Screening of lactic acid bacteria with potential protective effects against cadmium toxicity

Food Control

Volumn 54, Issue , 2015, Pages 23-30

  Zhai, Qixiao ^a   Yin, Ruijie ^a   Yu, Leilei ^a   Wang, Gang ^a   Tian, Fengwei ^a   Yu, Ruipeng ^a   Zhao, Jianxin ^a   Liu, Xiaoming ^a   Chen, Yong Q ^a,b   Zhang, Hao ^a   Chen, Wei ^a,b  

^a JIANGNAN UNIVERSITY   (China)

^b Synergistic Innovation Center for Food Safety and Nutrition   (China)

Author keywords

Antioxidative activity; Cadmium binding ability; Cadmium tolerance; Cadmium toxicity; Lactic acid bacteria

Indexed keywords

ANIMALIA; LACTOBACILLUS PLANTARUM; LACTOBACILLUS RHAMNOSUS;

EID: 84922569054     PISSN: 09567135     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodcont.2015.01.037     Document Type: Article

References (51)

1. Abou-Shanab R., Van Berkum P., Angle J. Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 2007, 68(2):360-367.
2. Akinbowale O.L., Peng H., Grant P., Barton M.D. Antibiotic and heavy metal resistance in motile aeromonads and pseudomonads from rainbow trout (Oncorhynchus mykiss) farms in Australia. International Journal of Antimicrobial Agents 2007, 30(2):177-182.
3. Araúz I.L.C., Afton S., Wrobel K., Caruso J.A., Corona J., Wrobel K. Study on the protective role of selenium against cadmium toxicity in lactic acid bacteria: an advanced application of ICP-MS. Journal of Hazardous Materials 2008, 153(3):1157-1164.
4. ATSDR Toxic guide for cadmium 2012, Retrieved from, Accessed 21.01.15. http://www.atsdr.cdc.gov/toxguides/toxguide-5.pdf.
5. Bhakta J., Munekage Y., Ohnishi K., Jana B. Isolation and identification of cadmium-and lead-resistant lactic acid bacteria for application as metal removing probiotic. International Journal of Environmental Science and Technology 2012, 9(3):433-440.
6. Bhakta J., Ohnishi K., Munekage Y., Iwasaki K., Wei M. Characterization of lactic acid bacteria-based probiotics as potential heavy metal sorbents. Journal of Applied Microbiology 2012, 112(6):1193-1206.
7. Bhattacharyya M., Whelton B., Peterson D., Carnes B., Moretti E., Toomey J., et al. Skeletal changes in multiparous mice fed a nutrient-sufficient diet containing cadmium. Toxicology 1988, 50(2):193-204.
8. Chen P., Zhang Q., Dang H., Liu X., Tian F., Zhao J., et al. Screening for potential new probiotic based on probiotic properties and α-glucosidase inhibitory activity. Food Control 2014, 35(1):65-72.
9. Dorta D.J., Leite S., DeMarco K.C., Prado I.M., Rodrigues T., Mingatto F.E., et al. Aproposed sequence of events for cadmium-induced mitochondrial impairment. Journal of Inorganic Biochemistry 2003, 97(3):251-257.
10. Doyle J.J., Marshall R.T., Pfander W.H. Effects of cadmium on the growth and uptake of microorganisms. Applied Microbiology 1975, 29(4):562-564.
11. El-Nezami H.S., Chrevatidis A., Auriola S., Salminen S., Mykkänen H. Removal of common Fusarium toxins invitro by strains of Lactobacillus and Propionibacterium. Food Additives and Contaminants 2002, 19(7):680-686.
12. FAO/WHO Evaluation of certain food contaminants: 64th report of the Joint FAO/WHO Expert Committee on Food Additives 2006, Geneva, Retrieved from, Accessed 21.01.15. http://whqlibdoc.who.int/trs/WHO_TRS_930_eng.pdf.
13. Fazeli M., Hassanzadeh P., Alaei S. Cadmium chloride exhibits a profound toxic effect on bacterial microflora of the mice gastrointestinal tract. Human and Experimental Toxicology 2011, 30(2):152-159.
14. Forsyth C.B., Farhadi A., Jakate S.M., Tang Y., Shaikh M., Keshavarzian A. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 2009, 43(2):163-172.
15. Goyal N., Rishi P., Shukla G. Lactobacillus rhamnosus GG antagonizes Giardia intestinalis induced oxidative stress and intestinal disaccharidases: an experimental study. World Journal of Microbiology & Biotechnology 2013, 29(6):1049-1057.
16. 1 in rats. Applied and Environmental Microbiology 2006, 72(11):7398-7400.
17. Guo Z., Wang J., Yan L., Chen W., Liu X., Zhang H. Invitro comparison of probiotic properties of Lactobacillus casei Zhang, a potential new probiotic, with selected probiotic strains. LWT-Food Science and Technology 2009, 42(10):1640-1646.
18. Halttunen T., Collado M., El-Nezami H., Meriluoto J., Salminen S. Combining strains of lactic acid bacteria may reduce their toxin and heavy metal removal efficiency from aqueous solution. Letters in Applied Microbiology 2008, 46(2):160-165.
19. Halttunen T., Salminen S., Tahvonen R. Rapid removal of lead and cadmium from water by specific lactic acid bacteria. International Journal of Food Microbiology 2007, 114(1):30-35.
20. Hong F., Jin T., Zhang A. Risk assessment on renal dysfunction caused by co-exposure to arsenic and cadmium using benchmark dose calculation in a Chinese population. Biometals 2004, 17(5):573-580.
21. Huang Y., Adams M.C. Invitro assessment of the upper gastrointestinal tolerance of potential probiotic dairy propionibacteria. International Journal of Food Microbiology 2004, 91(3):253-260.
22. Hyronimus B., Le Marrec C., Hadj Sassi A., Deschamps A. Acid and bile tolerance of spore-forming lactic acid bacteria. International Journal of Food Microbiology 2000, 61(2):193-197.
23. Ibrahim F., Halttunen T., Tahvonen R., Salminen S. Probiotic bacteria as potential detoxification tools: assessing their heavy metal binding isotherms. Canadian Journal of Microbiology 2006, 52(9):877-885.
24. IRIS Cadmium: Reference dose for chronic oral exposure 2012, Retrieved from, Accessed 21.01.15. http://www.epa.gov/iris/subst/0141.htm.
25. Jain S., Yadav H., Ravindra Sinha P. Antioxidant and cholesterol assimilation activities of selected lactobacilli and lactococci cultures. Journal of Dairy Research 2009, 76(04):385-391.
26. Järup L., Åkesson A. Current status of cadmium as an environmental health problem. Toxicology and Applied Pharmacology 2009, 238(3):201-208.
27. Kojima S., Sugimura Y., Hirukawa H., Kiyozumi M., Shimada H., Funakoshi T. Effects of dithiocarbamates on testicular toxicity in rats caused by acute exposure to cadmium. Toxicology and Applied Pharmacology 1992, 116(1):24-29.
28. Koyu A., Gokcimen A., Ozguner F., Bayram D.S., Kocak A. Evaluation of the effects of cadmium on rat liver. Molecular and Cellular Biochemistry 2006, 284(1-2):81-85.
29. Kullisaar T., Songisepp E., Mikelsaar M., Zilmer K., Vihalemm T., Zilmer M. Antioxidative probiotic fermented goats' milk decreases oxidative stress-mediated atherogenicity in human subjects. British Journal of Nutrition 2003, 90(02):449-456.
30. Lin M.Y., Chang F.J. Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Digestive Diseases and Sciences 2000, 45(8):1617-1622.
31. Lin M.Y., Yen C.L. Antioxidative ability of lactic acid bacteria. Journal of Agricultural and Food Chemistry 1999, 47(4):1460-1466.
32. Liu J., Li Q., Dong J., Chen J., Gu G. Multivariate modeling of aging in bottled lager beer by principal component analysis and multiple regression methods. Journal of Agricultural and Food Chemistry 2008, 56(16):7106-7112.
33. Liu J., Qu W., Kadiiska M.B. Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicology and Applied Pharmacology 2009, 238(3):209-214.
34. Matyar F., Kaya A., Dinçer S. Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey. Science of the Total Environment 2008, 407(1):279-285.
35. Minh N.D., Hough R.L., Thuy L.T., Nyberg Y., Mai L.B., Vinh N.C., et al. Assessing dietary exposure to cadmium in a metal recycling community in Vietnam: age and gender aspects. Science of the Total Environment 2012, 416(1):164-171.
36. Nordberg G.F., Nogawa K., Nordberg M., Friberg L. Cadmium. Handbook on the toxicology of metals 2011, 446-451. Academic Press, Burlington, MA. 3rd ed. G.F. Nordberg, B.A. Fowler, M. Nordberg, L. Friberg (Eds.).
37. Ognjanović B.I., Marković S.D., Dordević N.Z., Trbojević I.S., Štajn A.Š., Saičić Z.S. Cadmium-induced lipid peroxidation and changes in antioxidant defense system in the rat testes: protective role of coenzyme Q10 and vitamin E. Reproductive Toxicology 2010, 29(2):191-197.
38. Paul D., Hoskins L.C. Effect of oral lactobacillus feedings on fecal lactobacillus counts. The American Journal of Clinical Nutrition 1972, 25(8):763-765.
39. Pellegrini N., Serafini M., Colombi B., Del Rio D., Salvatore S., Bianchi M., et al. Total antioxidant capacity of plant foods, beverages and oils consumed in Italy assessed by three different invitro assays. The Journal of Nutrition 2003, 133(9):2812-2819.
40. Rehm S., Waalkes M.P. Cadmium-induced ovarian toxicity in hamsters, mice, and rats. Toxicological Sciences 1988, 10(4):635-647.
41. Satarug S., Garrett S.H., Sens M.A., Sens D.A. Cadmium, environmental exposure, and health outcomes. Environmental Health Perspectives 2011, 16(5):2587-2602.
42. Tao Y., Drabik K.A., Waypa T.S., Musch M.W., Alverdy J.C., Schneewind O., et al. Soluble factors from Lactobacillus GG activate MAPKs and induce cytoprotective heat shock proteins in intestinal epithelial cells. American Journal of Physiology-Cell Physiology 2006, 290(4):C1018-C1030.
43. Tellez-Plaza M., Navas-Acien A., Crainiceanu C.M., Guallar E. Cadmium exposure and hypertension in the 1999-2004 National Health and Nutrition Examination Survey (NHANES). Environmental Health Perspectives 2008, 116(1):51-56.
44. Thijssen S., Cuypers A., Maringwa J., Smeets K., Horemans N., Lambrichts I., et al. Low cadmium exposure triggers a biphasic oxidative stress response in mice kidneys. Toxicology 2007, 236(1):29-41.
45. Vig K., Megharaj M., Sethunathan N., Naidu R. Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Advances in Environmental Research 2003, 8(1):121-135.
46. Watterlot L., Rochat T., Sokol H., Cherbuy C., Bouloufa I., Lefèvre F., et al. Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice. International Journal of Food Microbiology 2010, 144(1):35-41.
47. Yan H., Carter C.E., Xu C., Singh P.K., Jones M.M., Johnson J.E., et al. Cadmium-induced apoptosis in the urogenital organs of the male rat and its suppression by chelation. Journal of Toxicology and Environmental Health 1997, 52(2):149-168.
48. Zafar S., Aqil F., Ahmad I. Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil. Bioresource Technology 2007, 98(13):2557-2561.
49. Zhang W.-L., Du Y., Zhai M.-M., Shang Q. Cadmium exposure and its health effects: a 19-year follow-up study of a polluted area in China. Science of the Total Environment 2014, 470(1):224-228.
50. Zhang S., Liu L., Su Y., Li H., Sun Q., Liang X., et al. Antioxidative activity of lactic acid bacteria in yogurt. African Journal of Microbiology Research 2011, 5(29):5194-5201.
51. Zhao D., Shah N.P. Changes in antioxidant capacity, isoflavone profile, phenolic and vitamin contents in soymilk during extended fermentation. LWT-Food Science and Technology 2014, 58(2):454-462.