1. bookAHEAD OF PRINT
Journal Details
License
Format
Journal
First Published
25 Nov 2011
Publication timeframe
4 times per year
Languages
English
access type Open Access

Protective effects of non-encapsulated and microencapsulated Lactobacillus delbrueckii subsp. bulgaricus in rainbow trout (Oncorhynchus mykiss) exposed to lead (Pb) via diet

Published Online: 29 May 2021
Page range: -
Received: 15 Jan 2021
Accepted: 15 Apr 2021
Journal Details
License
Format
Journal
First Published
25 Nov 2011
Publication timeframe
4 times per year
Languages
English
Abstract

The present study was designed to investigate the effects of dietary non-encapsulated and microencapsulated Lactobacillus delbrueckii subsp. bulgaricus on growth performance, intestinal enzymatic activities, antioxidant capacity and hepato-biochemical parameters of rainbow trout before or after exposure to lead via diet. Fingerling fish (16 ± 4 g) were divided into four groups: negative control (NC), positive control (PC), probiotic (PR) and encapsulated probiotic (EN-PR). During the pre-exposure period (days 0-45), fish in the NC and PC groups received the basal diet, whereas fish in the PR and EN-PR groups were fed with basal diet containing 108 CFU g−1 feed of non-encapsulated and microencapsulated probiotic, respectively. During the exposure period (days 46-66), the fish in the probiotic and PC groups were co-treated with 500 μg g−1 feed of lead nitrate. Blood, liver and gut samples were taken at days 0, 45, 52, 59 and 66. The results revealed that growth performance and intestinal enzymatic activities were significantly (p< 0.05) improved in the probiotic groups compared to the NC group (day 45). Dietary exposure to lead resulted in the highest levels of liver aspartate aminotransferase (AST), liver alkaline phosphatase (ALP) and serum malondialdehyde (MDA), and the lowest activities of serum superoxide dismutase (SOD) and catalase (CAT) in the PC group (day 66). The levels of liver ALP were significantly (p< 0.05) lower in the probiotic groups compared to the NC and PC groups prior to and after exposure to dietary lead. Serum levels of total protein, albumin, SOD, CAT and glutathione (GSH) were significantly increased in fish fed with both non-encapsulated and microencapsulated probiotics (p< 0.05). However, microencapsulated probiotic showed the greatest potential for alleviation of the disturbed activities of intestinal and hepatic enzymes, and improvement of serum biochemical and antioxidant parameters. Our findings suggest that L. delbrueckii subsp. bulgaricus, particularly in the microencapsulated form, can be used as a potential probiotic to protect rainbow trout from dietborne lead toxicity.

Keywords

Abdel-Tawwab, M., Mousa, M. A., & Mohammed, M. A. (2010). Use of live baker’s yeast, Saccharomyces cerevisiae, in practical diet to enhance the growth performance of Galilee tilapia, Sarotherodon galilaeus (L.), and its resistance to environmental copper toxicity. Journal of the World Aquaculture Society, 41, 214-223.Search in Google Scholar

Adamse, P., Van der Fels-Klerx, H.J. and de Jong, J., (2017). Cadmium, lead, mercury and arsenic in animal feed and feed materials–trend analysis of monitoring results. Food Additives & Contaminants: Part A, 34(8), 1298-1311.Search in Google Scholar

Ahamed, M., & Siddiqui, M. K. J. (2007). Environmental lead toxicity and nutritional factors. Clinical Nutrition, 26(4), 400-408.Search in Google Scholar

Ahmed, F., Soliman, F.M., Adly, M.A., Soliman, H.A., El-Matbouli, M. and Saleh, M., (2021). Dietary chitosan nanoparticles: potential role in modulation of rainbow trout (Oncorhynchus mykiss) antibacterial fefense and intestinal immunity against enteric redmouth disease. Marine drugs, 19(2), 72.Search in Google Scholar

Ahmed, M. K., Parvin, E., Islam, M. M., Akter, M. S., Khan, S., & Al-Mamun, M. H. (2014). Lead- and cadmium-induced histopathological changes in gill, kidney and liver tissue of freshwater climbing perch Anabas testudineus (Bloch, 1792). Chemistry and Ecology, 30(6), 532-540.Search in Google Scholar

Al-Dohail, M. A., Hashim, R., & Aliyu-Paiko, M. (2011). Evaluating the use of Lactobacillus acidophilus as a biocontrol agent against common pathogenic bacteria and the effects on the haematology parameters and histopathology in African catfish Clarias gariepinus juveniles. Aquaculture Research, 42(2), 196-209.Search in Google Scholar

Ali, H., Khan, E., & Ilahi, I. (2019). Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. Journal of chemistry, 2019. https://doi.org/10.1155/2019/6730305Search in Google Scholar

Álvarez-González, C.A., Martínez-Sánchez, L., Peña-Marín, E.S., Guerrero-Zárate, R., Jesús-Ramírez, F., Morales-García, V., Uribe-López, M. and Núñez-Nogueira, G. (2020). Effects on the Growth and Digestive Enzyme Activity in Nile Tilapia Fry (Oreochromis niloticus) by Lead Exposure. Water, Air, & Soil Pollution, 231(9), 1-15.Search in Google Scholar

Alves, L. C., Glover, C. N., & Wood, C. M. (2006). Dietary Pb accumulation in juvenile freshwater rainbow trout (Oncorhynchus mykiss). Archives of environmental contamination and toxicology, 51(4), 615.Search in Google Scholar

Anal, A.K. and Singh, H., (2007). Recent advances in microencapsulation of probiotics for industrial applications and targeted delivery. Trends in Food Science & Technology, 18(5), 240-251.Search in Google Scholar

Awoyemi, O. M., Bawa-Allah, K. A., & Otitoloju, A. A. (2014). Accumulation and anti-oxidant enzymes as biomarkers of heavy metal exposure in Clarias gariepinus and Oreochromis niloticus. Applied Ecology and Environmental Sciences, 2(5), 114-122.Search in Google Scholar

Balakrishnan, R., Kumar, C. S., Reddy, K. K., Rani, M. U., Srikanth, M. K., Kavitha, K., et al. (2014). Antioxidant activity of coated probiotic Lactobacillus casei on chromium (VI) induced oxidative stress in rats. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 84(2), 305-310.Search in Google Scholar

Banwo, K., Alonge, Z., & Sanni, A. I. (2021). Binding capacities and antioxidant activities of Lactobacillus plantarum and Pichia kudriavzevii against cadmium and lead toxicities. Biological Trace Element Research, 199, 779–791.Search in Google Scholar

Belinskaia, D. A., Voronina, P. A., Shmurak, V. I., Vovk, M. A., Batalova, A. A., Jenkins, R. O., & Goncharov, N. V. (2020). The Universal Soldier: Enzymatic and Non-Enzymatic Antioxidant Functions of Serum Albumin. Antioxidants, 9(10), 966.Search in Google Scholar

Berti, G., Fossati, P., Tarenghi, G., Musitelli, C. and d’Eril, G.V., (1988). Enzymatic colorimetric method for the determination of inorganic phosphorus in serum and urine. Journal of clinical chemistry and clinical biochemistry, 26(6), 399-404.Search in Google Scholar

Bhakta, J. N., Ohnishi, K., Munekage, Y., Iwasaki, K., & Wei, M. Q. (2012). Characterization of lactic acid bacteria-based probiotics as potential heavy metal sorbents. Journal of applied microbiology, 112(6), 1193-1206.Search in Google Scholar

Bhattacharya, S. (2019). Probiotics against alleviation of lead toxicity: recent advances. Interdisciplinary Toxicology, 12(2), 89-92.Search in Google Scholar

Bhattacharya, S., (2020). The role of probiotics in the amelioration of cadmium toxicity. Biological trace element research, 197, 440-444.Search in Google Scholar

Bi, B., Liu, X., Guo, X., & Lu, S. (2018). Occurrence and risk assessment of heavy metals in water, sediment, and fish from Dongting Lake, China. Environmental Science and Pollution Research, 25(34), 34076-34090.Search in Google Scholar

Chromý, V., Svoboda, V. and Štěpánová, I., (1973). Spectrophotometric determination of magnesium in biological fluids with xylidyl blue II. Biochemical medicine, 7(2), 208-217.Search in Google Scholar

Dabrowska-Bouta, B., Struzynska, L., & Rafalowska, U. (1996). Effect of acute and chronic lead exposure on the level of sulfhydryl groups in rat brain. Acta neurobiologiae experimentalis, 56(1), 233-236.Search in Google Scholar

Dai, B., Hou, Y., Hou, Y. and Qian, L., (2019). Effects of multienzyme complex and probiotic supplementation on the growth performance, digestive enzyme activity and gut microorganisms composition of snakehead (Channa argus). Aquaculture Nutrition, 25(1), 15-25.Search in Google Scholar

Dai, S.Y., Jones, B., Lee, K.M., Li, W., Post, L. and Herrman, T.J., (2016). Heavy metal contamination of animal feed in Texas. Journal of Regulatory Science, 4(1), 21-32.Search in Google Scholar

Dai, W., Du, H., Fu, L., Jin, C., Xu, Z., & Liu, H. (2009). Effects of dietary Pb on accumulation, histopathology, and digestive enzyme activities in the digestive system of tilapia (Oreochromis niloticus). Biological trace element research, 127(2), 124-131.Search in Google Scholar

Dawood, M. A., Koshio, S., Ishikawa, M., Yokoyama, S., El Basuini, M. F., Hossain, M. S., et al. (2016). Effects of dietary supplementation of Lactobacillus rhamnosus or/and Lactococcus lactis on the growth, gut microbiota and immune responses of red sea bream, Pagrus major. Fish & Shellfish Immunology, 49, 275-285.Search in Google Scholar

El-Haroun, E.R., Goda, A.S. and Kabir Chowdhury, M.A., (2006). Effect of dietary probiotic Biogen® supplementation as a growth promoter on growth performance and feed utilization of Nile tilapia Oreochromis niloticus (L.). Aquaculture Research, 37(14), 1473-1480.Search in Google Scholar

El-Shafei, H. M. (2017). Alterations in the leucocytes and serum biochemistry in grey mullet (Mugil cephalus L.) fingerlings exposed to sub lethal doses of lead for different exposure periods. Journal of Aquaculture Research and Development, 8, 1-5.Search in Google Scholar

Fantin, A. M. B., Trevisan, P., Pederzoli, A., & Bergomi, M. (1988). Effects of acute experimental pollution by lead on some haematological parameters in Carassius carassius (L.) var. auratus. Italian Journal of Zoology, 55(1-4), 251-255.Search in Google Scholar

Fırat, Ö., & Kargın, F. (2010). Individual and combined effects of heavy metals on serum biochemistry of Nile tilapia Oreochromis niloticus. Archives of environmental contamination and toxicology, 58(1), 151-157.Search in Google Scholar

Fırat, Ö., Cogun, H. Y., Yüzereroğlu, T. A., Gök, G., Fırat, Ö., Kargin, F., & Kötemen, Y. (2011). A comparative study on the effects of a pesticide (cypermethrin) and two metals (copper, lead) to serum biochemistry of Nile tilapia, Oreochromis niloticus. Fish Physiology and Biochemistry, 37(3), 657-666.Search in Google Scholar

Ghanei-Motlagh, R., Baghshani, H., Shahsavani, D., & Ghodrati Azadi, H. (2017). Effect of dietary supplementation of garlic and vitamin E on lipid and protein oxidation in common carp meat during different storage times. Iranian Journal of Veterinary Science and Technology, 8(2), 40-47.Search in Google Scholar

Ghanei-Motlagh, R., Gharibi, D., Mohammadian, T., Khosravi, M., Mahmoudi, E., Zarea, M., Menanteau-Ledouble, S. and El-Matbouli, M., (2021). Feed supplementation with quorum quenching probiotics with anti-virulence potential improved innate immune responses, antioxidant capacity and disease resistance in Asian seabass (Lates calcarifer). Aquaculture, 535, 736345.Search in Google Scholar

Ghanei-Motlagh, R., Mohammadian, T., Gharibi, D., Khosravi, M., Mahmoudi, E., Zarea, M., et al. (2020). Quorum quenching probiotics modulated digestive enzymes activity, growth performance, gut microflora, haemato-biochemical parameters and resistance against Vibrio harveyi in Asian seabass (Lates calcarifer). Aquaculture, 531, 735874.Search in Google Scholar

Giri, S. S., Yun, S., Jun, J. W., Kim, H. J., Kim, S. G., Kang, J. W., et al. (2018). Therapeutic effect of intestinal autochthonous Lactobacillus reuteri P16 against waterborne lead toxicity in Cyprinus carpio. Frontiers in immunology, 9, 1824.Search in Google Scholar

Grotto, D., Maria, L. S., Valentini, J., Paniz, C., Schmitt, G., Garcia, S. C., et al. (2009). Importance of the lipid peroxidation biomarkers and methodological aspects for malondialdehyde quantification. Quimica Nova, 32(1), 169-174.Search in Google Scholar

Haddad, J. J., & Harb, H. L. (2005). l-γ-Glutamyl-l-cysteinyl-glycine (glutathione; GSH) and GSH-related enzymes in the regulation of pro-and anti-inflammatory cytokines: a signaling transcriptional scenario for redox (y) immunologic sensor (s)?. Molecular immunology, 42(9), 987-1014.Search in Google Scholar

Hahor, W., Thongprajukaew, K. and Suanyuk, N., (2019). Effects of dietary supplementation of oligosaccharides on growth performance, gut health and immune response of hybrid catfish (Pangasianodon gigas × Pangasianodon hypophthalmus). Aquaculture, 507, 97-107.Search in Google Scholar

Haux, C., & Larsson, Å. (1982). Influence of inorganic lead on the biochemical blood composition in the rainbow trout, Salmo gairdneri. Ecotoxicology and environmental safety, 6(1), 28-34.Search in Google Scholar

Hong, F. S. (2003). Study of the effect of Pb2+ on alpha-amylase activity by spectroscopy (in Chinese). Guang pu xue yu guang pu fen xi, 23(3), 583. PMID: 12953548.Search in Google Scholar

Hooshyar, Y., Abedian Kenari, A., Paknejad, H., & Gandomi, H. (2020). Effects of Lactobacillus rhamnosus ATCC 7469 on different parameters related to health status of rainbow trout (Oncorhynchus mykiss) and the protection against Yersinia ruckeri. Probiotics and Antimicrobial Proteins, 12, 1370-1384.Search in Google Scholar

Hoseini, S. M., Yousefi, M., Hoseinifar, S. H., & Van Doan, H. (2019). Antioxidant, enzymatic and hematological responses of common carp (Cyprinus carpio) fed with myrcene-or menthol-supplemented diets and exposed to ambient ammonia. Aquaculture, 506, 246-255.Search in Google Scholar

Hoseinifar, S. H., Yousefi, S., Van Doan, H., Ashouri, G., Gioacchini, G., Maradonna, F., & Carnevali, O. (2020). Oxidative Stress and Antioxidant Defense in Fish: The Implications of Probiotic, Prebiotic, and Synbiotics. Reviews in Fisheries Science & Aquaculture, 1-20.Search in Google Scholar

Janbakhsh, S., Hosseini Shekarabi, S.P. and Shamsaie Mergan, M., (2018). Nutritional value and heavy metal content of fishmeal from the Southwest Caspian Sea. Caspian Journal of Environmental Sciences, 16(4), 307-317.Search in Google Scholar

Jang, W. J., Lee, J. M., Hasan, M. T., Lee, B. J., Lim, S. G., & Kong, I. S. (2019). Effects of probiotic supplementation of a plant-based protein diet on intestinal microbial diversity, digestive enzyme activity, intestinal structure, and immunity in olive flounder (Paralichthys olivaceus). Fish & shellfish immunology, 92, 719-727.Search in Google Scholar

Javed, M., Ahmad, M. I., Usmani, N., & Ahmad, M. (2017). Multiple biomarker responses (serum biochemistry, oxidative stress, genotoxicity and histopathology) in Channa punctatus exposed to heavy metal loaded waste water. Scientific reports, 7(1), 1-11.Search in Google Scholar

Kailasapathy, K., 2002. Microencapsulation of probiotic bacteria: technology and potential applications. Current issues in intestinal microbiology, 3(2), 39-48.Search in Google Scholar

Kaya, H., Akbulut, M., & Yılmaz, S. (2015). Influence of sublethal lead concentrations on glucose, serum enzymes and ion levels in tilapia (Oreochromis mossambicus). In: Proceedings of the 7th International Conference on Information and Communication Technologies in Agriculture, Food and Environment (HAICTA, 2015), 858–866.Search in Google Scholar

Khan, M.S., Javed, M., Rehman, M.T., Urooj, M. and Ahmad, M.I., (2020). Heavy metal pollution and risk assessment by the battery of toxicity tests. Scientific Reports, 10(1), 1-10.Search in Google Scholar

Kim, J. H., & Kang, J. C. (2017). Toxic effects on bioaccumulation and hematological parameters of juvenile rockfish Sebastes schlegelii exposed to dietary lead (Pb) and ascorbic acid. Chemosphere, 176, 131-140.Search in Google Scholar

Kirillova, A. V., Danilushkina, A. A., Irisov, D. S., Bruslik, N. L., Fakhrullin, R. F., Zakharov, Y. A., et al. (2017). Assessment of resistance and bioremediation ability of Lactobacillus strains to lead and cadmium. International journal of microbiology, 2017. https://doi.org/10.1155/2017/9869145.Search in Google Scholar

Kong, Y., Olejar, K. J., On, S. L., & Chelikani, V. (2020). The potential of Lactobacillus spp. for modulating oxidative stress in the gastrointestinal tract. Antioxidants, 9(7), 610.Search in Google Scholar

Kurhaluk, N., Sliuta, A., Kyriienko, S., & Winklewski, P. J. (2017). Melatonin restores white blood cell count, diminishes glycated haemoglobin level and prevents liver, kidney and muscle oxidative stress in mice exposed to acute ethanol intoxication. Alcohol and Alcoholism, 52(5), 521-528.Search in Google Scholar

Lee, J. W., Choi, H., Hwang, U. K., Kang, J. C., Kang, Y. J., Kim, K. I., & Kim, J. H. (2019). Toxic effects of lead exposure on bioaccumulation, oxidative stress, neurotoxicity, and immune responses in fish: a review. Environmental toxicology and pharmacology, 68, 101-108.Search in Google Scholar

Li, B., Jin, D., Yu, S., Etareri Evivie, S., Muhammad, Z., Huo, G., & Liu, F. (2017). In vitro and in vivo evaluation of Lactobacillus delbrueckii subsp. bulgaricus KLDS1. 0207 for the alleviative effect on lead toxicity. Nutrients, 9(8), 845.Search in Google Scholar

Madreseh, S., Ghaisari, H. R., & Hosseinzadeh, S. (2019). Effect of lyophilized, encapsulated Lactobacillus fermentum and lactulose feeding on growth performance, heavy metals, and Trace element residues in rainbow trout (Oncorhynchus mykiss) tissues. Probiotics and antimicrobial proteins, 11(4), 1257-1263.Search in Google Scholar

Mager, E. M., (2012). Lead. In: Homeostasis and toxicology of non-essential metals, C. M. Wood. A. P. Farrell. & C. J. Brauner (Eds.). Academic Press, US, pp. 185-236.Search in Google Scholar

Martinez, C. B. R., Nagae, M. Y., Zaia, C. T. B. V., & Zaia, D. A. M. (2004). Acute morphological and physiological effects of lead in the neotropical fish Prochilodus lineatus. Brazilian Journal of Biology, 64(4), 797-807.Search in Google Scholar

Masindi, V., & Muedi, K. L. (2018). Environmental contamination by heavy metals. In: Heavy metals, H. Saleh (Ed.), Intechopen, London, pp. 115-132.Search in Google Scholar

Mirmazloomi, S., Shahsavani, D., & Baghshani, H. (2015). Studies on the protective effects of ascorbic acid and thiamine on lead-induced lipid and protein oxidation as well as enzymatic alterations in some tissues of Cyprinus carpio. Comparative Clinical Pathology, 24(5), 1231-1236.Search in Google Scholar

Mittal, N., Kanwar, S. S., & Sanyal, S. N. (2008). Effect of nonsteroidal anti-inflammatory drugs and the procarcinogen 1, 2-dimethylhydrazine on the antioxidant defense system. International journal of toxicology, 27(2), 169-174.Search in Google Scholar

Mohammadian, T., Alishahi, M., Tabandeh, M. R., Ghorbanpoor, M., Gharibi, D., Tollabi, M., & Rohanizade, S. (2016). Probiotic effects of Lactobacillus plantarum and L. delbrueckii ssp. bulguricus on some immune-related parameters in Barbus grypus. Aquaculture International, 24(1), 225-242.Search in Google Scholar

Mohammadian, T., Dezfuly, Z. T., Motlagh, R. G., Jangaran-Nejad, A., Hosseini, S. S., Khaj, H., & Alijani, N. (2019a). Effect of encapsulated Lactobacillus bulgaricus on innate immune system and hematological parameters in rainbow trout (Oncorhynchus mykiss), post-administration of Pb. Probiotics and Antimicrobial Proteins, 12, 375–388.Search in Google Scholar

Mohammadian, T., Ghanei-Motlagh, R., Molayemraftar, T., Mesbah, M., Zarea, M., Mohtashamipour, H. and Nejad, A.J., (2021). Modulation of growth performance, gut microflora, non-specific immunity and gene expression of proinflammatory cytokines in shabout (Tor grypus) upon dietary prebiotic supplementation. Fish & Shellfish Immunology, 112, 38-45.Search in Google Scholar

Mohammadian, T., Nasirpour, M., Tabandeh, M. R., Heidary, A. A., Ghanei-Motlagh, R., & Hosseini, S. S. (2019b). Administrations of autochthonous probiotics altered juvenile rainbow trout Oncorhynchus mykiss health status, growth performance and resistance to Lactococcus garvieae, an experimental infection. Fish & shellfish immunology, 86, 269-279.Search in Google Scholar

Monachese, M., Burton, J.P. and Reid, G., (2012). Bioremediation and tolerance of humans to heavy metals through microbial processes: a potential role for probiotics?. Applied and environmental microbiology, 78(18), 6397-6404.Search in Google Scholar

Mrvčić, J., Stanzer, D., Šolić, E., & Stehlik-Tomas, V. (2012). Interaction of lactic acid bacteria with metal ions: opportunities for improving food safety and quality. World Journal of Microbiology and Biotechnology, 28(9), 2771-2782.Search in Google Scholar

Mu, G., Li, H., Tuo, Y., Gao, Y., & Zhang, Y. (2019). Antioxidative effect of Lactobacillus plantarum Y44 on 2, 2′-azobis (2-methylpropionamidine) dihydrochloride (ABAP)-damaged Caco-2 cells. Journal of dairy science, 102(8), 6863-6875.Search in Google Scholar

Muhammad, Z., Ramzan, R., Zhang, S., Hu, H., Hameed, A., Bakry, A. M., et al. (2018). Comparative assessment of the bioremedial potentials of potato resistant starch-based microencapsulated and non-encapsulated Lactobacillus plantarum to alleviate the effects of chronic lead toxicity. Frontiers in microbiology, 9, 1306.Search in Google Scholar

Mustafa, S. A. (2020). Histopathology and heavy metal bioaccumulation in some tissues of Luciobarbus xanthopterus collected from Tigris River of Baghdad, Iraq. The Egyptian Journal of Aquatic Research. 46(2) 123-129.Search in Google Scholar

Naderi, M., Keyvanshokooh, S., Ghaedi, A., Salati, A.P., (2019). Interactive effects of dietary Nano selenium and vitamin E on growth, haematology, innate immune responses, antioxidant status and muscle composition of rainbow trout under high rearing density. Aquaculture Nutrition. 25 (5), 1156–1168.Search in Google Scholar

Noor-Ul, H., Haokun, L., Junyan, J., Xiaoming, Z., Dong, H., Yunxia, Y., & Shouqi, X. (2020). Dietary supplementation of Geotrichum candidum improves growth, gut microbiota, immune-related gene expression and disease resistance in gibel carp CAS III (Carassius auratus gibelio). Fish & Shellfish Immunology, 99, 144-153.Search in Google Scholar

Pinpimai, K., Rodkhum, C., Chansue, N., Katagiri, T., Maita, M., & Pirarat, N. (2015). The study on the candidate probiotic properties of encapsulated yeast, Saccharomyces cerevisiae JCM 7255, in Nile tilapia (Oreochromis niloticus). Research in veterinary science, 102, 103-111.Search in Google Scholar

Puzas, J. E., Campbell, J., O’Keefe, R. J., & Rosier, R. N. (2004). Lead toxicity in the skeleton and its role in osteoporosis. In: Nutrition and bone health, M. F. Holick & B. Dawson-Hughes (Eds.). Humana Press, NJ, pp. 363-376.Search in Google Scholar

Ringø, E., Hoseinifar, S. H., Ghosh, K., Doan, H. V., Beck, B. R., & Song, S. K. (2018). Lactic acid bacteria in finfish-an update. Frontiers in Microbiology, 9, 1818.Search in Google Scholar

Roche, M., Rondeau, P., Singh, N. R., Tarnus, E., & Bourdon, E. (2008). The antioxidant properties of serum albumin. FEBS letters, 582(13), 1783-1787.Search in Google Scholar

Rogers, J. T., Richards, J. G., & Wood, C. M. (2003). Ionoregulatory disruption as the acute toxic mechanism for lead in the rainbow trout (Oncorhynchus mykiss). Aquatic toxicology, 64(2), 215-234.Search in Google Scholar

Safari, R., Adel, M., Lazado, C.C., Caipang, C.M.A. and Dadar, M., (2016). Host-derived probiotics Enterococcus casseliflavus improves resistance against Streptococcus iniae infection in rainbow trout (Oncorhynchus mykiss) via immunomodulation. Fish & shellfish immunology, 52, 198-205.Search in Google Scholar

Salinas, I., Abelli, L., Bertoni, F., Picchietti, S., Roque, A., Furones, D., et al. (2008). Monospecies and multispecies probiotic formulations produce different systemic and local immunostimulatory effects in the gilthead seabream (Sparus aurata L.). Fish & shellfish immunology, 25(1-2), 114-123.Search in Google Scholar

Serrano, X., Hernández, A.J., Morales, G., Larson, M., Ruiz, J., Orellana, P., Díaz, M., Moyano, F.J. and Márquez, L., (2018). Effects of dietary melanoidins on digestive physiology, nutrient digestibility and plasmatic antioxidant capacity of the rainbow trout Oncorhynchus mykiss. Aquaculture, 495, 153-160.Search in Google Scholar

Srivastav, A. K., Rai, R., Suzuki, N., Mishra, D., & Srivastav, S. K. (2013). Effects of lead on the plasma electrolytes of a freshwater fish, Heteropneustes fossilis. International Aquatic Research, 5(1), 4.Search in Google Scholar

Song, H., Yu, W., Gao, M., Liu, X. and Ma, X., (2013). Microencapsulated probiotics using emulsification technique coupled with internal or external gelation process. Carbohydrate polymers, 96(1), 181-189.Search in Google Scholar

Suzer, C., Çoban, D., Kamaci, H. O., Saka, Ş., Firat, K., Otgucuoğlu, Ö., & Küçüksari, H. (2008). Lactobacillus spp. bacteria as probiotics in gilthead sea bream (Sparus aurata, L.) larvae: effects on growth performance and digestive enzyme activities. Aquaculture, 280(1-4), 140-145.Search in Google Scholar

Tarkhani, R., Imani, A., Hoseinifar, S. H., Ashayerizadeh, O., Moghanlou, K. S., Manaffar, R., et al. (2020). Comparative study of host-associated and commercial probiotic effects on serum and mucosal immune parameters, intestinal microbiota, digestive enzymes activity and growth performance of roach (Rutilus rutilus caspicus) fingerlings. Fish & Shellfish Immunology, 98, 661-669.Search in Google Scholar

Tewari, H., Gill, T. S., & Pant, J. (1987). Impact of chronic lead poisoning on the hematological and biochemical profiles of a fish, Barbus conchonius (Ham). Bulletin of environmental contamination and toxicology, 38(5), 748-752.Search in Google Scholar

Tian, F., Zhai, Q., Zhao, J., Liu, X., Wang, G., Zhang, H., et al. (2012). Lactobacillus plantarum CCFM8661 alleviates lead toxicity in mice. Biological trace element research, 150(1-3), 264-271.Search in Google Scholar

Tipple, T. E., & Rogers, L. K. (2012). Methods for the determination of plasma or tissue glutathione levels. In: Developmental Toxicology, Humana Press, NJ, Totowa, (pp. 315-324).Search in Google Scholar

Vazirzadeh, A., Roosta, H., Masoumi, H., Farhadi, A. and Jeffs, A., (2020). Long-term effects of three probiotics, singular or combined, on serum innate immune parameters and expressions of cytokine genes in rainbow trout during grow-out. Fish & shellfish immunology, 98, 748-757.Search in Google Scholar

Velíšek, J. and Svobodová, Z., (2004). Anaesthesia of Rainbow Trout (Oncorhynchus mykiss) with 2-phenoxyethanol: Acute toxicity and biochemical blood profile. Acta Veterinaria Brno, 73(3), 379-384.Search in Google Scholar

Wang, Y., Wu, Y., Wang, Y., Xu, H., Mei, X., Yu, D., et al. (2017). Antioxidant properties of probiotic bacteria. Nutrients, 9(5), 521.Search in Google Scholar

Yang, G., Shen, K., Yu, R., Wu, Q., Yan, Q., Chen, W., et al. (2020). Probiotic (Bacillus cereus) enhanced growth of Pengze crucian carp concurrent with modulating the antioxidant defense response and exerting beneficial impacts on inflammatory response via Nrf2 activation. Aquaculture, 529, 735691.Search in Google Scholar

Yang, L., Gao, Z., Cao, Y., Xing, R., & Zhang, X. (2005). Effect of PbII on the secondary structure and biological activity of trypsin. ChemBioChem, 6(7), 1191-1195.Search in Google Scholar

Yousefi, M., Hoseini, S. M., Vatnikov, Y. A., Kulikov, E. V., & Drukovsky, S. G. (2019). Rosemary leaf powder improved growth performance, immune and antioxidant parameters, and crowding stress responses in common carp (Cyprinus carpio) fingerlings. Aquaculture, 505, 473-480.Search in Google Scholar

Yu, L., Zhai, Q., Zhu, J., Zhang, C., Li, T., Liu, X., et al. (2017). Dietary Lactobacillus plantarum supplementation enhances growth performance and alleviates aluminum toxicity in tilapia. Ecotoxicology and environmental safety, 143, 307-314.Search in Google Scholar

Yu, Z., Zheng, Y. G., Du, H. L., Li, H. J., & Wu, L. F. (2020). Bioflocs protects copper-induced inflammatory response and oxidative stress in Rhynchocypris lagowski Dybowski through inhibiting NF-κB and Nrf2 signaling pathways. Fish & Shellfish Immunology, 98, 466-476.Search in Google Scholar

Zhai, Q., Narbad, A., & Chen, W. (2015). Dietary strategies for the treatment of cadmium and lead toxicity. Nutrients, 7(1), 552-571.Search in Google Scholar

Zhai, Q., Wang, H., Tian, F., Zhao, J., Zhang, H., & Chen, W. (2017). Dietary Lactobacillus plantarum supplementation decreases tissue lead accumulation and alleviates lead toxicity in Nile tilapia (Oreochromis niloticus). Aquaculture Research, 48(9), 5094-5103.Search in Google Scholar

Zhai, Q., Yu, L., Li, T., Zhu, J., Zhang, C., Zhao, J., et al. (2016). Effect of dietary probiotic supplementation on intestinal microbiota and physiological conditions of Nile tilapia (Oreochromis niloticus) under waterborne cadmium exposure. Antonie Van Leeuwenhoek, 110(4), 501-513.Search in Google Scholar

Zhao, L., Zheng, Y. G., Feng, Y. H., Li, M. Y., Wang, G. Q., & Ma, Y. F. (2020). Toxic effects of waterborne lead (Pb) on bioaccumulation, serum biochemistry, oxidative stress and heat shock protein-related genes expression in Channa argus. Chemosphere, 261, 127714.Search in Google Scholar

Zoghi, A., Khosravi-Darani, K., & Sohrabvandi, S. (2014). Surface binding of toxins and heavy metals by probiotics. Mini reviews in medicinal chemistry, 14(1), 84-98.Search in Google Scholar

Recommended articles from Trend MD

Plan your remote conference with Sciendo