Implications
The control of Salmonella in food animal production is of high priority. The European Union approach includes pre-harvest controls in poultry and pig production. Nutritional interventions to modify the gastro-intestinal environment have been shown to be useful tools to reduce Salmonella shedding in live animals. The dynamic and multi-factorial nature of Salmonella infections and the varying Salmonella prevalence in various production systems make it difficult to predict the effects of nutritional interventions on the Salmonella status of animals. This review aims to provide the reader a brief overview of the current nutritional strategies to control Salmonella in poultry and pigs.
Introduction
Salmonella enterica subspecies enterica (hereafter referred to as Salmonella) is a worldwide public health hazard and, despite extensive research and scientific knowledge, the bacterium continues to cause significant human morbidity and mortality, and increasing levels of antimicrobial resistance are causing concern (Boyle et al., Reference Boyle, Bishop, Grassl and Finlay2007). The European Union (EU) has shown clear initiatives to take on the challenge of reducing Salmonella in food animal production (EU Regulation 2160/2003). Post-harvest measures, such as hygienic slaughtering, processing and storage routines, can minimize the risks of Salmonella to consumers but they have yet to result in a sufficient reduction in human salmonellosis cases. The EU Member States have a very diverse Salmonella situation, ranging from negligible levels and a non-acceptance policy for Salmonella in the food animal production to a high prevalence with limited control measures in addition to those determined by the EU. The dominant serotypes of Salmonella vary between regions and countries. Most serotypes do not cause clinical disease in animals but are more of a public health concern.
The EU has enhanced the monitoring and control of Salmonella in food animal production and increasing focus has been placed on pre-harvest controls and surveillance. The Salmonella control programmes in poultry have proven effective in many countries and a reduction in human cases has been attributed to lower levels of Salmonella in layers and a reduced transmission to eggs (EFSA, 2010). EU countries are now also facing the challenge of minimizing Salmonella in pig production.
Good internal and external biosecurity measures are key components of Salmonella control programmes to avoid the introduction of Salmonella onto the farm or to reduce infection pressure when Salmonella is present. The importance of minimizing the introduction of Salmonella through the purchase of animals cannot be overemphasized and focus is placed on cleaning up the breeding herds. Hygienic measures should take into account animals, housing, management, cleaning and disinfection. Feed plays a significant role in the control of Salmonella on two levels. First, the feed may potentially be an important vector to introduce Salmonella onto the farm. Proper control programmes must, therefore, be in place at any feed manufacturing site, as well as on the farm to avoid ingestion of Salmonella by the animals. Second, when animals are exposed to Salmonella through feed and other sources, feed composition, texture and supplements can be used to additionally minimize the risk of colonization and shedding of Salmonella. This paper will present a non-exhaustive list of major examples of how feed and feed supplements can be tools to use in Salmonella control programmes.
The inclusion of feed additives for the control of Salmonella has yielded varying results and often the products and their inclusion rates have not been properly evaluated in clinical and field studies. One reason is that Salmonella culture methods have low sensitivity, although new strategies, such as real-time PCR methodology, are being developed (Malorny et al., Reference Malorny, Lofstrom, Wagner, Kramer and Hoorfar2008). Furthermore, the stochastic nature of Salmonella infections on farms makes it difficult to evaluate differences in intervention studies, especially if the studies are carried out in the field in regions where Salmonella frequently occurs in the production of that animal and the environment, as is the situation in most countries. Therefore, many strategies yield inconsistent results across studies and clinical trial results often cannot be directly transferred to practical use on farm. The purpose of this review is not to provide an extensive and all-inclusive list of publications on the subject but to aid the reader to see the overall nutritional-related strategies that can be considered in a Salmonella control programme.
Control of Salmonella in feed
Salmonella is frequently found in feed ingredients, especially protein-rich feed sources (Wierup and Häggblom, Reference Wierup and Häggblom2010). Salmonella may also be found in compounded feed and even in heat-treated and pelleted feed due to environmental contamination of feed mills and the high likelihood for cross contamination in the feed mill and during transport and storage at the farm (Binter et al., Reference Binter, Straver, Häggblom, Bruggeman, Lindqvist, Zentek and Andersson2011; Jones, Reference Jones2011). The difficulties in sampling and culturing Salmonella from feed sources may lead to an underestimation of this risk (Davies and Wales, Reference Davies and Wales2010). Many studies indicate and have shown that contaminated feed is a risk for the introduction of Salmonella onto the farm (Davies et al., Reference Davies, Scott, Funk, Fedorka-Cray and Jones2004; Molla et al., Reference Molla, Sterman, Mathews, Artuso-Ponte, Abley, Farmer, Rajala-Schultz, Morrow and Gebreyes2010). However, the role of contaminated animal feed as a risk for human salmonellosis from an individual farm may vary depending on many production systems and management approaches (Marin et al., Reference Marin, Balasch, Vega and Lainez2011; Torres et al., Reference Torres, Piquer, Algarra, de Frutos and Sobrino2011).
Heat treatment, usually during conditioning, pelleting or extrusion, has been shown to be an effective way to reduce microbial loads in feed materials and compound feed. Different studies have verified the Salmonella-reducing effect of heat treatment (Himathongkham et al., Reference Himathongkham, Pereira and Riemann1996). Heating between 80°C and 85°C for 1 min in most cases should eliminate Salmonella (Jones and Richardson, Reference Jones and Richardson2004). However, the elimination is dependent on the level of contamination (Himathongkham et al., Reference Himathongkham, Pereira and Riemann1996) and the set temperature and time range may not be reached in all parts of the feed. Heat treatment for more than 30 s at more than 75°C can achieve a 1000-fold (3 log) reduction of Salmonella. Acidification can be used to decrease the risk of introducing Salmonella-contaminated feed ingredients into feed mills (Wierup and Häggblom, Reference Wierup and Häggblom2010). Organic acids have varying capacity to inactivate Salmonella in feed and it should be noted that they may also mask the presence of viable Salmonella that have not been completely inactivated by the acid treatment. The best efficacy results and lowest masking were achieved for a formaldehyde-containing product (Carrique-Mas et al., Reference Carrique-Mas, Bedford and Davies2007). A thorough review of the use of various chemicals to reduce Salmonella contamination of feed contamination has recently been published (Wales et al., Reference Wales, Allen and Davies2010).
Nutritional Salmonella control strategies
Nutritional Salmonella intervention methods can be carried out via general diet formulation or feed additives. Through diet formulation, the availability of fermentable substrate and buffering capacity can be influenced. The enteric microbial population is highly influenced by diet, and any dietary change is likely to influence the microbial flora. A number of feed additives have gained commercial acceptance in helping to reduce Salmonella. The list of EU-approved additives according to Regulation EC No. 1831/2003 is continually being modified (European Commission, 2011).
Feed deprivation effects
Poultry
Egg producers sometimes induce a moult in older hens to improve productivity and decrease mortality of hens compared with non-moulted hens of the same age. The most common method is feed restriction for 10 to 14 days, combined with a reduction in the light period. It has been shown that moulting of layer hens can result in increased Salmonella shedding. Moulting hens in a Salmonella-infected flock may lead to an increased dissemination of the microbe as well as an increase in the number of Salmonella-contaminated eggs laid (Ricke, Reference Ricke2003; Golden et al., Reference Golden, Marks, Coleman, Schroeder, Bauer and Schlosser2008). Feed withdrawal changes the crop environment, resulting in an increased pH and decreased concentrations of lactate, glucose and amino acids compared with non-moulted birds. The first environment that Salmonella encounters when ingested is the crop and the crop environment can, therefore, influence the survival and virulence of Salmonella not only in the crop but also in the distal part of the intestinal tract. Studies were carried out comparing moulted hens with non-moulted hens that were experimentally infected with Salmonella Enteritidis. The moulted birds had greater Salmonella colonization of the crop and caeca and an increased invasion of the spleen and liver compared with the non-moulted birds (Durant et al., Reference Durant, Corrier, Byrd, Stanker and Ricke1999 and Reference Durant, Corrier, Stanker and Ricke2000).
Pigs
Pre-slaughter feed withdrawal in pigs has been used as a method of reducing carcass contamination that can be caused by digestive tract rupturing or faeces spilling onto the carcass. Faecal contamination of the carcass is a major food safety risk during slaughter. Traditionally, it was believed that pre-slaughter feed withdrawal can increase Salmonella shedding from pigs due to the stress created by fasting. However, recent research has showed that feed withdrawal may not be directly associated with Salmonella shedding and it is more likely caused by contaminated holding areas before slaughter, where pigs from different sources are mixed and held together (Morrow et al., Reference Morrow, See, Eisemann, Davies and Zering2002).
Organic acids
Organic acids may have dual functions in reducing Salmonella contamination. First, they may reduce Salmonella load in the feed and, second, they may reduce the potential for infection and shedding in the animal. Short-chain fatty acids (SCFA), such as formic, acetic, propionic and butyric acids, have all been shown to have an inhibitory effect on Salmonella growth (Van Immerseel et al., Reference Van Immerseel, Russell, Flythe, Gantois, Timbermont, Pasmans, Haesebrouck and Ducatelle2006). The bacteria, that are unable to decrease intracellular pH accumulate, accumulate organic acid anions according to their pH gradient across their cell membranes. SCFA butyrate specifically downregulates the expression of invasion genes in Salmonella spp. at low doses (Van Immerseel et al., Reference Van Immerseel, Russell, Flythe, Gantois, Timbermont, Pasmans, Haesebrouck and Ducatelle2006). The acids are usually added at a 0.5% to 3% inclusion rate depending on the buffering capacity of the feed and the acid. Acid-buffering capacity is the lowest in cereals and cereal by-products, higher in protein feedstuffs and the highest in minerals. These acids are often coated or encapsulated to protect them until they reach the lower intestine, where they are effective. Medium-chain fatty acids (MCFA), such as caproic, caprylic and capric acid, may have greater antibacterial properties against Salmonella than SCFA (Van Immerseel et al., Reference Van Immerseel, Russell, Flythe, Gantois, Timbermont, Pasmans, Haesebrouck and Ducatelle2006). The use of organic acids in feed and water may benefit overall animal performance through improved gut health.
Poultry
MCFA, caproic, caprylic and capric acid, were evaluated for the control of S. Enteritidis in chickens. The results suggested that MCFA decrease the ability of Salmonella spp. to invade epithelial cells, resulting in a reduction in the numbers of bacteria in vivo (Van Immerseel et al., Reference Van Immerseel, De Buck, Boyen, Bohez, Pasmans, Volf, Sevcik, Rychlik, Haesebrouck and Ducatelle2004).
Pigs
The reductions in Salmonella infection through the addition of various acids have not been consistent (O'Connor et al., Reference O'Connor, Denagamage, Sargeant, Rajic and McKean2008). Belgian research teams have been active in trying to find an acid to control Salmonella in pig production. A study evaluated four SCFA (formic acid, acetic acid, propionic acid and butyric acid) and two MCFA (caproic and caprylic acid) in vitro and in vivo in pigs experimentally infected with Salmonella. Coated butyric acid decreased Salmonella levels in pig caecal content, whereas uncoated acids did not (Boyen et al., Reference Boyen, Haesebrouck, Vanparys, Volf, Mahu, Van Immerseel, Rychlik, Dewulf, Ducatelle and Pasmans2008). Another in vitro laboratory study simulating the porcine caecum evaluated the influence of sodium caproate, sodium caprylate and sodium caprinate on Salmonella growth. The study indicated that Salmonella could be inhibited by caprylate. It was concluded that caprylate, in the form of encapsulated beads or as triacylglycerol oil, might have potential as a Salmonella-reducing additive in pig feed (Messens et al., Reference Messens, Goris, Dierick, Herman and Heyndrickx2010). A Belgian study (four herds, 600 pigs) investigated the effect of acidifying the water before slaughter. Treatment groups received acidified drinking water (pH = 3.6 to 4.0) and the control group received non-treated water (pH = 7.8 to 8.5) within 2 weeks before slaughter. The strategic application of a mixture of organic acids (formic, propionic, acetic and sorbic acid) in water during the last 2 weeks before slaughter did not seem to reduce Salmonella shedding and contamination of pigs shortly before and during slaughter (De Busser et al., Reference De Busser, Dewulf, Nollet, Houf, Schwarzer, De Sadeleer, De Zutter and Maes2009).
Physical properties of feed
The physical properties of feed greatly influence the passage and absorption of nutrients in the digestive tract and have been shown to influence Salmonella colonization and shedding in both poultry and pigs.
Poultry
Salmonella colonization in poultry may be influenced by grain type and particle size. A study was carried out investigating feeding coarse compared with fine-ground corn–soyabean meal and coarse ground with whole triticale–soyabean meal in broilers housed in cages and on litter (Santos et al., Reference Santos, Sheldon, Santos and Ferket2008). Feeding the whole or coarsely ground grains decreased caecal Salmonella populations in the 42-day-old broilers.
Pigs
The physical properties of feed have been shown to influence the susceptibility of pigs to Salmonella. Several epidemiological studies have identified that different forms of feed are associated with Salmonella prevalence in the herd. It is important to distinguish between the different forms of feed that may be included in these studies. Pelleting of pig feed is mainly carried out to improve feed conversion and not as a Salmonella control measure as it is in poultry production. In the wet feeding practice, the feed ingredients are simply mixed in water and distributed through tubes by pumps and the feed pH is almost neutral. Producers may include food industry by-products in the wet feeding system that may slightly reduce the pH, such as whey. Wet feed should not be confused with fermented wet feed, in which the wet feed after supplementation by selected lactic acid bacteria is allowed to ferment under controlled conditions, resulting in a feed with a pH < 4.
Studies in the Netherlands have indicated that liquid feed containing fermented by-products was associated with a decreased risk of Salmonella infection in the farms (van der Wolf et al., Reference van der Wolf, Bongers, Elbers, Franssen, Hunneman, van Exsel and Tielen1999 and Reference van der Wolf, Wolbers, Elbers, van der Heijden, Koppen, Hunneman, van Schie and Tielen2001). A French prospective study of 105 farrow-to-finish farms showed that the risk of Salmonella shedding at the end of the fattening period was increased when dry feed (v. wet feed) was provided during the fattening period (Beloeil et al., Reference Beloeil, Fravalo, Fablet, Jolly, Eveno, Hascoet, Chauvin, Salvat and Madec2004). Factors associated with pig herds testing Salmonella sero-positive (using the Salmonella mix ELISA tests) were evaluated in a study conducted in 359 finishing-pig herds in Germany, Denmark, Greece, the Netherlands and Sweden between 1996 and 1998 (Lo Fo Wong et al., Reference Lo Fo Wong, Dahl, Stege, van der Wolf, Leontides, von Altrock and Thorberg2004). Pigs fed non-pelleted feed (dry or wet) had 2 and 2.5 times lower odds of being sero-positive, compared with pigs fed pelleted feed. The protective effect of non-pelleted feed over pelleted feed was attributed to the structure and composition. The study also indicated that pigs fed whey (to drink or as the liquid part of the diet) had 2.6 times lower odds of testing sero-positive than pigs not receiving whey. Similar findings were reported in an European Food Safety Authority study of breeding pigs carried out in 2008, where feed of commercial compound origin or pelleted feed were found to be risk factors for increased Salmonella positivity (EFSA, 2011). In contrast to the above-mentioned studies, a Canadian study comparing 20 swine farms using liquid feeding with 61 farms using dry feeding found higher sero-prevalence for Salmonella and more Salmonella in faecal samples in farms using liquid feeding systems (Farzan et al., Reference Farzan, Friendship, Dewey, Warriner, Poppe and Klotins2006). The same research team evaluated the risk factors for Salmonella in 80 representative swine farms and Salmonella was more likely to be found in farms where pigs were fed pelleted feed compared with mash or liquid feed (Farzan et al., Reference Farzan, Friendship, Dewey, Poppe and Funk2010). The decreased levels of Salmonella shedding in wet feeding farms included in these studies may be partly attributed to the acidic form of the feed.
In some countries in Europe, coarse-ground meal is added to the diet of swine in herds with a high rate of Salmonella contamination. The intended effect is to decrease a too rapid passage through the stomach in pelleted fed pigs to allow the gastric acidification time to act and decrease the level of orally ingested Salmonella, usually from faecal contamination from pen mates (EFSA, 2008). Coarsely ground meal feed to pigs is believed to alter the physicochemical and microbial properties of content in the stomach, which decreases the survival of Salmonella during passage through the stomach. Coarse-ground meal, fine-ground meal, fine-pelleted meal and coarse-pelleted meal were compared in a study (Mikkelsen et al., Reference Mikkelsen, Naughton, Hedemann and Jensen2004). Stomach contents from pigs fed the coarse-ground non-pelleted diet showed increased in vitro death rate of Salmonella Typhimurium DT12. Another study evaluated Salmonella attachments in the intestines of pigs fed different diet forms. Using a pig intestine organ culture model, Salmonella adhered 60% less (P < 0.05) to the ileal tissue of pigs fed the non-pelleted diets than to those fed pelleted diets (Hedemann et al., Reference Hedemann, Mikkelsen, Naughton and Jensen2005; Farzan et al., Reference Farzan, Friendship, Dewey, Warriner, Poppe and Klotins2006). However, the study confirmed findings from previous studies indicating that the feed conversion was more efficient in pigs fed the pelleted diets compared with non-pelleted diets. The role of the physical properties of pig feed is, however, subject to debate and a meta-analysis of 44 studies from 1950 to 2005 (O'Connor et al., Reference O'Connor, Denagamage, Sargeant, Rajic and McKean2008) concluded that ‘there should be a low level of comfort among qualified scientists that the claimed association between non-pelleted feed and reduced Salmonella prevalence is scientifically valid’.
Probiotics
Probiotics have been defined as ‘live-microorganisms which, when administered in adequate amounts, confer a health benefit on the host’ (FAO/WHO, 2001). A challenge with probiotic supplements is to verify the bacterial composition of the product and this presents challenges for market approval in the EU. The current probiotics in the EU are approved based on improved animal digestive health and performance. There is a long list of probiotic products licensed in the EU as ‘gut flora stabilizers’ for different animals and production categories (European Commission, 2011). Another challenge is to achieve probiotics that are not destroyed by pelleting, and are shelf-stable and cost-effective. A large variety of Bacillus spores have been investigated with regard to their stability and heat tolerance. Several commercial spore-forming Bacillus cultures have been shown to reduce food-borne pathogens and ameliorate intestinal health in various species. The challenge is, however, to find a cost-effective method to achieving sufficient concentrations of spores in the feed (Hong et al., Reference Hong, Duc Le and Cutting2005).
Poultry
Lactic acid bacteria cultures have been extensively researched for their ability to reduce Salmonella infection in poultry. They have been used commercially for Salmonella control in poultry and turkey production in many countries (Higgins et al., Reference Higgins, Erf, Higgins, Henderson, Wolfenden, Gaona-Ramirez and Hargis2007 and Reference Higgins, Higgins, Wolfenden, Henderson, Torres-Rodriguez, Vicente, Hargis and Tellez2010). The effect of the yeast, Saccharomyces boulardii, was evaluated experimentally in the 1990s. Broilers were gavaged with Salmonella Typhimurium and Campylobacter jejuni and the frequency of Salmonella caecal colonization was significantly reduced from 70% in non-supplemented control birds to 20% and 5% in birds fed a diet containing 1 g or 100 g dried S. boulardii/kg feed, respectively (Line et al., Reference Line, Bailey, Cox, Stern and Tompkins1998). In a further experiment evaluating S. boulardii's ability to reduce populations of Salmonella and Campylobacter in broiler chickens subjected to transport stress, it was similarly found that yeast treatment significantly reduced the frequency of Salmonella colonization to lower than the pre-stress (before transport) levels, whereas non-supplemented birds had higher levels of Salmonella colonization (Line et al., Reference Line, Bailey, Cox and Stern1997).
Pigs
Probiotics approved for pigs include Bacillus sp., Lactobacillus sp., Lactococcus sp., Bifidobacteria sp., Pediococcus sp., Enterococcus sp. and Saccharomyces sp. (European Commission, 2011). Common products in pig feed are Bacillus spore probiotics that have good heat-stability, preserving their efficacy during feed processing. Other common probiotic species are usually included at higher rates in the pre-processed feed to take into account their lower heat tolerance. Isolation and characterization of anti-Salmonella lactic acid bacteria from the porcine gastro-intestinal tract has been carried out to find probiotics that survive in gastro-intestinal passage (Casey et al., Reference Casey, Casey, Gardiner, Tangney, Stanton, Ross, Hill and Fitzgerald2004). Lactic acid-producing probiotics have been shown to lead to an amelioration of diarrhoea in Salmonella Typhimurium-infected pigs early in the course of infection and reduced Salmonella counts over a longer time frame (Casey et al., Reference Casey, Gardiner, Casey, Bradshaw, Lawlor, Lynch, Leonard, Stanton, Ross, Fitzgerald and Hill2007). A Salmonella infection trial in pigs evaluated the addition of anaerobically fermented yeast products (Saccharomyces cerevisiae) to the starter diet in weaned pigs following a challenge with 109 cfu of Salmonella Typhimurium DT104. The pigs receiving the yeast supplement showed slightly better BW gains post-infection than non-supplemented controls but the supplemented group had a tendency towards increased Salmonella shedding (Price et al., Reference Price, Totty, Lee, Utt, Fitzner, Yoon, Ponder and Escobar2010).
Competitive exclusion (CE)
CE cultures are a form of probiotic culture that is only administered as a single dose. The CE culture is usually administered to the neonatal animal, such as the day-old chick or a newborn piglet, and it can also be used to restore the digestive tract flora after antimicrobial treatment. It is usually composed of a mixture of non-pathogenic bacteria typically found in the gastro-intestinal tract of the animal.
Poultry
CE was initially developed and used in poultry production, where newly hatched chicks can be protected from subsequent Salmonella infections by accelerating the establishment of a complex, protective microflora (Nurmi et al., Reference Nurmi, Nuotio and Schneitz1992; Schneitz et al., Reference Schneitz, Nuotio, Mead and Nurmi1992). Chicks hatched in sterile incubators are not normally colonized by intestinal flora compared with chicks hatched naturally under the hen in a nest containing faecal microbes. It is essential that the CE be administered before exposure to Salmonella. The Salmonella-preventing effect is also shown in field situations (Wierup et al., Reference Wierup, Wahlström and Engström1992), and the concept is now applied with a demonstrated effect also on other intestinal disorders (Schneitz et al., Reference Schneitz, Nuotio, Mead and Nurmi1992) and intestinal pathogens. There are several commercial CE cultures on the market also with efficacy against Campylobacter (Stern et al., Reference Stern, Cox, Bailey, Berrang and Musgrove2001) and Clostridium perfringens (Kaldhusdal et al., Reference Kaldhusdal, Schneitz, Hofshagen and Skjerve2001). The search for improved CE cultures with efficacy to both Salmonella and Campylobacter is on-going and a relatively recent study indicated that cultures from free-range chickens on family farms provided better CE cultures than commercial farm chickens (Zhang et al., Reference Zhang, Ma and Doyle2007). Furthermore, in the study by Santos et al. (Reference Santos, Sheldon, Santos and Ferket2008), broilers housed in cages were compared with those housed on litter. Broilers raised on litter had lower caecal Salmonella populations than the caged birds and it is speculated that this could have been due to the fact that litter intake may have modulated the intestinal microflora by increasing competitive exclusion microorganisms, which discouraged Salmonella colonization. A European multi-national study also indicated lower Salmonella levels in floor-raised layers compared with caged layers (Van Hoorebeke et al., Reference Van Hoorebeke, Van Immerseel, Schulz, Hartung, Harisberger, Barco, Ricci, Theodoropoulos, Xylouri, De Vylder, Ducatelle, Haesebrouck, Pasmans, de Kruif and Dewulf2010). These findings have been used as an excuse for not removing manure or cleaning and disinfecting between batches of broilers. Instead, the manure is removed only once a year, when it is also sometimes recycled. In addition, bedding is often home to Salmonella-contaminated rodents (Henzler and Opitz, Reference Henzler and Opitz1992). Using this production method, it is practically impossible to reach European Salmonella targets for reduction (Mead et al., Reference Mead, Lammerding, Cox, Doyle, Humbert, Kulikovskiy, Panin, do Nascimento and Wierup2010).
Pigs
A mucosal CE culture from swine (MCES) was produced from the caecum of a 6-week-old pig (Fedorka-Cray et al., Reference Fedorka-Cray, Bailey, Stern, Cox, Ladely and Musgrove1999) and administered to piglets within 6 h post-farrowing while a second group of piglets remained unsupplemented. The two groups were challenged with Salmonella cholerasuis 24 h post-farrowing. Seven days later, the pigs that received the MCES showed a 2- to 5-log10 reduction in Salmonella in the caecal contents or ileocaecal junction digesta compared with the controls. Administration of CE cultures to neonatal piglets has further been shown to reduce S. choleraesuis faecal shedding in pigs and pigs in contact with those that received the CE culture during the pre-weaning and the weaning period (Genovese et al., Reference Genovese, Anderson, Harvey, Callaway, Poole, Edrington, Fedorka-Cray and Nisbet2003).
Glycans
Carbohydrates (glycans) have long been known to be an important dietary component, seen predominantly as energy-yielding molecules and structural components of plant materials. A number of carbohydrates (based on glucose, mannose, galactose and fructose) have been shown to have anti-infective properties. Mannose and its polymers are the most commonly used products as feed additives and have been shown to reduce Salmonella colonization in chickens (Oyofo et al., Reference Oyofo, DeLoach, Corrier, Norman, Ziprin and Mollenhauer1989). The large majority of Salmonella contain mannose-specific lectins (Type 1 fimbriae) on the bacterial surface that bind to glycoproteins (rich in mannose) on the intestinal surface. Mannose sugars can thus compete with the intestinal glycoproteins for attachment sites and prevent colonization. Similar findings have been demonstrated with mannan oligosaccharide (MOS; Bio-Mos, Alltech Inc., Nicholasville, Kentucky, USA) at significantly lower concentrations than that required for purified mannose (Spring et al., Reference Spring, Wenk, Dawson and Newman2000). In a series of three trials in which 3-day-old chicks were orally challenged with 104 cfu S. Typhimurium, birds receiving 4000 ppm of dietary MOS showed a 1.4 log (more than a 10-fold) reduction in caecal Salmonella concentrations 1 week later. In another series of three trials with Salmonella Dublin as challenge bacteria, the number of birds that tested Salmonella positive 1 week later was significantly reduced in birds fed MOS (90% v. 56%, respectively) (Spring et al., Reference Spring, Wenk, Dawson and Newman2000).
Prebiotics
These are non-digestible food or feed ingredients that beneficially affect the host by selectively stimulating the growth and/or the activity of one or a limited number of bacteria in the colon, thus improving host health (Gibson et al., Reference Gibson, McCartney and Rastall2005). The prebiotic effect has been shown to not only influence the microbial composition of the gut but also to influence the immune system (Roberfroid et al., Reference Roberfroid, Gibson, Hoyles, McCartney, Rastall, Rowland, Wolvers, Watzl, Szajewska, Stahl, Guarner, Respondek, Whelan, Coxam, Davicco, Leotoing, Wittrant, Delzenne, Cani, Neyrinck and Meheust2010). Prebiotics are mainly medium- to long-chain carbohydrates called oligosaccharides (also known as soluble fibre) but can also be proteins, peptides and some types of lipids. These prebiotics feed probiotics or commensal enteric bacteria, offering them a competitive advantage over potential pathogens, such as Salmonella. However, some studies with fructo-oligosaccharides and inulin indicate that there may be increased colonization with Salmonella using these products (Ten Bruggencate et al., Reference Ten Bruggencate, Bovee-Oudenhoven, Lettink-Wissink, Katan and van der Meer2004).
Egg proteins
Experiments have indicated that egg components included in feed to layers reduced Salmonella colonization in the birds. Feed containing 5.0% (wt/wt) of non-immunized egg yolk powder was shown to eliminate an experimental challenge infection with S. Enteritidis and also prevent S. Enteritidis colonization in laying hens, with no adverse effects (Kassaify and Mine, Reference Kassaify and Mine2004a). Another experiment using experimental infection with S. Typhimurium indicated that a 10% egg yolk inclusion in the feed eliminated the infection and lower doses decreased infection (Kassaify and Mine, Reference Kassaify and Mine2004b). The Salmonella reduction properties of the egg yolk were investigated and attributed to the anti-adhesive properties of the egg yolk granule component, high-density lipoproteins (Kassaify et al., Reference Kassaify, Li and Mine2005). Egg yolks from hens hyperimmunized against Salmonella have also been shown to decrease Salmonella shedding in chicks (Rahimi et al., Reference Rahimi, Shiraz, Salehi, Torshizi and Grimes2007).
Essential oils
A range of essential oils have been shown to have bacteriostatic or bacteriocidal properties against Salmonella in vitro (Burt, Reference Burt2004). Citrus essential oils have been screened by a disc diffusion assay for their antibacterial action against 11 serovars of Salmonella and it was concluded that these oils have the potential to be used in organic and natural foods (O'Bryan et al., Reference O'Bryan, Crandall, Chalova and Ricke2008). Another study indicated that basil oil has the potential to reduce the growth of Salmonella in food (Rattanachaikunsopon and Phumkhachorn, Reference Rattanachaikunsopon and Phumkhachorn2010). Studies are currently lacking regarding the applicability as a Salmonella intervention in feed.
Bacteriophages
Bacteriophages are viruses that can infect bacteria and these bacteriophages can be found in the gut of food animals. These are currently being investigated as a potential intervention strategy to reduce Salmonella levels in the live animal. Clinical studies have indicated that anti-Salmonella phages isolated from faeces from commercial swine have the ability to reduce caecal populations and faecal shedding in weaned pigs (Callaway et al., Reference Callaway, Edrington, Brabban, Kutter, Karriker, Stahl, Wagstrom, Anderson, Poole, Genovese, Krueger, Harvey and Nisbet2011).
Conclusion
There are numerous feed additives with the potential to control Salmonella in the pre-harvest phase of pork and poultry production. The challenge with nutritional interventions for Salmonella control is that the results are highly variable and dependent on the management, nutrition and Salmonella status of the farm. The numerous scenarios for Salmonella contamination of poultry and pig production species make generalizations difficult. Producers need to assess the tools available and evaluate them in their own situation. It is important to thoroughly investigate claims for Salmonella reduction and specifically note in vitro, in vivo and field trials. The current situation indicates that nutritional interventions should be seen as an additional tool in a systems-based approach to decrease Salmonella prevalence in all components of the farm system.
Acknowledgements
This review is based on an invited presentation at the 61st Annual Meeting of the European Association for Animal Production held in Hereaklion, Greece, August 2010. It has been funded by Berge Veterinary Consulting, Vollezele, Belgium, and Alltech Inc., Lexington, Kentucky, USA. The authors are grateful to Helen Warren for reviewing the language.
