jovanovic M, Vasiljevic M. 2015. Comparative investigation of the efficacy of three different adsorbents against OTA-induced toxicity in broiler chickens. Toxins (Basel). 7(4):1174–1191. doi: 10.3390/toxins7041174.
   PubMed Web of Science ®Google Scholar
• Panichev AM, Baranovskaya NV, Seryodkin IV, Chekryzhov IY, Soktoev BR, Ivanov VV, Vakh EA, Desyatova TV, Lutsenko TN, Popov NY, et al. 2023. The main cause of geophagy according to extensive studies on Olkhon Island, Lake Baikal. Geosciences. 13(7):211. doi: 10.3390/geosciences13070211.
   Web of Science ®Google Scholar
• Patil RD, Degloorkar NM, Pawar PL. 2017. Effects of ochratoxin a feeding on organ weights and gross pathological changes in broiler chicken and its amelioration with Bantox®. J Poul Sci Tech. 5(4):44–51.
   Google Scholar
• Peivasteh-Roudsari L, Pirhadi M, Shahbazi R, Eghbaljoo-Gharehgheshlaghi H, Sepahi M, Mirza Alizadeh A, Tajdar-Oranj B, Jazaeri S. 2022. Mycotoxins: impact on health and strategies for prevention and detoxification in the food chain. Food Rev Intern. 38(sup1):193–224. doi: 10.1080/87559129.2020.1858858.
   Google Scholar
• Piotrowska M. 2021. Microbiological decontamination of mycotoxins: opportunities and limitations. Toxins (Basel). 13(11):819. doi: 10.3390/toxins13110819.
   PubMed Web of Science ®Google Scholar
• Phillips TD, Lemke SL, Grant PG. 2002. Characterization of clay-based enter sorbents for the prevention of aflatoxicosis. Adv Exp Med Biol. 504:157–171. doi: 10.1007/978-1-4615-0629-4_16.
   PubMed Web of Science ®Google Scholar
• Phillips TD, Wang M, Elmore SE, Hearon S, Wang JS. 2019. NovaSil clay for the protection of humans and animals from aflatoxins and other contaminants. Clays Clay Miner. 67(1):99–110. doi: 10.1007/s42860-019-0008-x.
   PubMed Web of Science ®Google Scholar
• Phillips TD, Afriyie-Gyawu E, Williams J, Huebner H, Ankrah N-A, Ofori-Adjei D, Jolly P, Johnson N, Taylor J, Marroquin-Cardona A, et al. 2008. Reducing human exposure to aflatoxin through the use of clay: a review. Food Addit Contam A Chem Anal Control Expo Risk Assess. 25(2):134–145. doi: 10.1080/02652030701567467.
   Web of Science ®Google Scholar
• Qu D, Huang X, Han J, Man N. 2017. Efficacy of mixed adsorbent in ameliorating ochratoxicosis in broilers fed ochratoxin A contaminated diets. Ital J Ani Sci. 16(4):573–579. doi: 10.1080/1828051X.2017.1302822.
   Web of Science ®Google Scholar
• Rodríguez-Rojas A, Rodríguez-Beltrán J, Valverde JR, Blázquez J. 2015. Can clays in livestock feed promote antibiotic resistance and virulence in pathogenic bacteria. Antibiotics. 4(3):299–308. doi: 10.3390/antibiotics4030299.
   Google Scholar
• Rovetto EI, Luz C, La Spada F, Meca G, Riolo M, Cacciola SO. 2023. Diversity of mycotoxins and other secondary metabolites recovered from blood oranges infected by colletotrichum, alternaria, and penicillium species. Toxins (Basel). 15(7):407. doi: 10.3390/toxins15070407.
   PubMed Web of Science ®Google Scholar
• Saleemi MK, Raza A, Khatoon A, Zubair M, Xu Y, Murtaza B, Basit A. 2023. Toxic effects of aflatoxin B1 on hematobiochemical and histopathological parameters of juvenile white leghorn male birds and their amelioration with vitamin E and Moringa oleifera. Pak Vet J.
   Web of Science ®Google Scholar
• Sharma M, Mandal A B, Singh R 2016. Effect of Aflatoxin, Ochratoxin and their interaction on growth performance, immunity and jejunal morphometry of broiler chickens. Indi. J.Poul. Sci, 51(3), 253–258. doi: 10.5958/0974-8180.2016.00056.8
   Google Scholar
• Sharma SK, Mandal TK, Jain S, Sharma A, Saxena M. Saraswati 2016. Source apportionment of PM 2.5 in Delhi, India using PMF model. Bull Environ Contam Toxicol. 97(2):286–293. doi: 10.1007/s00128-016-1836-1.
   PubMed Web of Science ®Google Scholar
• Sholikin MM, Irawan A, Sofyan A, Jayanegara A, Rumhayati B, Hidayat C, Adli DN, Julendra H, Herdian H, Manzila I, et al. 2022. A meta-analysis of the effects of clay mineral supplementation on alkaline phosphatase, broiler health, and performance. Poult Sci. 102(3):102456. doi: 10.1016/j.psj.2022.102456.
   PubMed Web of Science ®Google Scholar
• Singh R, Mandal AB, Sharma M, Biswas A. 2015. Effect of varying levels of dietary ochratoxin A on the performance of broiler chickens. Indian J Anim Sci. 85:296–300.
   Web of Science ®Google Scholar
• Tahir MA, Abbas A, Muneeb M, Bilal RM, Hussain K, Abdel-Moneim A-ME, Farag MR, Dhama K, Elnesr SS, Alagawany M. 2022. Ochratoxicosis in poultry: occurrence, environmental factors, pathological alterations and amelioration strategies. World’s Poult Sci J. 78(3):727–749. doi: 10.1080/00439339.2022.2090887.
   Web of Science ®Google Scholar
• Uyanga VA, Sun L, Liu Y, Zhang M, Zhao J, Wang X, Lin H. 2023. Effects of arginine replacement with L-citrulline on the arginine/nitric oxide metabolism in chickens: an animal model without urea cycle. J Ani Sci Biotech. 14(1):1–19.
   PubMed Web of Science ®Google Scholar
• Vlachou M, Pexara A, Solomakos N, Govaris A. 2023. Occurrence and contamination level of ochratoxin A in tissues of slaughtered pigs in Greece. Acta Vet Eurasia. 49(2):92–98. doi: 10.5152/actavet.2023.22104.
   Web of Science ®Google Scholar
• Vila-Donat P, Marín S, Sanchis V, Ramos AJ. 2018. A review of the mycotoxin adsorbing agents, with an emphasis on their multi-binding capacity, for animal feed decontamination. Food Chem Toxicol. 114:246–259. doi: 10.1016/j.fct.2018.02.044.
   PubMed Web of Science ®Google Scholar
• Watts CM, Chen YC, Ledoux DR, Broomhead JN, Bermudez AJ, Rottinghaus GE. 2003. Effects of multiple mycotoxins and a hydrated sodium calcium aluminosilicate in poultry. Int J Poultry Sci. 2(6):372–378. doi: 10.3923/ijps.2003.372.378.
   Google Scholar
• Wang L, Hua X, Shi J, Jing N, Ji T, Lv B, Liu L, Chen Y. 2022. Ochratoxin A: occurrence and recent advances in detoxification. Toxicon. 210:11–18. doi: 10.1016/j.toxicon.2022.02.010.
   PubMed Web of Science ®Google Scholar
• Wang M, Hearon SE, Phillips TD. 2020. A high capacity bentonite clay for the sorption of aflatoxins. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 37(2):332–341. doi: 10.1080/19440049.2019.1662493.
   PubMed Web of Science ®Google Scholar
• Więckowska M, Szelenberger R, Niemcewicz M, Harmata P, Poplawski T, Bijak M. 2023. Ochratoxin A—the current knowledge concerning hepatotoxicity, mode of action and possible prevention. Molecules. 28(18):6617. doi: 10.3390/molecules28186617.
   PubMed Web of Science ®Google Scholar
• Worker SB, Kielland K, Barboza PS. 2015. Effects of geophagy on food intake, body mass, and nutrient dynamics of snowshoe hares (Lepus americanus). Can J Zool. 93(4):323–329. doi: 10.1139/cjz-2014-0237.
   Google Scholar
• Yamini V, Iv TN. 2023. Effective bio-mediated nanoparticles for bioremediation of toxic metal ions from wastewater–a review. J. Environ Nanotechnol. 12(2):12–33.
   Google Scholar
• Yu J, Pedroso IR. 2023. Mycotoxins in cereal-based products and their impacts on the health of humans, livestock animals and pets. Toxins (Basel). 15(8):480. doi: 10.3390/toxins15080480.
   PubMed Web of Science ®Google Scholar
• Zheng X, Xia F, Li J, Zheng L, Rao S, Gao L, Yang Z. 2023. Reduction of ochratoxin A from contaminated food by Lactobacillus rhamnosus Bm01. Food Control. 143:109315. doi: 10.1016/j.foodcont.2022.109315.
   Web of Science ®Google Scholar