Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress

Poultry Science

Volumn 93, Issue 3, 2014, Pages 581-588

  Song, J ^a   Xiao, K ^a   Ke, Y L ^a   Jiao, L F ^a   Hu, C H ^a   Diao, Q Y ^b   Shi, B ^b   Zou, X T ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Broiler; Heat stress; Intestinal barrier; Intestinal microflora; Probiotic

Indexed keywords

AVIAN PROTEIN; PROBIOTIC AGENT; TIGHT JUNCTION PROTEIN;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; ARTICLE; BACILLUS; BROILER; CHEMISTRY; CHICKEN; DIET; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; HEAT STRESS; HISTOLOGY; INTESTINAL BARRIER; INTESTINE; INTESTINE FLORA; LACTOBACILLUS PLANTARUM; MALE; METABOLISM; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; TEMPERATURE; WESTERN BLOTTING;

BROILER; HEAT STRESS; INTESTINAL BARRIER; INTESTINAL MICROFLORA; PROBIOTIC;

ANIMAL FEED; ANIMALS; AVIAN PROTEINS; BACILLUS; BLOTTING, WESTERN; CHICKENS; DIET; GENE EXPRESSION REGULATION; HEAT-SHOCK RESPONSE; INTESTINES; LACTOBACILLUS PLANTARUM; MALE; MICROBIOTA; PROBIOTICS; TEMPERATURE; TIGHT JUNCTION PROTEINS;

EID: 84898807504     PISSN: 00325791     EISSN: 15253171     Source Type: Journal    
DOI: 10.3382/ps.2013-03455     Document Type: Article

References (39)

1. AOAC International. 2000. Official Methods of Analyses. 17th ed. W. Horwitz, ed. AOAC International, Gaithersburg, MD.
2. Bartlett, J. R., and M. O. Smith. 2003. Effects of different levels of zinc on the performance and immunocompetence of broilers under heat stress. Poult. Sci. 82:1580-1588.
3. Burkholder, K. M., K. L. Thompson, M. E. Einstein, T. J. Applegate, and J. A. Patterson. 2008. Influence of stressors on normal intestinal microbiota, intestinal morphology, and susceptibility to Salmonella Enteritidis colonization in broilers. Poult. Sci. 87:1734-1741.
4. Cosen-Binker, L. I., M. G. Binker, G. Negri, and O. Tiscornia. 2004. Influence of stress in acute pancreatitis and correlation with stress-induced gastric ulcer. Pancreatology 4:470-484.
5. Deng, W., X. F. Dong, J. M. Tong, and Q. Zhang. 2012. The probiotic Bacillus licheniformis ameliorates heat stress-induced impairment of egg production, gut morphology, and intestinal mucosal immunity in laying hens. Poult. Sci. 91:575-582.
6. Durant, J. A., D. E. Corrier, J. A. Byrd, L. H. Stanker, and S. C. Ricke. 1999. Feed deprivation affects crop environment and modulates Salmonella enteritidis colonization and invasion of leghorn hens. Appl. Environ. Microbiol. 65:1919-1923.
7. Elphick, D. A., and Y. R. Mahida. 2005. Paneth cells: Their role in innate immunity and inflammatory disease. Gut 54:1802-1809.
8. Feed Database in China. 2012. Table of Feed Composition and Nutritive Value in China. 23rd ed. China Feed, Beijing.
9. Fuller, R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66:365-378.
10. Giannenas, I., E. Papadopoulos, E. Tsalie, E. Triantafillou, S. Henikl, K. Teichmann, and D. Tontis. 2012. Assessment of dietary supplementation with probiotics on performance, intestinal morphology and microflora of chickens infected with Eimeria tenella. Vet. Parasitol. 188:31-40.
11. Hall, D. M., G. R. Buettner, L. W. Oberley, L. Xu, R. D. Matthes, and C. V. Gisolfi. 2001. Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am. J. Physiol-Heart. C. 280:H509-H521.
12. Hu, C. H., L. Y. Gu, Z. S. Luan, J. Song, and K. Zhu. 2012. Effects of montmorillonite-zinc oxide hybrid on performance, diarrhea, intestinal permeability and morphology of weanling pigs. Anim. Feed Sci. Technol. 177:108-115.
13. Hu, C. H., Z. C. Qian, J. Song, Z. S. Luan, and A. Y. Zuo. 2013a. Effects of zinc oxide-montmorillonite hybrid on growth performance, intestinal structure, and function of broiler chicken. Poult. Sci. 92:143-150.
14. Hu, C. H., K. Xiao, Z. S. Luan, and J. Song. 2013b. Early weaning increases intestinal permeability, alters expression of cytokine and tight junction proteins, and activates mitogen-activated protein kinases in pigs. J. Anim. Sci. 91:1094-1101.
15. Humphrey, T. 2006. Are happy chickens safer chickens? Poultry welfare and disease susceptibility. Br. Poult. Sci. 47:379-391.
16. Kim, J. S., S. L. Ingale, Y. W. Kim, K. H. Kim, S. Sen, M. H. Ryu, J. D. Lohakare, I. K. Kwon, and B. J. Chae. 2012. Effect of supplementation of multi-microbe probiotic product on growth performance, apparent digestibility, cecal microbiota and small intestinal morphology of broilers. J. Anim. Physiol. Anim. Nutr. 96:618-626.
17. Lambert, G. P. 2009. Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J. Anim. Sci. 87:E101-E108.
18. Lei, K. Y., and S. J. Slinger. 1970. Energy utilization in the chick in relation to certain environmental stresses. Can. J. Anim. Sci. 50:285-292.
19. Liu, F., J. Yin, M. Du, P. Yan, J. Xu, X. Zhu, and J. Yu. 2009. Heat-stress-induced damage to porcine small intestinal epithelium associated with downregulation of epithelial growth factor signaling. J. Anim. Sci. 87:1941-1949.
20. Martin, F. P., Y. Wang, N. Sprenger, I. K. Yap, T. Lundstedt, P. Lek, S. Rezzi, Z. Ramadan, P. van Bladeren, L. B. Fay, S. Kochhar, J. C. Lindon, E. Holmes, and J. K. Nicholson. 2008. Probiotic modulation of symbiotic gut microbial-host metabolic interactions in a humanized microbiome mouse model. Mol. Syst. Biol. 4:157.
21. Mevissen-Verhage, E. A., J. H. Marcelis, M. N. de Vos, A. W. Harmsen- van, and J. Verhoef. 1987. Bifidobacterium, Bacteroides, and Clostridium spp. in fecal samples from breast-fed and bottle-fed infants with and without iron supplement. J. Clin. Microbiol. 25:285-289.
22. Moeser, A. J., C. V. Klok, K. A. Ryan, J. G. Wooten, D. Little, V. L. Cook, and A. T. Blikslager. 2007. Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G173-G181.
23. Munoa, F. J., and R. Pares. 1988. Selective medium for isolation and enumeration of Bifidobacterium spp. Appl. Environ. Microbiol. 54:1715-1718.
24. Nazli, A., O. Chan, W. N. Dobson-Belaire, M. Ouellet, M. J. Tremblay, S. D. Gray-Owen, A. L. Arsenault, and C. Kaushic. 2010. Exposure to HIV-1 directly impairs mucosal epithelial barrier integrity allowing microbial translocation. PLoS Pathog. 6:e1000852.
25. NRC. 1994. Nutrient Requirements for Poultry. 9th rev. ed. Natl. Acad. Press, Washington, DC.
26. Quinteiro-Filho, W. M., A. V. S. Gomes, M. L. Pinheiro, A. Ribeiro, V. Ferraz-de-Paula, C. S. Astolfi-Ferreira, A. J. P. Ferreira, and J. Palermo-Neto. 2012. Heat stress impairs performance and induces intestinal inflammation in broiler chickens infected with Salmonella Enteritidis. Avian Pathol. 41:421-427.
27. Quinteiro-Filho, W. M., A. Ribeiro, V. Ferraz-de-Paula, M. L. Pinheiro, M. Sakai, L. R. Sa, A. J. Ferreira, and J. Palermo-Neto. 2010. Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poult. Sci. 89:1905-1914.
28. Rivera, L. R., M. Thacker, L. Pontell, H. J. Cho, and J. B. Furness. 2011. Deleterious effects of intestinal ischemia/reperfusion injury in the mouse enteric nervous system are associated with protein nitrosylation. Cell Tissue Res. 344:111-123.
29. Rodriguez-Cabezas, M. E., D. Camuesco, B. Arribas, N. Garrido- Mesa, M. Comalada, E. Bailon, M. Cueto-Sola, P. Utrilla, E. Guerra-Hernandez, C. Perez-Roca, J. Galvez, and A. Zarzuelo. 2010. The combination of fructooligosaccharides and resistant starch shows prebiotic additive effects in rats. Clin. Nutr. 29:832-839.
30. Sakurada, S., and J. R. Hales. 1998. A role for gastrointestinal endotoxins in enhancement of heat tolerance by physical fitness. J. Appl. Physiol. 84:207-214.
31. Sohail, M. U., M. E. Hume, J. A. Byrd, D. J. Nisbet, A. Ijaz, A. Sohail, M. Z. Shabbir, and H. Rehman. 2012. Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poult. Sci. 91:2235-2240.
32. Sohail, M. U., A. Ijaz, M. S. Yousaf, K. Ashraf, H. Zaneb, M. Aleem, and H. Rehman. 2010. Alleviation of cyclic heat stress in broilers by dietary supplementation of mannan-oligosaccharide and Lactobacillus-based probiotic: Dynamics of cortisol, thyroid hormones, cholesterol, C-reactive protein, and humoral immunity. Poult. Sci. 89:1934-1938.
33. Sohail, M. U., Z. U. Rahman, A. Ijaz, M. S. Yousaf, K. Ashraf, T. Yaqub, H. Zaneb, H. Anwar, and H. Rehman. 2011. Single or combined effects of mannan-oligosaccharides and probiotic supplements on the total oxidants, total antioxidants, enzymatic antioxidants, liver enzymes, and serum trace minerals in cyclic heat-stressed broilers. Poult. Sci. 90:2573-2577.
34. Song, J., Y. L. Li, and C. H. Hu. 2013. Effects of copper-exchanged montmorillonite, as alternative to antibiotic, on diarrhea, intestinal permeability and proinflammatory cytokine of weanling pigs. Appl. Clay Sci. 77-78:52-55.
35. Teeter, R. G., M. O. Smith, F. N. Owens, S. C. Arp, S. Sangiah, and J. E. Breazile. 1985. Chronic heat stress and respiratory alkalosis: Occurrence and treatment in broiler chicks. Poult. Sci. 64:1060-1064.
36. Wampler, J. L., K. P. Kim, Z. Jaradat, and A. K. Bhunia. 2004. Heat shock protein 60 acts as a receptor for the Listeria adhesion protein in Caco-2 cells. Infect. Immun. 72:931-936.
37. Xia, M. S., C. H. Hu, and Z. R. Xu. 2005. Effects of copper bearing montmorillonite on the growth performance, intestinal microflora and morphology of weanling pigs. Anim. Feed Sci. Technol. 118:307-317.
38. Xu, Z. R., C. H. Hu, M. S. Xia, X. A. Zhan, and M. Q. Wang. 2003. Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult. Sci. 82:1030-1036.
39. Zulkifli, I., N. Abdulllah, N. M. Azrin, and Y. W. Ho. 2000. Growth performance and immune response of two commercial broiler strains fed diets containing Lactobacillus cultures and oxytetracycline under heat stress conditions. Br. Poult. Sci. 41:593-597.