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Nutritional strategies to combat Salmonella in mono-gastric food animal production

Published online by Cambridge University Press:  17 November 2011

A. C. Berge  and
M. Wierup
A. C. Berge*
Affiliation:
Department of Reproduction, Obstretics and Herd Health, Unit for Veterinary Epidemiology, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium
M. Wierup
Affiliation:
Department of Biomedical Sciences and Veterinary Public Health, Swedish University of Agricultural Sciences, P.O. Box 7028; 750 07 Uppsala, Sweden
*
†E-mail: [email protected]
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Abstract

Nutritional strategies to minimize Salmonella in food animal production are one of the key components in producing safer food. The current European approach is to use a farm-to-fork strategy, where each sector must implement measures to minimize and reduce Salmonella contamination. In the pre-harvest phase, this means that all available tools need to be used such as implementation of biosecurity measures, control of Salmonella infections in animals at the farm as well as in transport and trade, optimal housing and management including cleaning, disinfection procedures as well as efforts to achieve Salmonella-free feed production. This paper describes some nutritional strategies that could be used in farm control programmes in the major mono-gastric food production animals: poultry and pigs. Initially, it is important to prevent the introduction of Salmonella onto the farm through Salmonella-contaminated feed and this risk is reduced through heat treatment and the use of organic acids and their salts and formaldehyde. Microbiological sampling and monitoring for Salmonella in the feed mills is required to minimize the introduction of Salmonella via feed onto the farm. In addition, feed withdrawal may create a stressful situation in animals, resulting in an increase in Salmonella shedding. Physical feed characteristics such as coarse-ground meal to pigs can delay gastric emptying, thereby increasing the acidity of the gut and thus reducing the possible prevalence of Salmonella. Coarse-ground grains and access to litter have also been shown to decrease Salmonella shedding in poultry. The feed can also modify the gastro-intestinal tract microflora and influence the immune system, which can minimize Salmonella colonization and shedding. Feed additives, such as organic acids, short- and medium-chain fatty acids, probiotics, including competitive exclusion cultures, prebiotics and certain specific carbohydrates, such as mannan-based compounds, egg proteins, essential oils and bacteriophages, have the potential to reduce Salmonella levels when added to the feed. These nutritional strategies could be evaluated and used in farm control programmes.

Keywords

Salmonella controlnutritionpoultrypigssupplements
Type
Full Paper
Information
animal , Volume 6 , Issue 4 , April 2012 , pp. 557 - 564
Copyright
Copyright © The Animal Consortium 2011

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References

Beloeil, PA, Fravalo, P, Fablet, C, Jolly, JP, Eveno, E, Hascoet, Y, Chauvin, C, Salvat, G, Madec, F 2004. Risk factors for Salmonella enterica subsp. enterica shedding by market-age pigs in French farrow-to-finish herds. Preventive Veterinary Medicine 63, 103–120.CrossRefGoogle ScholarPubMed
Binter, C, Straver, JM, Häggblom, P, Bruggeman, G, Lindqvist, PA, Zentek, J, Andersson, MG 2011. Transmission and control of Salmonella in the pig feed chain: a conceptual model. International Journal of Food Microbiology 145 (suppl. 1), S7–S17.CrossRefGoogle Scholar
Boyen, F, Haesebrouck, F, Vanparys, A, Volf, J, Mahu, M, Van Immerseel, F, Rychlik, I, Dewulf, J, Ducatelle, R, Pasmans, F 2008. Coated fatty acids alter virulence properties of Salmonella Typhimurium and decrease intestinal colonization of pigs. Veterinary Microbiology 132, 319–327.CrossRefGoogle ScholarPubMed
Boyle, EC, Bishop, JL, Grassl, GA, Finlay, BB 2007. Salmonella: from pathogenesis to therapeutics. Journal of Bacteriology 189, 1489–1495.CrossRefGoogle ScholarPubMed
Burt, S 2004. Essential oils: their antibacterial properties and potential applications in foods – a review. International Journal of Food Microbiology 94, 223–253.CrossRefGoogle ScholarPubMed
Callaway, TR, Edrington, TS, Brabban, A, Kutter, B, Karriker, L, Stahl, C, Wagstrom, E, Anderson, R, Poole, TL, Genovese, K, Krueger, N, Harvey, R, Nisbet, DJ 2011. Evaluation of phage treatment as a strategy to reduce Salmonella populations in growing swine. Foodborne Pathogens and Disease 8, 261–266.CrossRefGoogle ScholarPubMed
Carrique-Mas, JJ, Bedford, S, Davies, RH 2007. Organic acid and formaldehyde treatment of animal feeds to control Salmonella: efficacy and masking during culture. Journal of Applied Microbiology 103, 88–96.CrossRefGoogle ScholarPubMed
Casey, PG, Casey, GD, Gardiner, GE, Tangney, M, Stanton, C, Ross, RP, Hill, C, Fitzgerald, GF 2004. Isolation and characterization of anti-Salmonella lactic acid bacteria from the porcine gastrointestinal tract. Letters in Applied Microbiology 39, 431–438.CrossRefGoogle ScholarPubMed
Casey, PG, Gardiner, GE, Casey, G, Bradshaw, B, Lawlor, PG, Lynch, PB, Leonard, FC, Stanton, C, Ross, RP, Fitzgerald, GF, Hill, C 2007. A five-strain probiotic combination reduces pathogen shedding and alleviates disease signs in pigs challenged with Salmonella enterica Serovar Typhimurium. Applied Environmental Microbiology 73, 1858–1863.CrossRefGoogle ScholarPubMed
Davies, PR, Scott, HH, Funk, JA, Fedorka-Cray, PJ, Jones, FT 2004. The role of contaminated feed in the epidemiology and control of Salmonella enterica in pork production. Foodborne Pathogens and Disease 1, 202–215.CrossRefGoogle ScholarPubMed
Davies, RH, Wales, AD 2010. Investigations into Salmonella contamination in poultry feedmills in the United Kingdom. Journal of Applied Microbiology 109, 1430–1440.CrossRefGoogle ScholarPubMed
De Busser, EV, Dewulf, J, Nollet, N, Houf, K, Schwarzer, K, De Sadeleer, L, De Zutter, L, Maes, D 2009. Effect of organic acids in drinking water during the last 2 weeks prior to slaughter on Salmonella shedding by slaughter pigs and contamination of carcasses. Zoonoses and Public Health 56, 129–136.CrossRefGoogle ScholarPubMed
Durant, JA, Corrier, DE, Stanker, LH, Ricke, SC 2000. Expression of the hilA Salmonella typhimurium gene in a poultry Salm. enteritidis isolate in response to lactate and nutrients. Journal of Applied Microbiology 89, 63–69.CrossRefGoogle Scholar
Durant, JA, Corrier, DE, Byrd, JA, Stanker, LH, Ricke, SC 1999. Feed deprivation affects crop environment and modulates Salmonella enteritidis colonization and invasion of leghorn hens. Applied Environmental Microbiology 65, 1919–1923.CrossRefGoogle ScholarPubMed
EFSA 2008. Microbiological risk assessment in feedingstuffs for food-producing animals. EFSA Journal 720, 1–84.Google Scholar
EFSA 2010. The community summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA Journal 8, 1496–1906.CrossRefGoogle Scholar
EFSA 2011. Analysis of the baseline survey on the prevalence of Salmonella in holdings with breeding pigs, in the EU, 2008 – Part B: factors associated with Salmonella pen positivity. EFSA Journal 9, 1–158.Google Scholar
European Commission 2003. REGULATION (EC) No 2160/2003 of the European parliament and of the council of 17 November 2003 on the control of Salmonella and other specified food-borne zoonotic agents. Official Journal of the European Union L325, 1–15.Google Scholar
European Commission 2011. European Union Register of Feed Additives Pursuant to Regulation (EC) No. 1831/2003, Appendixes 3 and 4. Retrieved November 7, 2011, from http://ec.europa.eu/food/food/animalnutrition/feedadditives/comm_register_feed_additives_1831-03.pdfGoogle Scholar
FAO/WHO 2001. Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Joint FAO/WHO Expert Consultation. Retrieved November 7, 2011, from from http://www.who.int/foodsafety/publications/fs_management/probiotics/en/Google Scholar
Farzan, A, Friendship, RM, Dewey, CE, Poppe, C, Funk, J 2010. Evaluation of the risk factors for shedding Salmonella with or without antimicrobial resistance in swine using multinomial regression method. Zoonoses and Public Health 57 (suppl. 1), 85–93.CrossRefGoogle ScholarPubMed
Farzan, A, Friendship, RM, Dewey, CE, Warriner, K, Poppe, C, Klotins, K 2006. Prevalence of Salmonella spp. on Canadian pig farms using liquid or dry-feeding. Preventive Veterinary Medicine 73, 241–254.CrossRefGoogle ScholarPubMed
Fedorka-Cray, PJ, Bailey, JS, Stern, NJ, Cox, NA, Ladely, SR, Musgrove, M 1999. Mucosal competitive exclusion to reduce Salmonella in swine. Journal of Food Protection 62, 1376–1380.CrossRefGoogle ScholarPubMed
Genovese, KJ, Anderson, RC, Harvey, RB, Callaway, TR, Poole, TL, Edrington, TS, Fedorka-Cray, PJ, Nisbet, DJ 2003. Competitive exclusion of Salmonella from the gut of neonatal and weaned pigs. Journal of Food Protection 66, 1353–1359.CrossRefGoogle ScholarPubMed
Gibson, GR, McCartney, AL, Rastall, RA 2005. Prebiotics and resistance to gastrointestinal infections. British Journal of Nutrition 93 (suppl. 1), 31–34.CrossRefGoogle ScholarPubMed
Golden, NJ, Marks, HH, Coleman, ME, Schroeder, CM, Bauer, NE Jr, Schlosser, WD 2008. Review of induced molting by feed removal and contamination of eggs with Salmonella enterica serovar Enteritidis. Veterinary Microbiology 131, 215–228.CrossRefGoogle ScholarPubMed
Hedemann, MS, Mikkelsen, LL, Naughton, PJ, Jensen, BB 2005. Effect of feed particle size and feed processing on morphological characteristics in the small and large intestine of pigs and on adhesion of Salmonella enterica serovar Typhimurium DT12 in the ileum in vitro. Journal of Animal Science 83, 1554–1562.CrossRefGoogle ScholarPubMed
Henzler, DJ, Opitz, HM 1992. The role of mice in the epizootiology of Salmonella enteritidis infection on chicken layer farms. Avian Diseases 36, 625–631.CrossRefGoogle ScholarPubMed
Higgins, SE, Erf, GF, Higgins, JP, Henderson, SN, Wolfenden, AD, Gaona-Ramirez, G, Hargis, BM 2007. Effect of probiotic treatment in broiler chicks on intestinal macrophage numbers and phagocytosis of Salmonella Enteritidis by abdominal exudate cells. Poultry Science 86, 2315–2321.CrossRefGoogle ScholarPubMed
Higgins, JP, Higgins, SE, Wolfenden, AD, Henderson, SN, Torres-Rodriguez, A, Vicente, JL, Hargis, BM, Tellez, G 2010. Effect of lactic acid bacteria probiotic culture treatment timing on Salmonella Enteritidis in neonatal broilers. Poultry Science 89, 243–247.CrossRefGoogle ScholarPubMed
Himathongkham, S, Pereira, MG, Riemann, H 1996. Heat destruction of Salmonella in poultry feed: effect of time, temperature, and moisture. Avian Diseases 40, 72–77.CrossRefGoogle ScholarPubMed
Hong, HA, Duc Le, H, Cutting, SM 2005. The use of bacterial spore formers as probiotics. FEMS Microbiology Reviews 29, 813–835.CrossRefGoogle ScholarPubMed
Jones, FT 2011. A review of practical Salmonella control measures in animal feed. Journal of Applied Poultry Research 20, 102–113.CrossRefGoogle Scholar
Jones, FT, Richardson, KE 2004. Salmonella in commercially manufactured feeds. Poultry Science 83, 384–391.CrossRefGoogle ScholarPubMed
Kaldhusdal, M, Schneitz, C, Hofshagen, M, Skjerve, E 2001. Reduced incidence of Clostridium perfringens-associated lesions and improved performance in broiler chickens treated with normal intestinal bacteria from adult fowl. Avian Diseases 45, 149–156.CrossRefGoogle ScholarPubMed
Kassaify, ZG, Mine, Y 2004a. Effect of food protein supplements on Salmonella Enteritidis infection and prevention in laying hens. Poultry Science 83, 753–760.CrossRefGoogle ScholarPubMed
Kassaify, ZG, Mine, Y 2004b. Nonimmunized egg yolk powder can suppress the colonization of Salmonella Typhimurium, Escherichia coli O157:H7, and Campylobacter jejuni in laying hens. Poultry Science 83, 1497–1506.CrossRefGoogle ScholarPubMed
Kassaify, ZG, Li, EW, Mine, Y 2005. Identification of antiadhesive fraction(s) in nonimmunized egg yolk powder: in vitro study. Journal of Agricultural Food Chemistry 53, 4607–4614.CrossRefGoogle ScholarPubMed
Line, JE, Bailey, JS, Cox, NA, Stern, NJ 1997. Yeast treatment to reduce Salmonella and Campylobacter populations associated with broiler chickens subjected to transport stress. Poultry Science 76, 1227–1231.CrossRefGoogle ScholarPubMed
Line, JE, Bailey, JS, Cox, NA, Stern, NJ, Tompkins, T 1998. Effect of yeast-supplemented feed on Salmonella and Campylobacter populations in broilers. Poultry Science 77, 405–410.CrossRefGoogle ScholarPubMed
Lo Fo Wong, DM, Dahl, J, Stege, H, van der Wolf, PJ, Leontides, L, von Altrock, A, Thorberg, BM 2004. Herd-level risk factors for subclinical Salmonella infection in European finishing-pig herds. Preventive Veterinary Medicine 62, 253–266.CrossRefGoogle ScholarPubMed
Malorny, B, Lofstrom, C, Wagner, M, Kramer, N, Hoorfar, J 2008. Enumeration of Salmonella bacteria in food and feed samples by real-time PCR for quantitative microbial risk assessment. Applied and Environmental Microbiology 74, 1299–1304.CrossRefGoogle ScholarPubMed
Marin, C, Balasch, S, Vega, S, Lainez, M 2011. Sources of Salmonella contamination during broiler production in Eastern Spain. Preventive Veterinary Medicine 98, 39–45.CrossRefGoogle ScholarPubMed
Mead, G, Lammerding, AM, Cox, N, Doyle, MP, Humbert, F, Kulikovskiy, A, Panin, A, do Nascimento, V, Wierup, M 2010. Scientific and technical factors affecting the setting of Salmonella criteria for raw poultry: a global perspective. Journal of Food Protection 73, 1566–1590.CrossRefGoogle ScholarPubMed
Messens, W, Goris, J, Dierick, N, Herman, L, Heyndrickx, M 2010. Inhibition of Salmonella Typhimurium by medium-chain fatty acids in an in vitro simulation of the porcine cecum. Veterinary Microbiology 141, 73–80.CrossRefGoogle Scholar
Mikkelsen, LL, Naughton, PJ, Hedemann, MS, Jensen, BB 2004. Effects of physical properties of feed on microbial ecology and survival of Salmonella enterica serovar Typhimurium in the pig gastrointestinal tract. Applied and Environmental Microbiology 70, 3485–3492.CrossRefGoogle ScholarPubMed
Molla, B, Sterman, A, Mathews, J, Artuso-Ponte, V, Abley, M, Farmer, W, Rajala-Schultz, P, Morrow, WE, Gebreyes, WA 2010. Salmonella enterica in commercial swine feed and subsequent isolation of phenotypically and genotypically related strains from fecal samples. Applied and Environmental Microbiology 76, 7188–7193.CrossRefGoogle ScholarPubMed
Morrow, WE, See, MT, Eisemann, JH, Davies, PR, Zering, K 2002. Effect of withdrawing feed from swine on meat quality and prevalence of Salmonella colonization at slaughter. Journal of American Veterinary Medical Association 220, 497–502.CrossRefGoogle ScholarPubMed
Nurmi, E, Nuotio, L, Schneitz, C 1992. The competitive exclusion concept: development and future. International Journal of Food Microbiology 15, 237–240.CrossRefGoogle Scholar
O'Bryan, CA, Crandall, PG, Chalova, VI, Ricke, SC 2008. Orange essential oils antimicrobial activities against Salmonella spp. Journal of Food Science 73, M264–M267.CrossRefGoogle ScholarPubMed
O'Connor, AM, Denagamage, T, Sargeant, JM, Rajic, A, McKean, J 2008. Feeding management practices and feed characteristics associated with Salmonella prevalence in live and slaughtered market-weight finisher swine: a systematic review and summation of evidence from 1950 to 2005. Preventive Veterinary Medicine 87, 213–228.CrossRefGoogle ScholarPubMed
Oyofo, BA, DeLoach, JR, Corrier, DE, Norman, JO, Ziprin, RL, Mollenhauer, HH 1989. Prevention of Salmonella Typhimurium colonization of broilers with D-mannose. Poultry Science 68, 1357–1360.CrossRefGoogle ScholarPubMed
Price, KL, Totty, HR, Lee, HB, Utt, MD, Fitzner, GE, Yoon, I, Ponder, MA, Escobar, J 2010. Use of Saccharomyces cerevisiae fermentation product on growth performance and microbiota of weaned pigs during Salmonella infection. Journal of Animal Science 88, 3896–3908.CrossRefGoogle ScholarPubMed
Rahimi, S, Shiraz, ZM, Salehi, TZ, Torshizi, AK, Grimes, JL 2007. Prevention of Salmonella infection in poultry by specific egg-derived antibody. International Journal of Poultry Science 6, 230–235.CrossRefGoogle Scholar
Rattanachaikunsopon, P, Phumkhachorn, P 2010. Antimicrobial activity of basil (Ocimum basilicum) oil against Salmonella Enteritidis in vitro and in food. Bioscience Biotechnology and Biochemistry 74, 1200–1204.CrossRefGoogle ScholarPubMed
Ricke, SC 2003. The gastrointestinal tract ecology of Salmonella Enteritidis colonization in molting hens. Poultry Science 82, 1003–1007.CrossRefGoogle ScholarPubMed
Roberfroid, M, Gibson, GR, Hoyles, L, McCartney, AL, Rastall, R, Rowland, I, Wolvers, D, Watzl, B, Szajewska, H, Stahl, B, Guarner, F, Respondek, F, Whelan, K, Coxam, V, Davicco, MJ, Leotoing, L, Wittrant, Y, Delzenne, NM, Cani, PD, Neyrinck, AM, Meheust, A 2010. Prebiotic effects: metabolic and health benefits. British Journal of Nutrition 104 (suppl. 2), S1–S63.CrossRefGoogle ScholarPubMed
Santos, FB, Sheldon, BW, Santos, AA Jr, Ferket, PR 2008. Influence of housing system, grain type, and particle size on Salmonella colonization and shedding of broilers fed triticale or corn–soybean meal diets. Poultry Science 87, 405–420.CrossRefGoogle ScholarPubMed
Schneitz, C, Nuotio, L, Mead, G, Nurmi, E 1992. Competitive exclusion in the young bird: challenge models, administration and reciprocal protection. International Journal of Food Microbiology 15, 241–244.CrossRefGoogle Scholar
Spring, P, Wenk, C, Dawson, KA, Newman, KE 2000. The effects of dietary mannan-oligosaccharides on cecal parameters and the concentrations of enteric bacteria in the ceca of Salmonella-challenged broiler chicks. Poultry Science 79, 205–211.CrossRefGoogle Scholar
Stern, NJ, Cox, NA, Bailey, JS, Berrang, ME, Musgrove, MT 2001. Comparison of mucosal competitive exclusion and competitive exclusion treatment to reduce Salmonella and Campylobacter spp. colonization in broiler chickens. Poultry Science 80, 156–160.CrossRefGoogle ScholarPubMed
Ten Bruggencate, SJ, Bovee-Oudenhoven, IM, Lettink-Wissink, ML, Katan, MB, van der Meer, R 2004. Dietary fructo-oligosaccharides and inulin decrease resistance of rats to Salmonella: protective role of calcium. Gut 53, 530–535.CrossRefGoogle ScholarPubMed
Torres, GJ, Piquer, FJ, Algarra, L, de Frutos, C, Sobrino, OJ 2011. The prevalence of Salmonella enterica in Spanish feed mills and potential feed-related risk factors for contamination. Preventive Veterinary Medicine 98, 81–87.CrossRefGoogle ScholarPubMed
van der Wolf, PJ, Bongers, JH, Elbers, AR, Franssen, FM, Hunneman, WA, van Exsel, AC, Tielen, MJ 1999. Salmonella infections in finishing pigs in The Netherlands: bacteriological herd prevalence, serogroup and antibiotic resistance of isolates and risk factors for infection. Veterinary Microbiology 67, 263–275.CrossRefGoogle ScholarPubMed
van der Wolf, PJ, Wolbers, WB, Elbers, AR, van der Heijden, HM, Koppen, JM, Hunneman, WA, van Schie, FW, Tielen, MJ 2001. Herd level husbandry factors associated with the serological Salmonella prevalence in finishing pig herds in the Netherlands. Veterinary Microbiology 78, 205–219.CrossRefGoogle ScholarPubMed
Van Hoorebeke, S, Van Immerseel, F, Schulz, J, Hartung, J, Harisberger, M, Barco, L, Ricci, A, Theodoropoulos, G, Xylouri, E, De Vylder, J, Ducatelle, R, Haesebrouck, F, Pasmans, F, de Kruif, A, Dewulf, J 2010. Determination of the within and between flock prevalence and identification of risk factors for Salmonella infections in laying hen flocks housed in conventional and alternative systems. Preventive Veterinary Medicine 94, 94–100.CrossRefGoogle ScholarPubMed
Van Immerseel, F, Russell, JB, Flythe, MD, Gantois, I, Timbermont, L, Pasmans, F, Haesebrouck, F, Ducatelle, R 2006. The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy. Avian Pathology 35, 182–188.CrossRefGoogle ScholarPubMed
Van Immerseel, F, De Buck, J, Boyen, F, Bohez, L, Pasmans, F, Volf, J, Sevcik, M, Rychlik, I, Haesebrouck, F, Ducatelle, R 2004. Medium-chain fatty acids decrease colonization and invasion through hilA suppression shortly after infection of chickens with Salmonella enterica serovar Enteritidis. Applied and Environmental Microbiology 70, 3582–3587.CrossRefGoogle ScholarPubMed
Wales, AD, Allen, VM, Davies, RH 2010. Chemical treatment of animal feed and water for the control of Salmonella. Foodborne Pathogens and Disease 7, 3–15.CrossRefGoogle ScholarPubMed
Wierup, M, Häggblom, P 2010. An assessment of soybeans and other vegetable proteins as source of Salmonella contamination in pig production. Acta Veterinaria Scandinavia 52, 1–9.Google ScholarPubMed
Wierup, M, Wahlström, H, Engström, B 1992. Experience of a 10-year use of competitive exclusion treatment as part of the Salmonella control programme in Sweden. International Journal of Food Microbiology 15, 287–291.CrossRefGoogle ScholarPubMed
Zhang, G, Ma, L, Doyle, MP 2007. Potential competitive exclusion bacteria from poultry inhibitory to Campylobacter jejuni and Salmonella. Journal of Food Protection 70, 867–873.CrossRefGoogle ScholarPubMed