Effects of Schizochytrium sp. and Lactoferrin on Diarrhea, Growth Performance, Fecal Score and Serum Antioxidant Indices of Sucking Calves Challenged with Escherichia coli K99

  • Alatengzhula ,
  • LIU Wenhui ,
  • MA Lu ,
  • REN Lijuan ,
  • GAO Shengtao ,
  • BU Dengpan
Expand
  • 1. State Key Laboratory of Animal Nutrition, Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193, China;
    2. Chinese Academy of Agricultural Sciences and World Agroforestry Center Joint Lab on Agroforestry and Sustainable Animal Husbandry, Beijing 100193, China

Received date: 2020-03-21

  Online published: 2020-09-17

Abstract

This study aimed to determine the alleviating effects of Schizochytrium sp. and lactoferrin on diarrhea of sucking calves challenged with Escherichia coli K99, and the effects of Schizochytrium sp. and lactoferrin on growth performance and serum antioxidant indices of sucking calves. Fifty 1-day-old newborn male Holstein calves were randomly assigned to 5 groups with 10 calves per group. The control group (C group) was fed a basic diet without Schizochytrium sp. and lactoferrin, the lactoferrin group (LF group) was fed the basic diet+1 g/d lactoferrin, the Schizochytrium sp. group (SZ group) was fed the basic diet+20 g/d Schizochytrium sp., and the lactoferrin+Schizochytrium sp. group (LF+SZ group) was fed the basic diet+1 g/d lactoferrin+20 g/d Schizochytrium sp. At the same time, the non-challenged E. coli group was set as reference. On 7 days of age, all the calves were challenged with Escherichia coli K99 (10 mL, 1×1011 CFU/mL) orally except the non-challenged Escherichia coli group, and the experiment ended at 14 days of age. The results showed as follows:1) during 1 to 7 days of age, dietary Schizochytrium sp tended to increase the average daily gain (P=0.093); during 8 to 11 days of age, compared with C group, the fecal score of LF, SZ and LF+SZ groups was significantly decreased (P<0.05), and lactoferrin and Schizochytrium sp had a synergistic action tendency on decreasing fecal score (P=0.074). 2) At 11 days of age, compared with C group, the serum catalase (CAT) activity of LF, SZ and LF+SZ groups was significantly increased (P<0.05), and LF+SZ group was significantly higher than LF and SZ groups (P<0.05); at 14 days of age, the serum CAT activity of LF+SZ group was significantly higher than that of SZ and C groups (P<0.05). At 14 days of age, compared with C group, the serum superoxide dismutase (SOD) activity of SZ and LF+SZ groups was significantly increased (P<0.05). At 7 days of age, compared with SZ and LF+SZ group, the serum glutathione peroxidase (GSH-Px) activity of LF group was significantly increased (P<0.05). At 11 days of age, compared with LF group, the serum malondialdehyde (MDA) content of SZ and LF+SZ groups was significantly increased (P<0.05); at 14 days of age, the serum MDA content of LF+SZ group was significantly higher than that of other groups (P<0.05). In conclusion, when sucking calves are under the condition of challenged with Escherichia coli K99, dietary Schizochytrium sp. and lactoferrin can promote intestinal health, reduce diarrhea and improve antioxidant capacity. Lactoferrin is better than Schizochytrium sp. on improving the antioxidant capacity of calves, and Schizochytrium sp. combined with lactoferrin have synergistic action on reduce the fecal score of sucking calves, and effectively alleviated diarrhea of calves.

Cite this article

Alatengzhula , LIU Wenhui , MA Lu , REN Lijuan , GAO Shengtao , BU Dengpan . Effects of Schizochytrium sp. and Lactoferrin on Diarrhea, Growth Performance, Fecal Score and Serum Antioxidant Indices of Sucking Calves Challenged with Escherichia coli K99[J]. Chinese Journal of Animal Nutrition, 2020 , 32(9) : 4166 -4176 . DOI: 10.3969/j.issn.1006-267x.2020.09.026

References

[1] HEINRICHS A J,HEINRICHS B S.A prospective study of calf factors affecting first-lactation and lifetime milk production and age of cows when removed from the herd[J].Journal of Dairy Science,2011,94(1):336-341.  
[2] SOBERON F,RAFFRENATO E,EVERETT R W,et al.Preweaning milk replacer intake and effects on long-term productivity of dairy calves[J].Journal of Dairy Science,2012,95(2):783-793.  
[3] BUTLER D G,CLARKE R C.Diarrhoea and dysentery in calves[M]//GYLES C L.Escherichia coli in domestic animals and humans.Wallingford:CAB International,1994:91-116.
[4] IZZO M M,KIRKLAND P D,MOHLER V L,et al.Prevalence of major enteric pathogens in Australian dairy calves with diarrhoea[J].Australian Veterinary Journal,2011,89(5):167-173.  
[5] CHO Y I,YOON K J.An overview of calf diarrhea-infectious etiology,diagnosis,and intervention[J].Journal of Veterinary Science,2014,15(1):1-17.  
[6] YIMER M,GEZHAGNE M,BIRUK T,et al.A review on major bacterial causes of calf diarrhea and its diagnostic method[J].Journal of Veterinary Medicine and Animal Health,2015,7(5):173-185.  
[7] TRIPATHI N N,MISHRA A K,TRIPATHI S.Antibacterial potential of plant volatile oils:a review[J].Proceedings of the National Academy of Sciences,India-Section B:Biological Sciences,2011,81:23-68.
[8] MOSELE J I,MACIA A,MOTILVA M J.Metabolic and microbial modulation of the large intestine ecosystem by non-absorbed diet phenolic compounds:a review[J].Molecules,2015,20(9):17429-17468.  
[9] BRENES A,VIVEROS A,CHAMORRO S,et al.Use of polyphenol-rich grape by-products in monogastric nutrition.A review[J].Animal Feed Science and Technology,2016,211:1-17.
[10] FLAGA J,KORYTKOWSKI ?,GÓRKA P,et al.The effect of docosahexaenoic acid-rich algae supplementation in milk replacer on performance and selected immune system functions in calves[J].Journal of Dairy Science,2019,102(10):8862-8873.  
[11] CHOI Y,GOEL A,HOSSEINDOUST A,et al.Effects of dietary supplementation of Ecklonia cava with or without probiotics on the growth performance,nutrient digestibility,immunity and intestinal health in weanling pigs[J].Italian Journal of Animal Science,2016,15(1):62-68.  
[12] GEBERT S,DAVIS E,REHBERGER T,et al.Lactobacillus brevis strain 1E1 administered to piglets through milk supplementation prior to weaning maintains intestinal integrity after the weaning event[J].Beneficial Microbes,2011,2(1):35-45.  
[13] YU J H,WANG Y,SUN J,et al.Antioxidant activity of alcohol aqueous extracts of Crypthecodinium cohnii and Schizochytrium sp.[J].Journal of Zhejiang University-Science B,2017,18(9):797-806.  
[14] SIJBEN J W,CALDER P C.Differential immunomodulation with long-chain n-3 PUFA in health and chronic disease[J].Proceedings of the Nutrition Society,2007,66(2):237-259.  
[15] CALDER P C,GRIMBLE R F.Polyunsaturated fatty acids,inflammation and immunity[J].European Journal of Clinical Nutrition,2002,56(Suppl.3):14-19.
[16] KEW S,MESA M D,TRICON S T,et al.Effects of oils rich in eicosapentaenoic and docosahexaenoic acids on immune cell composition and function in healthy humans[J].The American Journal of Clinical Nutrition,2004,79(4):674-681.  
[17] JHO D H,COLE S M,LEE E M,et al.Role of omega-3 fatty acid supplementation in inflammation and malignancy[J].Integrative Cancer Therapies,2004,3(2):98-111.  
[18] SHIMAZAWA M,NAKAJIMA Y,MASHIMA Y,et al.Docosahexaenoic acid (DHA) has neuroprotective effects against oxidative stress in retinal ganglion cells[J].Brain Research,2009,1251:269-275.
[19] TSIPLAKOU E,CHATZIKONSTANTINOU M,MITSIOPOULOU C,et al.Effect of soya bean and fish oil inclusion in diets on milk and plasma enzymes from sheep and goat related to oxidation[J].Journal of Animal Physiology and Animal Nutrition,2017,101(4):733-742.  
[20] LI M H,ROBINSON E H,TUCKER C S,et al.Effects of dried algae Schizochytrium sp.,a rich source of docosahexaenoic acid,on growth,fatty acid composition,and sensory quality of channel catfish Ictalurus punctatus[J].Aquaculture,2009,292(3/4):232-236.
[21] SIMOPOULOS A P,LEAF A,SALEM N S Jr.Workshop on the essentiality of and recommended dietary intakes for omega-6 and omega-3 fatty acids[J].Asia Pacific Journal of Clinical Nutrition,1999,8(4):300-301.  
[22] MEADUS W J,DUFF P,ROLLAND D,et al.Feeding docosahexaenoic acid to pigs reduces blood triglycerides and induces gene expression for fat oxidation[J].Canadian Journal of Animal Science,2011,91(4):601-612.  
[23] SHIN K,YAMAUCHI K,TERAGUCHI S,et al.Antibacterial activity of bovine lactoferrin and its peptides against enterohaemorrhagic Escherichia coli O157:H7[J].Letters in Applied Microbiology,1998,26(6):407-411.  
[24] TOMITA M,BELLAMY W,TAKASE M,et al.Potent antibacterial peptides generated by pepsin digestion of bovine lactoferrin[J].Journal of Dairy Science,1991,74(12):4137-4142.  
[25] REITER B,BROCK J H,STEEL E D.Inhibition of Escherichia coli by bovine colostrum and post colostral milk.Ⅱ.The bacteriostatic effect of lactoferrin on a serum susceptible and serum resistant strain of E.coli[J].Immunology,1975,28(1):83-95.
[26] KUME S I, TANABE S.Effect of supplemental lactoferrin with ferrous iron on iron status of newborn calves[J].Journal of Dairy Science, 1996, 79(3):0-464.
[27] MIYAUCHI H,HASHIMOTO S I,NAKAJIMA M,et al.Bovine lactoferrin stimulates the phagocytic activity of human neutrophils:identification of its active domain[J].Cellular Immunology,1998,187(1):34-37.  
[28] EMBLETON N D,BERRINGTON J E,MCGUIRE W,et al.Lactoferrin:antimicrobial activity and therapeutic potential[J].Seminars in Fetal and Neonatal Medicine,2013,18(3):143-149.  
[29] HIROTANI Y,IKEDA K,KATO R,et al.Protective effects of lactoferrin against intestinal mucosal damage induced by lipopolysaccharide in human intestinal Caco-2 cells[J].Yakugaku Zasshi,2008,128(9):1363-1368.  
[30] TERAGUCHI S,OZAWA K,YASUDA S,et al.The bacteriostatic effects of orally administered bovine lactoferrin on intestinal Enterobacteriaceae of SPF mice fed bovine milk[J].Bioscience,Biotechnology,and Biochemistry,1994,58(3):482-487.  
[31] ZHANG P,SAWICKI B,HANSON L,et al.Human lactoferrin in the milk of transgenic mice increases intestinal growth in ten-day-old suckling neonates[J].Advances in Experimental Medicine and Biology,2001,501:107-113.
[32] OGATA T,TERAGUCHI S,SHIN K,et al.The mechanism of in vivo bacteriostasis of bovine lactoferrin[M]//SPIK G,LEGRAND D,MAZURIER J,et al.Advances in lactoferrin research.Boston:Springer,1998,443:239-246.
[33] JOSLIN R S,ERICKSON P S,SANTORO H M,et al.Lactoferrin supplementation to dairy calves[J].Journal of Dairy Science,2002,85(5):1237-1242.  
[34] ROBBLEE E D,ERICKSON P S,WHITEHOUSE N L,et al.Supplemental lactoferrin improves health and growth of Holstein calves during the preweaning phase[J].Journal of Dairy Science,2003,86(4):1458-1464.  
[35] YEKTA M A,COX E,GODDEERIS B M,et al.Reduction of Escherichia coli O157:H7 excretion in sheep by oral lactoferrin administration[J].Veterinary Microbiology,2011,150(3/4):373-378.
[36] KIECKENS E,RYBARCZYK J,DE ZUTTER L,et al.Clearance of Escherichia coli O157:H7 infection in calves by rectal administration of bovine lactoferrin[J].Applied and Environmental Microbiology,2015,81(5):1644-1651.  
[37] PAL B,PACHAURI S P.Effect of oral rehydration in neonatal calves treated for diarrhoea induced with Escherichia coli (0101:K99) infection[J].The Indian Journal of Veterinary Research,2008,17(1):19-26.
[38] STILL J,DELAHAUT P,COPPE P,et al.Treatment of induced enterotoxigenic colibacillosis (Scours) in calves by the lactoperoxidase system and lactoferrin[J].Annals of Veterinary Research,1990,21(2):143-152.
[39] NRC.Nutrient requirements of dairy cattle[S].7th ed.Washington,D.C.National Academy of Science,2001.
[40] AOAC.Official methods of analysis of the association of official analytical chemists[S].17th ed.Washington D.C.:AOAC,2000.
[41] VAN SOEST P J,ROBERTSON J B,LEWIS B A Symposium:carbohydrate methodology,metabolism,and nutritional implications in dairy cattle[J].Journal of Dairy Science,1991,74(10):3583-3597.
[42] MAGALHÃES V J,SUSCA F,LIMA F S,et al.Effect of feeding yeast culture on performance,health,and immunocompetence of dairy calves[J].Journal of Dairy Science,2008,91(4):1497-1509.  
[43] SHAMS Z,TAHAMTAN Y,POURBAKHSH A,et al.Detection of enterotoxigenic K99(F5) and F41 from fecal sample of calves by molecular and serological methods[J].Comparative Clinical Pathology,2012,21(4):475-478.  
[44] OK M,GVLER L,TURGUT K,et al.The studies on the aetiology of diarrhoea in neonatal calves and determination of virulence gene markers of Escherichia coli strains by multiplex PCR[J].Zoonoses and Public Health,2010,56(2):94-101.
[45] WEI H K,ZHOU Y F,JIANG S Z,et al.Feeding a DHA-enriched diet increases skeletal muscle protein synthesis in growing pigs:association with increased skeletal muscle insulin action and local mRNA expression of insulin-like growth factor[J].British Journal of Nutrition,2013,110(4):671-680.  
[46] LEONARD S G,SWEENEY T,BAHAR B,et al.Effect of dietary seaweed extracts and fish oil supplementation in sows on performance,intestinal microflora,intestinal morphology,volatile fatty acid concentrations and immune status of weaned pigs[J].British Journal of Nutrition,2011,105(4):549-560.  
[47] GABLER N K,SPENCER J D,WEBEL D M,et al.In utero and postnatal exposure to long chain (n-3) PUFA enhances intestinal glucose absorption and energy stores in weanling pigs[J].The Journal of Nutrition,2007,137(11):2351-2358.  
[48] MOON H W,ISAACSON R E,POHLENZ J.Mechanisms of association of enteropathogenic Escherichia coli with intestinal epithelium[J].The American Journal of Clinical Nutrition,1979,32(1):119-127.  
[49] ELASS-ROCHARD E,ROSEANU A,LEGRAND D,et al.Lactoferrin-lipopolysaccharide interaction:involvement of the 28-34 loop region of human lactoferrin in the high-affinity binding to Escherichia coli 055B5 lipopolysaccharide[J].Biochemical Journal,1995,312(3):839-845.  
[50] WANG X Y,PAN L Y,LU J,et al.n-3 PUFAs attenuate ischemia/reperfusion induced intestinal barrier injury by activating Ⅰ-FABP-PPARγ pathway[J].Clinical Nutrition,2012,31(6):951-957.  
[51] MCCRACKEN V J,LORENZ R G.The gastrointestinal ecosystem:a precarious alliance among epithelium,immunity and microbiota[J].Cellular Microbiology,2001,3:1-11.
[52] KHALED M A.Oxidative stress in childhood malnutrition and diarrhoeal diseases[J].Journal of Diarrhoeal Diseases Research,1994,12(3):165-172.
[53] GOLDEN M H,RAMDATH D D.Free radicals in the pathogenesis of kwashiorkor[J].Proceedings of the Nutrition Society,1987,46(1):53-68.  
[54] GODIN D V,WOHAIEB S A.Nutritional deficiency,starvation,and tissue antioxidant status[J].Free Radical Biology and Medicine,1988,5(3):165-176.  
[55] KONINGSBERGER J C,MARX J J,VAN HATTUM C.Radicals in gastroenterology[J].Scandinavian Journal of Gastroenterology,1965,23(4):30-40.
[56] DARMON N,PÉLISSIER M G,HEYMAN M,et al.Oxidative stress may contribute to the intestinal dysfunction of weanling rats fed a low protein diet[J].Journal of Nutrition,1993,123(6):1068-1075.
[57] LINDLEY K J,GOSS-SAMPSON M A,MULLER D P R,et al.Lipid peroxidation and electrogenic ion transport in the jejunum of the vitamin E deficient rat[J].Gut,1994,35(1):34-39.  
[58] HUANG C J,FWU M L.Protein insufficiency aggravates the enhanced lipid peroxidation and reduced activities of antioxidative enzymes in rats fed diets high in polyunsaturated fat[J].The Journal of Nutrition,1990,122(5):1182-1189.
[59] SONG P X,ZHANG R J,WANG X X,et al.Dietary grape-seed procyanidins decreased postweaning diarrhea by modulating intestinal permeability and suppressing oxidative stress in rats[J].Journal of Agricultural and Food Chemistry,2011,59(11):6227-6232.  
[60] WANG X Q,OU D Y,YIN J D,et al.Proteomic analysis reveals altered expression of proteins related to glutathione metabolism and apoptosis in the small intestine of zinc oxide-supplemented piglets[J].Amino Acids,2009,37(1):209-218.  
[61] DI PAOLA R,ESPOSITO E,MAZZON E,et al.3,5-dicaffeoyl-4-malonylquinic acid reduced oxidative stress and inflammation in a experimental model of inflammatory bowel disease[J].Free Radical Research,2010,44(1):74-89.  
[62] LANGIE S A S,WILMS L C,HÄMÄLÄINEN S,et al.Modulation of nucleotide excision repair in human lymphocytes by genetic and dietary factors[J].The British Journal of Nutrition,2010,103(4):490-501.  
[63] KVHN H,BORCHERT A.Regulation of enzymatic lipid peroxidation:the interplay of peroxidizing and peroxide reducing enzymes[J].Free Radical Biology and Medicine,2002,33(2):154-172.  
[64] HALLIWELL B,CHIRICO S.Lipid peroxidation:its mechanism,measurement,and significance[J].American Journal of Clinical Nutrition,1993,57(Suppl.1):715S-725S.
[65] DAS K,ROYCHOUDHURY A.Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants[J].Frontiers in Environmental Science,2014,2:53.
[66] LYKKESFELDT J,SVENDSEN O.Oxidants and antioxidants in disease:oxidative stress in farm animals[J].The Veterinary Journal,2007,173(3):502-511.  
[67] WU G Y,FANG Y Z,YANG S,et al.Glutathione metabolism and its implications for health[J].The Journal of Nutrition,2004,134(3):489-492.  
[68] YOUSEF M I,SAAD A A,EL-SHENNAWY L K.Protective effect of grape seed proanthocyanidin extract against oxidative stress induced by cisplatin in rats[J].Food and Chemical Toxicology,2009,47(6):1176-1183.  
[69] NIELSEN F,MIKKELSEN B B,BO NIELSEN J,et al.Plasma malondialdehyde as biomarker for oxidative stress:reference interval and effects of life-style factors[J].Clinical Chemistry,1997,43(7):1209-1214.  
[70] GROTTO D,MARIA L S,VALENTINI J,et al.Importance of the lipid peroxidation biomarkers and methodological aspects FOR malondialdehyde quantification[J].Química Nova,2009,32(1):169-174.  
[71] MAVROMMATIS A,CHRONOPOULOU E G,SOTIRAKOGLOU K,et al.The impact of the dietary supplementation level with Schizochytrium sp,on the oxidative capacity of both goats' organism and milk[J].Livestock Science,2018,218:37-43.
[72] RUIZ-GUTIÉRREZ V,PÉREZ-ESPINOSA A,VÁZQUEZ C M,et al.Effects of dietary fats (fish,olive and high-oleic-acid sunflower oils) on lipid composition and antioxidant enzymes in rat liver[J].British Journal of Nutrition,1999,82(3):233-241.  
[73] YUAN Y V,KITTS D D.Dietary (n-3) fat and cholesterol alter tissue antioxidant enzymes and susceptibility to oxidation in SHR and WKY rats[J].Jrounal of Nutrition,2003,133(3):679-688.
[74] YUAN Y V,KITTS D D.Dietary fat source and cholesterol interactions alter plasma lipids and tissue susceptibility to oxidation in spontaneously hypertensive (SHR) and normotensive Wistar Kyoto (WKY) rats[J].Molecular and Cellular Biochemistry,2002,232(1/2):33-47.  
[75] LINDMARK-MÁNSSON H,AKESSON B.Antioxidative factors in milk[J].British Journal of Nutrition,2000,84(Suppl.1):S103-S110.
Outlines

/