Lysozyme as an alternative to antibiotics improves growth performance and small intestinal morphology in nursery pigs

Journal of Animal Science

Volumn 91, Issue 7, 2013, Pages 3129-3136

  Oliver, W T ^a   Wells, J E ^a  

^a U S MEAT ANIMAL RESEARCH CENTER   (United States)

Author keywords

Antimicrobial; Growth; Intestine; Lysozyme; Swine

Indexed keywords

EID: 84882689030     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2012-5782     Document Type: Article

References (40)

1. Al-Nakkash, L., L. Batia, M. Bhakta, A. Peterson, N. Hale, R. Skinner, S. Sears, and J. Jensen. 2011. Stimulation of murine intestinal secretion by daily genistein injections: Gender-dependent differences. Cell. Physiol. Biochem. 28:239-250.
2. Argenzio, R. A., and J. A. Liacos. 1990. Endogenous prostanoids control ion transport across neonatal porcine ileum in vitro. Am. J. Vet. Res. 51:747-751.
3. Argenzio, R. A., J. A. Liacos, M. L. Levy, D. J. Meuten, J. G. Lecce, and D. W. Powell. 1990. Villous atrophy, crypt hyperplasia, cellular infltration, and impaired glucose-Na absorption in enteric cryptosporidiosis of pigs. Gastroenterology 98:1129-1140.
4. Azain, M. J., T. Tomkins, J. S. Sowinski, R. A. Arentson, and D. E. Jewell. 1996. Effect of supplemental pig milk replacer on litter performance: Seasonal variation in response. J. Anim. Sci. 74:2195-2202.
5. Bosi, P., L. Casini, A. Finamore, C. Cremokolini, G. Merialdi, P. Trevisi, F. Nobili, and E. Mengheri. 2004. Spray-dried plasma improves growth performance and reduces inflammatory status of weaned pigs challenged with enterotoxigenic Escherichia coli K88. J. Anim Sci. 82:1764-1772.
6. Boyd, R. D., R. S. Kensinger, R. J. Harrell, and D. E. Bauman. 1995. Nutrient uptake and endocrine regulation of milk synthesis by mammary tissue of lactating sows. J. Anim. Sci. 73(Suppl. 2):36-56.
7. Brundige, D. R., E. A. Maga, K. C. Klasing, and J. D. Murray. 2008. Lysozyme transgenic goats' milk influences gastrointestinal morphology in young pigs. J. Nutr. 138:921-926.
8. Brundige, D. R., E. A. Maga, K. C. Klasing, and J. D. Murray. 2010. Consumption of pasteurized human lysozyme transgenic goats' milk alters serum metabolite profle in young pigs. Transgenic Res. 19:563-574.
9. Clarke, T. B., K. M. Davis, E. S. Lysenko, A. Y. Zhou, Y. Yu, and J. N. Weiser. 2010. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16:228-231.
10. Cooper, C. A., D. R. Brundige, W. A. Reh, E. A. Maga, and J. D. Murray. 2011. Lysozyme transgenic goats' milk positively impacts intestinal cytokine expression and morphology. Transgenic Res. 20:1235-1243.
11. Cromwell, G. L. 2002. Why and how antibiotics are used in swine production. Anim. Biotechnol. 13:7-27.
12. Ellison, R. T., III and T. J. Giehl. 1991. Killing of gram-negative bacteria by lactoferrin and lysozyme. J. Clin. Invest. 88:1080-1091.
13. Goll, D. E., G. Neti, S. W. Mares, and V. F. Thompson. 2008. Myofbrillar protein turnover: The proteasome and the calpains. J. Anim. Sci. 86:E19-E35.
14. Homma, H., E. Hoy, D. Z. Xu, Q. Lu, R. Feinman, and E. A. Deitch. 2005. The female intestine is more resistant than the male intestine to gut injury and inflammation when subjected to conditions associated with shock states. Am. J. Physiol. Gastrointest. Liver Physiol. 288:G466-G472.
15. Humphrey, B. D., N. Huang, and K. C. Klasing. 2002. Rice expressing lactoferrin and lysozyme has antibiotic-like properties when fed to chicks. J. Nutr. 132:1214-1218.
16. Kawano, M., Y. Namba, and M. Hanaoka. 1981. Regulatory factors of lymphocyte-lymphocyte interaction. I. Con A-induced mi-togenic factor acts on the late G1 stage of T-cell proliferation. Microbiol. Immunol. 25:505-515.
17. Koldovsky, O., M. Dobiasova, P. Hahn, J. Kolinska, J. Kraml, and J. Pacha. 1995. Development of gastrointestinal functions. Physiol. Res. 44:341-348.
18. Luna, L. G. 1968. Manual of histologic staining methods of the Armed Forces Institute of Pathology. 3rd ed. McGraw-Hill, New York.
19. Maga, E. A., R. L. Walker, G. B. Anderson, and J. D. Murray. 2006. Consumption of milk from transgenic goats expressing human lysozyme in the mammary gland results in the modulation of intestinal microfora. Transgenic Res. 15:515-519.
20. May, K. D., J. E. Wells, C. V. Maxwell, and W. T. Oliver. 2012. Granulated lysozyme as an alternative to antibiotics improves growth performance and small intestinal morphology of 10-day-old pigs. J. Anim. Sci. 90:1118-1125.
21. Moeser, A. J., K. A. Ryan, P. K. Nighot, and A. T. Blikslager. 2007. Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs. Am. J. Physiol. Gastrointest. Liver Physiol. 293:G413-G421.
22. NRC. 1998. Nutrient requirements of swine. 10th ed. Natl. Acad. Press, Washington, DC.
23. Nyachoti, C. M., E. Kiarie, S. K. Bhandari, G. Zhang, and D. O. Krause. 2012. Weaned pig responses to Escherichia coli K88 (ETEC) oral challenge when receiving a lysozyme-supplement. J. Anim. Sci. 90:252-260.
24. O'Mahony, F., R. Alzamora, V. Betts, F. LaPaix, D. Carter, M. Irnaten, and B. J. Harvey. 2007. Female gender-specific inhibition of KCNQ1 channels and chloride secretion by 17β-estradiol in rat distal colonic crypts. J. Biol. Chem. 282:24563-24573.
25. Oliver, W. T., S. A. Mathews, O. Phillips, E. E. Jones, J. Odle, and R. J. Harrell. 2002. Efficacy of partially hydrolyzed corn syrup solids as a replacement for lactose in manufactured liquid diets for neonatal pigs. J. Anim. Sci. 80:143-153.
26. Oliver, W. T., and J. R. Miles. 2010. A low-fat liquid diet increases protein accretion and alters cellular signaling for protein synthesis in 10-day-old pigs. J. Anim Sci. 88:2576-2584.
27. Oliver, W. T., J. R. Miles, D. E. Diaz, J. J. Dibner, G. E. Rottinghaus, and R. J. Harrell. 2012. Zearalenone enhances reproductive tract development, but does not alter skeletal muscle signaling in prepubertal gilts. Anim. Feed. Sci. Technol. 174:79-85.
28. Pacha, J. 1997. Ontogeny of Na+ transport in rat colon. Comp. Biochem. Physiol. A Physiol. 118:209-210.
29. Piva, A., E. Grilli, L. Fabbri, V. Pizzamiglio, P. P. Gatta, F. Galvano, M. Bognanno, L. Fiorentini, J. Wolinski, R. Zabielski, and J. A. Patterson. 2008. Intestinal metabolism of weaned piglets fed a typical United States or European diet with or without supplementation of tributyrin and lactitol. J. Anim. Sci. 86:2952-2961.
30. Schwarz, S., C. Kehrenberg, and T. R. Walsh. 2001. Use of antimicrobial agents in veterinary medicine and food animal production. Int. J. Antimicrob. Agents 17:431-437.
31. Shen, Y. B., X. S. Piao, S. W. Kim, L. Wang, P. Liu, I. Yoon, and Y. G. Zhen. 2009. Effects of yeast culture and supplementation on growth performance, intestinal health, and immune response of nursery pigs. J. Anim. Sci. 87:2614-2624.
32. Silhavy, T. J., D. Kahne, and S. Walker. 2010. The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2:A000414.
33. Smith, M. W. 1988. Postnatal development of transport function in the pig intestine. Comp. Biochem. Physiol. A Comp. Physiol. 90:577-582.
34. Steel, R. G. D., J. H. Torrie, and D. A. Dickey. 1997. Principles and procedures of statistics: A biomedical approach. 3rd ed. McGraw-Hill, New York.
35. Suzuki, K., and S. Fagarasan. 2008. How host-bacterial interactions lead to IgA synthesis in the gut. Trends Immunol. 29:523-531.
36. Thymann, T., K. U. Sorensen, M. S. Hedemann, J. Elnif, B. B. Jensen, H. Banga-Mboko, T. D. Leser, and P. T. Sangild. 2007. Antimicrobial treatment reduces intestinal microfora and improves protein digestive capacity without changes in villous structure in weanling pigs. Br. J. Nutr. 97:1128-1137.
37. Van den Broeck, W., E. Cox, and B. M. Goddeeris. 1999. Receptor-dependent immune responses in pigs after oral immunization with F4 fmbriae. Infect. Immun. 67:520-526.
38. Verstegen, M. W., and B. A. Williams. 2002. Alternatives to the use of antibiotics as growth promoters for monogastric animals. Anim. Biotechnol. 13:113-127.
39. Wells, J. E., N. Kalchayanand, E. D. Berry, and W. T. Oliver. 2013. Effects of antimicrobials fed as dietary growth promoters on faecal shedding of Campylobacter, Salmonella, and shiga-toxin producing Escherichia coli in swine. J. Appl. Microbiol. 114(2):318-328.
40. Zijlstra, R. T., K. Y. Whang, R. A. Easter, and J. Odle. 1996. Effect of feeding a milk replacer to early-weaned pigs on growth, body composition, and small intestinal morphology, compared with suckled littermates. J. Anim. Sci. 74:2948-2959.