CC-BY 4.0

The nisin improves broiler chicken growth performance and interacts with salinomycin in terms of gastrointestinal tract microbiota composition

M. Rawski 1,  
J. Długosz 1,  
E.M. Engberg 4,  
D. Józefiak 1  
Poznań University of Life Sciences, Department of Animal Nutrition and Feed Management, Wołyńska 33, 60-637 Poznań, Poland
Poznań University of Life Sciences, Department of Animal Physiology and Biochemistry, Wołyńska 33, 60-637 Poznań, Poland
National Research Institute of Animal Production, Department of Animal Nutrition and Feed Science, 32-083 Balice, Poland
Aarhus University, Department of Animal Science, 8830 Tiele, Denmark
J. Anim. Feed Sci. 2016;25(4):309–316
Publication date: 2016-12-15
The aim of present study was to evaluate the potential synergistic effect of salinomycin and nisin on gastrointestinal tract microbial ecology and activity as well as the influence of nisin on broiler chicken growth performance. In the first experiment, which lasted 35 days, such dietary additions as: NA – no additives, SAL – salinomycin (60 mg · kg−1 diet), NIS – nisin (2700 IU · kg−1 diet) were used. Nisin addition in comparison to salinomycin and control treatments, improved body weight gain in the entire experiment (days 1–35) as well as increased feed intake and decreased feed conversion ratio, but only in the starter period (days 1–14). In the second experiment the same dietary additions and also SAL+NIS – salinomycin and nisin (60 mg · kg−1 diet and 2700 IU · kg−1 diet, respectively) were applied. The results of the second experiment indicated that salinomycin and nisin combination decreased the total bacteria counts, as well as Enterobacteriaceae, Clostridium perfringens, Lactobacillus spp./ Enterococcus spp. and Clostridium coccoidesEubacterium rectale cluster in the ileum. Furthermore, the interaction between applied factors was noticed in the decreasing total bacteria counts, Lactobacillus spp. Enterococcus spp., Clostridium coccoides–Eubacterium rectale cluster and increasing signals from Bifidobacterium spp. as well as Streptococcus sp. Lactococcus. There were no interactions between nisin and salinomycin in terms of organic acids concentration in the crop, gizzard, ileum and caecum, as well as pH value, except gizzard. The results of the present study have indicated the positive effect of nisin on broiler growth performance and the fact that nisin and salinomycin can act synergistically in scope of ileal microbiota ecology modification.
D. Józefiak   
Poznań University of Life Sciences, Department of Animal Nutrition and Feed Management, Wołyńska 33, 60-637 Poznań, Poland
1. Alloui M.N., Szczurek W., Świątkiewicz S., 2013. The usefulness of prebiotics and probiotics in modern poultry nutrition: a review. Ann. Anim. Sci. 13, 17–32, https://doi.org/10.2478/v10220...
2. Arqués J.L., Fernández J., Gaya P., Nuñez M., Rodrìguez E., Medina M., 2004. Antimicrobial activity of reuterin in combination with nisin against food-borne pathogens. Int. J. Food Microbiol. 95, 225–229, https://doi.org/10.1016/j.ijfo.... 2004.03.009
3. Augustine P.C., Watkins K.L., Danforth H.D., 1992. Effect of monensin on ultrastructure and cellular invasion by the turkey coccidia Eimeria adenoeides and Eimeria meleagrimitis. Poultry Sci. 71, 970–978, https://doi.org/10.3382/ps.071...
4. Bjerrum L., Pedersen K., Engberg R.M., 2005. The influence of whole wheat feeding on Salmonella infection and gut flora composition in broilers. Avian Dis. 49, 9–15, https://doi. org/10.1637/7223-061504R
5. Bouttefroy A., Millière J.-B., 2000. Nisin–curvaticin 13 combinations for avoiding the regrowth of bacteriocin resistant cells of Listeria monocytogenes ATCC 15313. Int. J. Food Microbiol. 62, 65–75, https://doi.org/10.1016/S0168-...
6. Boziaris I.S., Adams M.R., 1999. Effect of chelators and nisin produced in situ on inhibition and inactivation of Gram negatives. Int. J. Food Microbiol. 53, 105–113, https://doi.org/10.1016/S0168-...
7. Brewer R., Adams M.R., Park S.F., 2002. Enhanced inactivation of Listeria monocytogenes by nisin in the presence of ethanol. Lett. Appl. Microbiol. 34, 18–21, https://doi.org/10.1046/j.1472... 765x.2002.01035.x
8. Canibe N., Højberg O., Badsberg J.H., Jensen B.B., 2007. Effect of feeding fermented liquid feed and fermented grain on gastrointestinal ecology and growth performance in piglets. J. Anim. Sci. 85, 2959–2971, https://doi.org/10.2527/jas.20...
9. Czerwiński J., Højberg O., Smulikowska S., Engberg R.M., Mieczkowska A., 2012. Effects of sodium butyrate and salinomycin upon intestinal microbiota, mucosal morphology and performance of broiler chickens. Arch. Anim. Nutr. 66, 102–116, https://doi.org/10.1080/174503...
10. Engberg R.M., Hedemann M.S., Leser T.D., Jensen B.B., 2000. Effect of zinc bacitracin and salinomycin on intestinal microflora and performance of broilers. Poultry Sci. 79, 1311–1319, https://doi.org/10.1093/ps/79....
11. Food and Drug Administration, 1988. Nisin preparation: affirmation of GRAS status as a direct human food ingredient. Fed. Reg. 53, 11247–11251
12. Franks A.H., Harmsen H.J.M., Raangs G.C., Jansen G.J., Schut F., Welling G.W., 1998. Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl. Environ. Microbiol. 64, 3336–3345
13. Gálvez A., Abriouel H., López R.L., Omar N.B., 2007. Bacteriocin-based strategies for food biopreservation. Int. J. Food Microbiol. 120, 51–70, https://doi.org/10.1016/j.ijfo...
14. Janes M.E., Kooshesh S., Johnson M.G., 2002. Control of Listeria monocytogenes on the surface of refrigerated, ready-to-eat chicken coated with edible zein film coatings containing nisin and/or calcium propionate. J. Food Sci. 67, 2754–2757, https://doi.org/10.1111/j.1365...
15. Józefiak D., Kierończyk B., Juśkiewicz J., Zduńczyk Z., Rawski M., Długosz J., Sip A., Højberg O., 2013. Dietary nisin modulates the gastrointestinal microbial ecology and enhances growth performance of the broiler chickens. PloS ONE 8, e85347, https://doi.org/10.1371/journa...
16. Józefiak D., Sip A., 2013. Bacteriocins in poultry nutrition – a review. Ann. Anim. Sci. 13, 449–462, https://doi.org/10.2478/aoas- 2013-0031
17. Józefiak D., Sip A., Rawski M., Steiner T., Rutkowski A., 2011. The dose response effects of liquid and lyophilized Carnobacterium divergens AS7 bacteriocin on the nutrient retention and performance of broiler chickens. J. Anim. Feed Sci. 20, 401–411, https://doi.org/10.22358/jafs/...
18. Józefiak D., Sip A., Rutkowski A., Rawski M., Kaczmarek S., Wołuń- Cholewa M., Engberg R.M., Højberg O., 2012. Lyophilized Carnobacterium divergens AS7 bacteriocin preparation improves performance of broiler chickens challenged with Clostridium perfringens. Poultry Sci. 91, 1899–1907, https://doi.org/10.3382/ps.201...
19. Kierończyk B., Rawski M., Długosz J., Świątkiewicz S., Józefiak D., 2016. Avian crop function – a review. Ann. Anim. Sci. 16, 653–678, https://doi.org/10.1515/aoas-2...
20. Klaver F.A., van der Meer R., 1993. The assumed assimilation of cholesterol by Lactobacilli and Bifidobacterium bifidum is due to their bile salt-deconjugating activity. Appl. Environ. Microb. 59, 1120–1124
21. Liffers S.-T., Tilkorn D.J., Stricker I., Junge C.G., Al-Benna S., Vogt M., Verdoodt B., Steinau H.-U., Tannapfel A., Tischoff I., Mirmohammadsadegh A., 2013. Salinomycin increases chemosensitivity to the effects of doxorubicin in soft tissue sarcomas. BMC Cancer 13, 490, https://doi.org/10.1186/1471-2...
22. Macfarlane G.T., Gibson G.R., 1995. Microbiological aspects of the production of short-chain fatty acids in the large bowel. In: J.H. Cummings, J.L. Rombeau, T. Sakata (Editors). Physiological and Clinical Aspects of Short-Chain Fatty Acids. Cambridge University Press, Cambridge (UK), pp. 87–105
23. Mansour M., Amri D., Bouttefroy A., Linder M., Milliere J.B., 1999. Inhibition of Bacillus licheniformis spore growth in milk by nisin, monolaurin, and pH combinations. J. Appl. Microbiol. 86, 311–324, https://doi.org/10.1046/j.1365...
24. Marteau P., Pochart P., Doré J., Béra-Maillet C., Bernalier A., Corthier G., 2001. Comparative study of bacterial groups within the human cecal and fecal microbiota. Appl. Environ. Microbiol. 67, 4939–4942, https://doi.org/10.1128/AEM.67...
25. Masuda N., 1981. Deconjugation of bile salts by Bacteroides and Clostridium. Microbiol. Immunol. 25, 1–11, https://doi.org/10.1111/j.1348...
26. Ogita A., Konishi Y., Borjihan B., Fujita K.-i., Tanaka T., 2009. Synergistic fungicidal activities of polymyxin B and ionophores, and their dependence on direct disruptive action of polymyxin B on fungal vacuole. J. Antibiot. 62, 81–87, https://doi.org/10.1038/ja.200...
27. Riddell C., Kong X.-M., 1992. The influence of diet on necrotic enteritis in broiler chickens. Avian Dis. 36, 499–503, https://doi.org/10.2307/159174....
28. Sghir A., Gramet G., Suau A., Rochet V., Pochart P., Dore J., 2000. Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization. Appl. Environ. Microbiol. 66, 2263–2266, https://doi.org/10.1128/AEM.66...
29. Teo A.Y.-L., Tan H.-M., 2005. Inhibition of Clostridium perfringens by a novel strain of Bacillus subtilis isolated from the gastrointestinal tracts of healthy chickens. Appl. Environ. Microbiol. 71, 4185–4190, https://doi.org/10.1128/AEM.71...
30. Thomas L.V., Davies E.A., Delves-Broughton J., Wimpenny J.W.T., 1998. Synergist effect of sucrose fatty acid esters on nisin inhibition of gram-positive bacteria. J. Appl. Microbiol. 85, 1013–1022, https://doi.org/10.1111/j.1365...
31. Thomas L., Isak T., 2005. Nisin synergy with natural antioxidant extracts of the herb rosemary. In: Proceedings of the Ist International Symposium on Natural Preservatives in Food Systems. Princeton (USA). Acta Hortic. 709, 109–114
32. Vescovo M., Orsi C., Scolari G., Torriani S., 1995. Inhibitory effect of selected lactic acid bacteria on microflora associated with ready-to-use vegetables. Lett. Appl. Microbiol. 21, 121–125, https://doi.org/10.1111/j.1472...
33. Zottola E.A., Yezzi T.L., Ajao D.B., Roberts R.F., 1994. Utilization of cheddar cheese containing nisin as an antimicrobial agent in other foods. Int. J. Food Microbiol. 24, 227–238, https://doi.org/10.1016/0168-1....
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