J. Verbr. Lebensm. 1 (2006): 197209 1661-5751/06/030197-13 DOI 10.

1007/s00003-006-0036-z Birkhuser Verlag, Basel, 2006

Journal fr Verbraucherschutz und Lebensmittelsicherheit Journal of Consumer Protection and Food Safety

Animal Feed Production and Contamination by Foodborne Salmonella

K.G. Maciorowski1,2, P. Herrera1, M.M. Kundinger1,3, and S.C. Ricke1
2

Poultry Science Dept. Texas A&M University, College Station, TX 77843 Current address: Agriculture & Natural Resources Dept., Delaware State University, Dover, DE 19901 3 Current address: University of Wisconsin, 2000 W. 5th Street, Marsheld WI 54449

Correspondence to: Dr. S. C. Ricke, Dept. of Food Science, 2659 N. Young Avenue, University of Arkansas, Fayetteville, AR 72704, USA, Tel.: 479-575-4678, Fax: 479-575-6836, E-mail: sricke@uark.edu Received: September 16, 2005; Accepted: March 3, 2006

Key words: Salmonella, animal feeds, poultry feeds, contamination, foodborne disease Abstract: Animal feeds can potentially become contaminated with foodborne Salmonella either during harvesting, processing at the feed mill or during storage. Any environment that comes in contact with feed during these stages that also harbors Salmonella can theoretically contaminate the feed. This also holds true for ingredients that are combined with feeds as they are being mixed at the feed mill. Animal feeds are also potential reservoirs for cross contamination from Salmonella containing vectors and environmental sources while being fed to animals. Although several factors may determine the extent of contamination, the potential for infection in animals these have not been well characterized. In addition, certain animal management and feeding programs can lead to animals becoming more susceptible to Salmonella colonization and invasion. Control measures to limit Salmonella contamination of feed include agents that directly reduce or destroy the organism in feed. Antimicrobial compounds and management strategies have also been developed for preventing colonization and eliminating Salmonella colonized in the gastrointestinal tract. The future prospects for minimizing Salmonella contaminated feed will probably involve combining more efcient monitoring and sampling approaches with more rapid and sensitive detection technologies. Zusammenfassung (Redaktion): Futtermittel knnen schon bei der Ernte der Futterpanzen sowie whrend der Futter-Herstellung oder -Lagerung von Salmonellen kontaminiert werden; grundstzlich kann dies berall dort passieren, wo Futtermittel mit der Auenwelt (mit Salmonellen) in Kontakt kommen. Dies gilt ebenso fr Zusatzstoffe, die den Futtermitteln in Futtermhlen beigemengt werden. Futtermittel sind auch potenzielle Reservoire fr die Kontamination mit Salmonellen whrend des Ftterns von Tieren. Obwohl das Ausma einer solchen Kontamination mit Salmonellen von etlichen Faktoren bestimmt wird, sind die Umstnde, die zur Infektion der Tiere fhren kn-

nen, noch nicht ausreichend charakterisiert worden. Auerdem knnen bestimmte Tierhaltungs- und Ftterungsverfahren eine Infektion von Tieren durch Salmonella sogar begnstigen. Um dieses zu verhindern, knnen Wirkstoffe eingesetzt werden, welche die Salmonella-Populationen im Futter reduzieren oder zerstren. Es wurden ebenso Verfahren mit antimikrobiell wirksamen Stoffen entwickelt, um eine Besiedlung des Gastrointestinaltraktes durch Salmonella zu verhindern bzw. dort bereits vorhandene Samonellen abzutten. Zuknftig mu ein effektiveres Monitoring- und Probenahme-Verfahren mit schnelleren und empndlicheren Nachweisverfahren kombiniert werden, um eine eventuelle Kontamination von Futtermitteln durch Salmonella zu minimieren.

1. Introduction Foodborne Salmonella spp. are gram-negative rod shaped foodborne pathogens that can originate from a variety of sources and are responsible for causing localized gastroenteritis in humans (Lax et al., 1995). Salmonella is believed to be the source of between 800, 000 and 4 million cases of foodborne illness each year in the United States (Angulo and Swerdlow, 1998). Symptoms of Salmonella include diarrhea, fever, nausea, vomiting, headache, and abdominal pain (DAoust, 1991). The onset of these symptoms is usually between eight to seventy-two hours and is generally limited to a period of within ve days (DAoust, 1991). The more severe systemic versions occur in susceptible humans such as immunosuppressed individuals that have less ability to initiate resistance to infection (Lax et al., 1995). Over 2000 different serotypes of Salmonella have been identied (Lax et al., 1995). Although many of these serotypes are capable of initiating localized gastroenteritis in humans, Salmonella enterica serovar Enteritidis (S. Enteritidis) and Salmonella enterica serovar Typhimurium (S. Typhimurium) represent the most signicant foodborne pathogen serotypes (Lax et al., 1995). Since 1970, the disease has occurred primarily as large outbreaks

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of nontyphoid human salmonellosis traced to contaminated foods originating from animals (Tauxe, 1991). As livestock operations become larger and post harvest processing capacity is increased, the characteristic epidemiology of foodborne pathogens has become sustained on a more international level (Morales, 1996). Given the persistence of foodborne Salmonella, understanding the routes of tr ansmission in food animals continues to be a major concern. In conned animal operations, enclosed facilities such as poultry and swine housing are more controlled environments, but the exposure level can be amplied due to the proximity of higher numbers of animals. This also holds true for exposure to outside sources of pathogens such as air ventilation, fans, and incoming feed. Animal feed represents an additional concern due to the multitude of potential contamination sources for the individual feed components and primary ingredients. Feed mixing and ingredient sources have become more uniform, but the mass production nature of feed manufacture can increase the opportunity for more animals to become exposed to contaminated feed. Combining larger animal units of operation with bulk feed processing provides additional opportunities for widespread infestation. There is also more potential for contaminated animal feed or animal feed ingredients to be transported nationally as well as internationally (Crump et al., 2002). In this review the role of feed management practices, foodborne Salmonella spp. contamination of animal feeds and feed ingredients and control measures will be discussed.

deprivation can lead to increased susceptibility of animals to Salmonella infection (Lax et al., 1995). This has been demonstrated in several animal species. Removing feed has been shown to increase levels of Salmonella in the gastrointestinal tracts of mice, chickens, and ruminants (Miller and Bohnhoff, 1962; Brownlie and Grau, 1967; Grau et al., 1968; Tannock and Smith, 1972; Tannock and Savage, 1974; Humphrey et al., 1993; Holt et al., 1994; Durant et al., 1999). Of the feed withdrawal animal models examined, poultry are probably the most extensively studied and best understood (Ricke, 2003a). The following sections describe specic feed management practices in poultry production which have been associated with feed withdrawal and increased Salmonella infection levels. 2.2 Feed withdrawal in preslaughter broiler production Market age broilers prior to preslaughter undergo a feed withdrawal just before being transported to the slaughter plant. In the United States the goal is to sufciently empty the gastrointestinal tract of broilers prior to slaughter to reduce the potential for feed and fecal contamination of poultry carcasses (Rasekh et al., 2005). From a managerial perspective the goal is to simultaneously evacuate the gastrointestinal contents and fecal material while avoiding substantial decreases in the nal eviscerated carcass weight (Wabek, 1972; Veerkamp, 1986; Lyon et al., 1991). Withdrawing feed within a particular time frame (8 to 12 hours) prior to shipping is believed to be optimal for minimizing fecal contamination and retaining maximal eviscerated yields (Wabeck, 1972; Veerkamp, 1986; Taylor et al., 2002). However, feed withdrawal time periods, particularly if they occur for an extended period of time, may increase the risk for intestinal infection by Salmonella spp. This has been demonstrated primarily in the crop where Salmonella populations have increased as much as seven-fold in some studies during preslaughter withdrawal and Campylobacter increased as well (Ramirez et al., 1997; Byrd et al., 1998; Corrier et. al., 1999). Salmonella cecal infection rates are less conclusive as both increases and minimal changes have been reported (Rigby and Pettit, 1980; Moran and Bilgili, 1990; Ramirez et al., 1997; Corrier et al., 1999; Hinton et al., 2000a). The increase in crop infection is believed to be caused by a decrease in crop lactic acid bacteria and the diminished ability of the resulting crop microenvironment (less acidic) to prevent pathogen establishment (Hinton et al., 2000b). Prevention strategies have centered around approaches that either provide nutrients to sustain the crop lactic acid bacteria or supplement with external antimicrobial compounds that simulate the preventative nature of the crop (Barnhart et al., 1999; Hinton et al., 2000c; Byrd et al., 2001; Hinton et al., 2002; Byrd et al., 2003). During feed withdrawal these compounds or nutrients are generally administered via the drinking water to retain the effect of feed withdrawal for minimizing fecal contamination. Farhat et al. (2002) demonstrated that low nutritive residue diets could serve as a solid phase supplement as a highly digestible feed during feed withdrawal without preventing gastrointestinal emptying or live weight loss. It is conceivable that some of the compounds currently proposed as being added in the drinking water could be administered as amendments to these highly digestible solid phase diets.

2. Foodborne Salmonella in feed management 2.1 Incidence in food animal production Foodborne salmonellosis outbreaks have been associated with foods such as pork, beef, seafood, poultry, eggs, and dairy products (Tauxe, 1991). Salmonella spp. is commonly found in the gastrointestinal tracts of animals and is widely disseminated in the environment (Murray, 1991). These reservoirs can serve as points of origins for widespread infestations in conned food animal operations. Foodborne Salmonella has been isolated in swine herds and liquid and solid excreta (Letellier et al., 1999; Ramrez et al., 2005). With cattle both the age of the animal and the type of management can be important with young animals and animals in intensive breeding facilities being at greater risk than adults and range bred cattle, respectively (Murray, 1991). In poultry Salmonella can be isolated from the feed, litter, and feces of birds (Jones et al., 1991). These organisms could conceivably be spread to other animals either on the same poultry farm or at the slaughter facility (Heyndrickx et al., 2002). When foodborne Salmonella infection occurs in animals it can result in localized gastroenteritis but generally is transient with minimal impact (Lax et al., 1995). However, animals that are asymptomatic can continue to contaminate the food supply because they harbor the foodborne disease organisms yet they exhibit no apparent clinical signs of illness (Morales, 1998). Salmonella infestation in ocks and herds can occur under a variety of circumstances but particular feed management practices can amplify infection in susceptible animals. Feed

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2.3 Feed withdrawal in layer hen egg production Egg producers articially induce laying hens to undergo molt to arrest reproductive activity and after a period of non-egg laying return the birds to a second egg laying cycle (North and Bell, 1990). Induced molting is considered economically benecial compared to non-molting management alternatives (Lee, 1982; Webster et al., 1998; Alodan and Mashaly, 1999). Historically, the practice of feed withdrawal has been viewed as an efcient method to induce a molt because it is easy, economically advantageous and results in satisfactory postmolt performance for the commercial layer industry (Brake, 1993). However, a long period of feed withdrawal is more controversial. Birds molted by feed withdrawal may be more susceptible to S. Enteritidis infection because induced molting by feed withdrawal depresses the cellular immune response (Holt, 1999). During the molting periods, S. Enteritidis is readily transmitted to uninfected birds from infected birds (Holt, 1995; Holt et al., 1998). The increased susceptibility of molted hens to S. Enteritidis colonization may be related to decreased fermentation and production of volatile fatty acid (VFA)-producing bacteria present in the ceca and crop (Corrier et al., 1997; Durant et al., 1999). Durant et al. (1999) observed that induced molting increased crop pH, and decreased the Lactobacilli populations and the concentrations of lactic, acetic, propionic, butyric, and VFA of the crop. They also reported that increased S. Enteritidis colonization in the crop was due to the high pH and lowered concentrations of lactate and total VFA. Given the susceptibility of laying hens to S. Enteritidis colonization during feed withdrawal induced molt it has become a research focus to devise alternative molt procedures that avoid feed removal and reduction of microbial fermentation but retain the economic benets of induced molt. Alternative approaches have usually involved the feeding of diets that nutritionally restrict the laying hen either by reducing intake via supplementation of minerals such as zinc or feeding high ber / low energy diets such as wheat middlings or alfalfa (Holt, 2003; Ricke, 2003a; Park et al., 2004). Several of these alternative diets have been shown to limit S. Enteritidis and induce molt when consumed by hens during infection studies (Seo et al., 2001; Moore et al., 2004; Ricke et al., 2004b; McReynolds et al., 2005; Woodward et al., 2005). In addition optimal microbial fermentation and resident microbial populations in the crop and ceca are generally retained in many of these alternative molting diets (Hume et al., 2003; Moore et al., 2004; Ricke et al., 2004a and b; McReynolds et al., 2005; Woodward et al., 2005). When these alternative molting diets were compared with laying hens that have undergone feed withdrawal, similar egg production responses were observed (Biggs et al., 2003 and 2004; Donalson et al., 2005; Landers et al., 2005a and b).

can become infected by horizontal transmission from a variety of environmental sources including airborne routes (Holt, 1995 and 2003; Holt et al., 1998). These represent specic management circumstances that generate susceptible animals. Animals can also be at risk from the consumption of Salmonella spp. contaminated feed at any time during the production cycle. Animal feeds may become contaminated with foodborne Salmonella either during harvesting, processing at the feed mill or during storage. Any environment that comes in contact with feed during these stages that also harbors Salmonella can subsequently contaminate the feed. This also holds true for ingredients that are combined with feeds as they are being mixed at the feed mill. Animal feeds are also potential reservoirs for cross contamination from Salmonella containing vectors and environmental sources while being fed to animals. Although several factors may determine the extent of contamination and the potential for infection in animals, these have not been well characterized. In the following sections feed sources and processes are described and the occurrence of Salmonella contamination in these sources and stages of feed processing. 3.2 Complete diets and Salmonella spp. contamination Complete diets consisting primarily of cereal grains are economically attractive for both the optimal growth of livestock and the production of agricultural products. In the United States, depending on current market prices, beef cattle can be fed a variety of grains including corn, oilseed meals, sorghum, wheat, and rye (Cheeke, 1991; Cecava, 1995). Pigs and chickens are commonly fed cereal grain-based rations (Cheeke, 1991; Jurgens, 1993). Even sheep, which are primarily considered as foraging animals, are routinely offered supplement block. Supplements may include molasses, oats or barley, although an animals supplement consumption may vary depending upon supplement formulation, previous exposure to feed type, social interactions during feeding, and whether animals are fed individually or in a group (Bowman and Sowell, 1997). In dairy operations, feed costs usually comprise a substantial proportion of the total cost for milk production (Bath, 1985). Poultry also are major consumers of grain-based complete diets. Feed intakes of laying hens can vary, depending on metabolizable energy intakes and environmental temperature (North, 1978; Jurgens, 1993). Ad libitum broiler intake varies depending on numerous factors, such as growth rate, diet composition, ambient temperature and corticosterone concentration (Dale and Fuller, 1980; Gous, 1998; Koh and Macleod, 1999; Nasir et al 1999). Dale and Fuller (1980) reported that feed to gain ratios for poultry may also depend upon species, as exotic species such as ostriches and cockerels have been shown to metabolize energy more efciently than poultry (Cilliers et al., 1999). Given the scope of livestock production in the United States, an organized, commercial animal feed network has evolved to maximize nutrient intake and minimize food costs for producers and consumers. Complete diets have been examined as a contributor to the transmission of Salmonella to food animals (Williams, 1981a; Crump et al., 2002; Maciorowski et al., 2004). S. Montevideo was a consistent serotype isolated from poultry, cattle and swine feeds in early studies (Smyser et al., 1966; Allred

3. Salmonella contamination of animal feeds and ingredients 3.1 Introduction As discussed in the previous sections removal of feed can lead to gastrointestinal conditions favourable for foodborne Salmonella spp. colonization in animals. Under these conditions animals

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et al., 1967). Over a quarter of a century later Veldman et al. (1995) screened Dutch poultry feed samples and identied 20 distinguishable serotypes with S. Agona, S. Livingstone and S. Mbandaka being the most frequent isolates. Despite the occurrence of an epidemic of S. Enteritidis in poultry during the same time frame this serotype was not isolated in any of the feeds examined (Veldman et al., 1995). However, Davies and Wray (1996) did isolate S. Enteritidis and S. Typhimurium from spillage and dust samples and Shirota et al., (2000) isolated 20 strains of S. Enteritidis from eastern Japanese commercial layer rations. Further work by these authors using pulsed-gel electrophoresis patterns demonstrated a linkage between the feed contaminant S. Enteritidis serovar and the S. Enteritidis isolated from egg contents (Shirota et al., 2001). S. Typhimurium has also been isolated from poultry broiler and breeder diets (MacKenzie and Bains, 1976; Jones et al., 1991). S. Worthington was the most frequently isolated serotype in feeds sampled from multiple swine farms across several states in the United States (Harris et al., 1997). 3.3 Salmonella in specic protein supplements Cereal grains Soybean meal (SBM) is the most common choice for protein supplementation in the United States (Cullison and Lowrey, 1987; Jurgens, 1993). Whole, raw soybeans are usually not fed to monogastric animals due to a trypsin inhibitor which decreases digestibility and gain in poultry and swine (Jurgens, 1993). Raw soybeans also contain urease which may degrade urea in ruminant diets, and are usually processed to extract economically valuable soybean oil before feeding to cattle (Cecava, 1995). Typical diets fed to monogastric animals, may include corn as an energy source, SBM as a protein source, and premixes to supplement vitamins and minerals. Other alternative sources of protein, such as cottonseed meal, may be substituted, though gossypol toxicity (in the case of cottonseed meal) and regional availability limit their use (Cullison and Lowrey, 1987). Salmonella incidence from feed ingredients of plant origins including the major cereal grains used in feed production have become recognized as sources of Salmonella spp. contamination (Crump et al., 2002; Jones and Richardson, 2004; Davies et al., 2004). Hacking et al. (1978) failed to isolate Salmonella from either ground corn, barley or soybean meal in an Ontario feed mill. However, MacKenzie and Bains (1976) were able to isolate a wide variety of serotypes from several seeds and cereal grains including peanut meal, sunower meal, bran meal, barley, corn sorghum, SBM, and wheat. Sunower yielded the highest number of positive samples with S. Birnum being the most common while S. Singapore was isolated at the highest frequency in SBM (MacKenzie and Bains, 1976). S. California was the predominant serotype in plant-based feed from Spanish feed mills (Alvarez et al., 2003). Salmonella contaminated cereal and plant ingredients have also been linked directly with animal Salmonella infection. Jones et al. (1982) was able to demonstrate the transmission of S. Mbandaka to cattle after consumption of a vegetable fat containing palm oil, with palm kernel and ground straw as the carrier base. S. Typhimurium originating from wheat was demonstrated to be associated with clinical outbreaks in young broiler ocks (Bains and MacKenzie, 1974)

3.4 Salmonella in specic protein sources Animal byproducts In addition to grain-based protein sources, animal tissue left over from processing is typically rendered for creation of protein meals. Inedible animal byproducts produced annually in the United States are recycled by rendering (Ockerman and Hansen, 1988). Protein meals can be classied depending upon composition but the nutritional quality is variable (Cheeke, 1991; Jurgens, 1993). Some meals are classied by species origin: for example, poultry by-product meal contains tissue left over from poultry processing and unfavorable poultry carcasses (Cullison and Lowrey, 1987). Animal protein and byproduct ingredients originating from animals have always been considered a major source of Salmonella spp. in feeds (Williams, 1981a; Davies et al., 2004). Levels of contamination in sh meal and animal byproducts have been estimated from nearly ve to thirty-one percent respectively (Allred et al., 1967). Hacking et al., (1978) identied Salmonella isolates from Ontario feed mills, and meat meal yielded predominantly S. Montevideo isolates while the majority of the isolates from feather meal were S. Agona and S. Schwarzengrund. Although Mackenzie and Bains (1976) isolated S. Montevideo from meat meals, the primary isolates were S. Havana, S. Lille, and S. Eimsbuettel. When MacKenzie and Bains (1976) examined feather meal they recovered higher frequencies of S. Tennessee and S. Anatum than S. Agona. Nabbut (1978) isolated a high frequency of S. Meleagridis from bone meal samples and S. Montevideo and S. Newport from sh meal samples collected from feed additives imported into Lebanon and from Lebanese animal feed plants. Fish meal appears to be particularly problematic. Veldman et al. (1995) found that 31 % of the sh meal samples they examined from Dutch feeds were positive for Salmonella compared to only 4% of the remaining animal-based ingredients. The rise in S. Agona isolations from human cases in the United States in the 1970s was attributable to poultry fed Peruvian sh meal contaminated with this serotype (Clark et al., 1973; Crump et al., 2002).

4. Salmonella contamination during feed processing 4.1 Introduction After the raw feed ingredients are harvested and stored, feed may be physically and chemically processed to increase its feed value, digestibility, palatability, and ease of handling by automated equipment. The application of physical treatment on feed has always been done to either improve feed efciency (feed / grain ratio) or rate of gain. Particle reduction is perhaps the least expensive feed treatment, and a necessary precursor to pelleting or chemical addition. Grinding or rolling fragments the outer cuticle layer of grains and seeds and exposes the starchy interior to eventual degradation by animal enzymes. After grinding, feed may be heated to destroy toxic factors to animals such as trypsin inhibitors or gossypol (Cullison and Lowrey, 1987; Jurgens, 1993). Feeds may be cooked in a jacketed chamber (dry rendered), roasted, popped by raising the temperature, or exposed to steam (Cullison and Lowrey, 1986; Jurgens, 1993).

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Extruded and pelleted diets increase feed density and reduce storage costs. Pellet hardness depends partially upon the pressure of the stream that is used to heat the feed (Thomas et al., 1999), while pellet size varies with demand. Cows feeding on low quality pasture may require larger cubes, while poultry require bite size pellets which depend upon the size of the bird and thus the size of the bite (North, 1978; Jurgens, 1993). Chemicals such as bentonites (montmorillonite or hydrated aluminum silicate), hemicellulose or lignin sulfonate may be added to reduce pellet crumbling and decrease wastage in automatic feeding systems (Cheeke, 1991). Concern has always existed that pelleting may gelatinize starch (Thomas et al., 1999) or alter the availability of proteins and amino acids (Evans and Butts, 1949; Boctor and Harper, 1968; Bjarnason and Carpenter, 1970; Anderson-Hafermann et al., 1993; Johnson et al., 1998). However, the bioavailability of lysine, phosphorus, and tryptophan in swine diets or the feed conversion ratios of rabbits is either not affected or increased by pelleting (Yen et al., 1971; King, 1974; Mavromichalis and Baker, 2000). In fact, van der Peol et al. (1998) suggested that feed intake is positively related to diet hardness and durability. 4.2 Salmonella incidence and feed processing During the various stages of feed grinding, mixing, and further processing such as heat application in the form of pelleting, there are many opportunities for initial foodborne Salmonella spp. contamination as well as recontamination after the feed has been processed. Steaming during pelleting has been shown to eliminate most contaminating bacteria (Stott et al., 1975; Furuta et al., 1980a and b). Conventional steam pelleting is also considered effective for specically reducing Salmonella feed contamination (Israelsen et al., 1997). After surveying Dutch poultry feeds Veldman et al. (1995) reported that layer-breeder mash feeds were much more heavily contaminated (21%) than pelleted feeds (1.4%). However, pelleting does not completely eliminate Salmonella contamination in feeds. Hacking et al. (1978) found 4.3% Salmonella in 93 nished pelleted broiler feeds from an Ontario feed mill. Jones et al. (1991) reported an 82% reduction of Salmonella spp. in contaminated feeds after they had undergone pelleting. It has been suggested that animal feeds be heated to 80 to 85 C to eliminate Salmonella (Veldman et al., 1995; Davies et al., 2004; Jones and Richardson, 2004). Caution must be exercised when using laboratory-based data to determine optimal temperature ranges for effective reduction of Salmonella spp. contamination in feed. For example, early research indicated that the relative effectiveness of heat application could vary depending on the type of protein meal and whether the protein source was naturally contaminated or inoculated as part of the experiment (Rasmussen et al., 1964). Davies et al. (2004) concluded that several factors including moisture, variation in Salmonella serovar thermal resistance and detection / monitoring difculties must be considered before making absolute recommendations. Part of the concern with pelleting and other thermal treatments of animal feeds is the potential for cross contamination and recontamination after the process. Whyte et al. (2003) found that 11.8% of feed ingredients and 33.3% of dust samples taken from preheat areas of the feed mills were found to be

positive for Salmonella. In addition, Salmonella was recovered from preheat and postheat areas in the feed mill with positive samples recovered at 18.8 and 22.6% for these two areas respectively (Whyte et al., 2003). Feed delivery vehicles were also found to have a high rate of contamination with 57.1% of them testing positive for Salmonella (Whyte et al., 2003). Since the level of feed contamination has become a problem, how this transfers to the actual poultry facility becomes a concern. Jones and Ricke (1994) recommended that pelleting mills maintain high standards of hygiene to prevent cross-contamination and pellet recontamination, including inspection and cleaning of stream traps, transition guards, and the proper disposal of oor sweepings (instead of mixing them back with the nal product). Although this would appear to be a somewhat daunting task, there are certain areas such as the pellet cooler which have been identied as a major site of recontamination that could be a site for better control measures (Israelsen et al., 1997). A systematic identication of high risk sites in animal feed production and implementation of a Hazard Analysis of Critical Control Points (HACCP) for feed mills has been suggested (Jones and Ricke, 1994; Ricke, 2005). Developing effective HACCP plans focused on Salmonella spp. feed contamination will require an accurate assessment of Salmonella spp. contamination levels at potential sites (Maciorowski et al., 2004; Ricke, 2005).

5. Detection of Salmonella spp. in feeds As discussed in the previous sections Salmonella spp. have been isolated, enumerated and in some cases the serovar identied from feed and / or feed ingredients in a number of studies (Cox et al., 1983; Jones et al., 1982 and 1991; Veldman et al., 1995; Whyte et al., 2003). However, assessing high risk sites will require sampling approaches that are appropriate and detection methodologies that are accurate (Maciorowski et al., 2004). A variety of Salmonella detection methods that have been applied to feeds have been extensively reviewed (Williams, 1981b; Ricke et al., 1998; Maciorowski et al., 2006). Cultural growthbased methods combined with selective media are the traditional approach for the isolation and enumeration of Salmonella in feeds (Williams, 1981b; Ricke et al., 1998; Maciorowski et al., 2006). Several attempts have been made to improve the efciency of cultural approaches for assessing bacterial contamination of feeds including development of selective media to eliminate fungal overgrowth on plates (Ha et al., 1995a and b), application of minimal media for more representative bacterial enumeration (Maciorowski et al., 2002a), and extraction procedures to improve recovery of bacterial populations attached to feeds (Maciorowski et al., 2002b). However, there is a need for more rapid methods to detect Salmonella directly on feeds and to avoid the requirement for growth of isolates (Ricke et al., 1998; Maciorowski et al., 2005). Immunological approaches may have sensitivity limitations which preclude routine use in feeds where Salmonella contamination levels may be not only low but unevenly distributed within a batch of feed (Ricke and Pillai, 1999; Jones and Richardson, 2004; Maciorowski et al., 2004 and 2006; Ricke, 2005). Immunoassay approaches combining immunomagnetic sepa-

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ration with an ELISA method have been used to improve detection sensitivity for specic Salmonella serovars in animal feeds and can accomplish recovery in less than 27 hours compared to 72 to 96 hours required for cultural isolation and detection (Manseld and Forsythe, 2001). However, this approach still required an 18 hour conventional preenrichment step and a 6 hour enrichment step (Manseld and Forsythe, 2001). Molecular-based approaches have been proposed as an alternative for direct detection and identication of Salmonella spp. in feeds to avoid cultural enrichment and achieve improved sensitivity (Ricke et al., 1998). For identication, DNA microarrays have been used to genetically classify isolates from feed mills (Alvarez et al., 2003). Polymerase chain reaction (PCR) assays have been successfully applied to detection of Salmonella spp. in animal feeds but some cultural preenrichment appears to be generally unavoidable to achieve optimal results (Maciorowski et al., 1998 and 2000; Stone et al., 1998; Schrank et al., 2001; Lfstrm et al., 2004; Salomonsson et al., 2005). To accomplish direct PCR detection several nucleic acid extraction methods and other means to improve bacterial DNA recovery from feed matrices have been examined with limited success (Maciorowski et al., 2001a and 2005). The inconsistent pattern of Salmonella feed contamination lead Jones and Richardson (2004) to emphasize the merits of using non-Salmonella indicator organisms for routine surveillance of microbial quality control in feed production. Enterobacteriaceae and Escherichia coli bacteriophage have been considered as possible indicator organisms in feeds (Veldman et al., 1995; Maciorowski et al., 2001b; Jones and Richardson, 2004; Ricke, 2005). Detection of bacterial ribosomal genes has also been examined as a potential indicator of microbial quality on animal and poultry feeds (Maciorowski et al., 2002c and d). There may also be alternative approaches to sampling for Salmonella in the feed mill that avoid the logistical problems of collecting large numbers of feed samples. Jones and Richardson (2004) noted the potential important contribution of Salmonella contaminated dust in feed mills and pointed out the need for control of dust control within areas such as the pellet feed mill. General airborne bacterial levels and Salmonella concentrations in dust have previously been examined for poultry house and animal waste sites using air samplers and molecular detection methods (Pea et al., 1999; Kwon et al., 1999, 2000a and b; Endley et al., 2001; Pillai and Ricke, 2002; Woodward et al., 2004). Combining rapid molecular techniques with aerosol sampling potentially represents a feasible means for quickly assessing environmental levels of Salmonella contamination in feed mill facilities.

6. Potential risk factors for Salmonella feed contamination Morales (1998) dened risk analysis for foodborne pathogens to essentially involve three components: (1) microbial risk assessment, (2) risk management and (3) risk communication. Microbial risk assessment has received considerable focus utilization for poultry meat and other animal food products (Kelly et al., 2003; Oscar, 2004). For animal feeds microbial risk assessment for Salmonella contaminated feeds essentially involves a 2-fold

question of how likely is a batch of feed to be contaminated and how likely is that contaminated feed to cause infection of the pathogen in animals that ingest this feed. From a public health perspective, an additional question which is much more difcult to address, involves the likelihood that these Salmonella infected animals can cause foodborne disease in humans (Davies et al., 2004). The importance of animal feed as a microbial foodborne risk has been extensively debated with mixed conclusions. This is partially due to the complexity of feed production as well as the lack of comprehensive epidemiological data for a wide spectrum of animal production systems. Levels of incidence in feeds and feed production, HACCP and detection methods have been discussed in previous sections. The following sections will address potential vectors for contaminating feeds and the role that physiological status of Salmonella may play after feed contamination. One of the primary issues for the likelihood of animal feeds in feed mills, storage sites and animal houses becoming contaminated with Salmonella spp. is the transmission routes between the environment and the location of the feed. A transmission route that always needs to be considered is the types of vectors present which may be harboring Salmonella spp. A partial list of non-mammalian wildlife that have been demonstrated to carry Salmonella and could potentially come in contact with feed sources and food production animals include toads, vultures, lizards, tree frogs, and wild passerine birds (Everard et al., 1979; Kapperud et al., 1998). A partial list of documented infected and / or carrier mammalian species include rats, mice, Sika deer, mongooses, bats, monkeys, and opossums (Thigpen et al., 1975; Everard et al., 1979; Henzler and Opitz, 1992; Singer et al., 1992; Sato et al., 2000). Domestic cats and companion animal facilities have also been shown to be problematic for Salmonella (Singer et al., 1992; van Immerseel et al., 2004a; Wright et al., 2005). Insects represent an additional potential carrier of Salmonella spp. in farm and feed facilities and cockroaches have been the most extensively characterized (Klowden and Greenberg, 1976 and 1977; Devi and Murray, 1991; Jones et al., 1991; Kopanic, Jr. et al., 1994). Since the range of vectors differs not only in type but even in mode of transport (for example vectors that can y versus ones that cannot) implementing these as potential risks is fairly complex and requires a comprehensive survey to identify individual vectors for the liklihood that they may come in contact with feed. When considering the potential risk of producing Salmonella positive animals through the consumption of contaminated feed, the issue of bacterial survival capabilities becomes a concern. Indirectly, feed can inuence the ability of Salmonella to survive in the animal. Mikkelson et al. (2004) found that physical feed processing such as grinding to produce a coarse ground feed particle size (versus a nely ground feed) could decrease survivability of S. Typhimurium in the pig gastrointestinal tract. Long term survival of Salmonella in the feed during storage is an issue as well. Ha et al. (1998) observed an average 0.5 log10 reduction of S. Typhimurium per gram of feed from experimentally inoculated poultry mash after fty-six days of storage at room temperature. It is unclear whether overall feed composition is an important factor as Ha et al. (1998) noted little difference in survival between feeds containing meat and

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bone meal versus SBM after this storage time. However, it does appear that survival of Salmonella in feed is both moisture and temperature dependent. Williams and Benson (1978) reported that Salmonella could survive up to sixteen months in feed stored at 25 C and at least 18 months at 11 C. Juven et al. (1984) noted that Salmonella survival was greater at lower water activities in dry foods and feeds. This corresponded to an earlier report by Carlson and Snoeyenbos (1970) that there appeared to be an inverse relationship between viable Salmonella population levels and moisture level. They observed that increases in moisture corresponded to decreases in viable Salmonella except at moisture levels that permitted bacterial growth. The ability of Salmonella to survive in animal feeds for extended periods of time could make it more difcult to track the initial source(s) of particular serotypes. This becomes an issue when the serotype may have contaminated the feed at some time both historically and geographically that is very far removed from the current storage or feeding site. The ability of Salmonella to elicit survival capabilities may have physiological and pathogenic ramications as well. Salmonella and other foodborne pathogens become virulent when exposed to different stress factors such as non-optimal pH, oxygen availability, and osmolarity (Mekalanos, 1992; Foster and Spector, 1995; Bajaj et al., 1996). In addition to the synthesis of toxins and survival factors, virulence is expressed via production of a variety of attachment and invasion proteins that interact with the intestinal cells (Darwin and Miller, 1999). It is conceivable that Salmonella is sufciently exposed to a number of byproducts from different production aspects both in feed and food product manufacture, where virulent activity could be activated. Although this has not been examined directly in feeds, limited evidence does exist for stimulation of a S. Typhimurium virulent gene after exposure to poultry drinking water and from extracts of some food matrices (Nutt et al., 2002 and 2003). However, the question remains as to whether feed processing directly inuences the virulence status of Salmonella contaminants. In addition, even if virulence is stimulated by certain processing conditions, the issue then becomes one of whether this physiological change is sufciently stable to impact the animal that consumes that feed. Technologically, this has been a difcult question to answer but the availability of quantitative PCR may allow for the capability of assessing the level of Salmonella gene expression during and after feed processing (Maciorowski et al., 2005). If it is possible to quantitate virulence expression in Salmonella, this would allow for a more accurate risk assessment of potential infectivity dosage for different feeds and feed processing conditions.

have included the addition of chemicals such as acids, alcohols and other compounds. Physical treatment such as heating, which has been discussed in a previous section of this review, can also be considered as an antimicrobial feed treatment. Irradiation has also been examined as a potential means to eliminate Salmonella spp. and other bacterial contaminants on feeds (Leeson and Marcotte, 1993). Acid feed disinfection using a wide variety of different organic acids has been extensively reviewed (Williams, 1981c; Ha et al., 2000; van Immerseel et al., 2002; Ricke, 2003b; Maciorowski et al., 2004; Ricke et al., 2005). The typical approach has been simply to add a certain amount of organic acid directly to the feed or to feed ingredients and either examine effectiveness for direct reduction of Salmonella spp. in the feed or subsequent reduction of colonization in the animal. Several attempts have been made to increase the effectiveness of organic acid treatments. Better delivery of acids to the intestine has been attempted using either carriers coated with mixtures of acids (Hinton and Linton, 1988; Iba and Berchieri, 1995; Berchieri and Barrow, 1996), activated charcoal (Watarai and Tana, 2005) or microencapsulation (van Immerseel et al., 2004b). To achieve increased potency, combining potentially synergistic acids such as formic and propionic acid have been demonstrated to effectively decrease Salmonella shedding in hens and broiler chickens (Thompson and Hinton, 1997; Hinton and Linton, 1988). Acid / non-acid combinations have proved effective in the feed as well. Matlho et al. (1997) noted that the destruction of S. Enteritidis in poultry feed could be increased by applying a heat treatment along with propionic acid. More recently, feeding fermented liquid feeds has been explored as a potential means to prevent colonization of Salmonella and Enterobacteriaceae in poultry and swine (van Winsen et al., 2001; Canibe and Jensen, 2003; Heres et al., 2003).

8. Feed additives to control Salmonella 8.1 Feed additives to prevent Salmonella spp. colonization Animal feeds have also been used as the carrier for feed amendments that are designed to prevent colonization of ingested Salmonella spp. Prebiotics are generally compounds that are not utilizable by the host animal but selectively used by the gut microora and are therefore stimulatory to a portion of the gut microora presumed to be benecial to the host (Patterson and Burkholder, 2003). Probiotic cultures consist of single microorganisms or combinations of several to many microorganisms that when ingested by the animal can become established and serve as a protective microora to prevent colonization in the gastrointestinal tract by pathogens. These protective cultures have been developed for control of Salmonella and other foodborne pathogens in most food animals including aquaculture and the theoretical and practical aspects have been extensively reviewed elsewhere (Fuller, 1992 and 1997; Ricke and Pillai, 1999; Verschuere et al., 2000; Nisbet, 2002; Patterson and Burkholder, 2003; Ricke et al., 2004c; Mead, 2005). Both prebiotics and probiotics are considered nonspecic in their prevention since limiting colonization of pathogens such as Salmonella by these compounds is dependent on either establishing or selecting for a gastrointestinal microbial popu-

7. Reduction and / or elimination of feedborne Salmonella Preventing Salmonella contaminated feed from infecting animals that consume it can be accomplished either by reducing or eliminating the level of Salmonella contamination in the feed and / or preventing subsequent colonization of ingested Salmonella spp. A number approaches have been devised in an attempt to reduce if not completely eliminate Salmonella spp. contamination in animals feeds. The primary control methods

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lation that is subsequently inhibitory to the ingested pathogen. A possible alternative that is more specic is the feeding of antibodies for oral passive immunization against bacterial pathogens (Kovacs-Nolan and Mine, 2004). Antibodies have advantages over other antimicrobial approaches in that they can attach to surface antigens and alter their colonization capability without disrupting the normal microora (Berghman et al., 2005). A primary limitation to antibody oral therapy is the risk of potential denaturation by the acidic pH of the stomach and degradation by digestive tract proteases (Berghman et al., 2005). There is a clear need for either generation of antibodies that are resistant to these conditions or development of another means for delivery of biologically active antibodies in the gastrointestinal system. Specic antibodies contained in crude egg yolk preparations have been shown to be more resistant to gastric acid pH and proteases than puried sources in vitro (Lsch et al., 1986; Schmidt et al., 1989) and in vivo oral administration of egg yolk antibodies has been successfully used for the prevention of salmonellosis infections in mice (Peralta et al., 1994; Yokoyama et al. 1998a) and calves (Yokoyama et al., 1998b). However, production of large quantities of specic antibodies still requires intensive animal management and antibody harvesting logistics which may preclude routine use of such sources. As an alternative, Berghman et al. (2005) have suggested that genetically engineering antibody production in corn and soybean crops may be a viable future source of antibodies for routine feeding to animals.

however, can be a limitation because as Joerger (2003) points out, no single phage is capable of attacking all Salmonella serovars. Another key for using bacteriophage as a biological feed amendment is assuring an effective oral administration of the phage and survival of the phage until it arrives to sites in the intestine colonized by the respective pathogen (Huff et al., 2004). However, this may be less of a concern since viable phage can be isolated from intestinal tracts as well as from feed (Macioroski et al., 2001b; Joerger, 2003). This suggests that phage survival in these potentially hostile environments is possible. Other limitations include the potential for gene transfer among phage infected bacteria, development of bacterial resistance, and potential governmental regulation issues (Huff et al., 2004).

9. Conclusions Animal feeds as a source of foodborne Salmonella spp. continues to be an ongoing issue. Questions still remain as to how important feeds are as a reservoir for Salmonella that will potentially infect and persist in poultry ocks and animal herds. Clearly, more extensive epidemiology and tracking studies need to be done to better assess the role of feeds in contributing to prevalent Salmonella spp. that are problematic to continuing foodborne disease occurrences. However, more emphasis will need to be placed on the survival and physiological status of the Salmonella that frequent feeds and feed ingredients. In addition, the inuence of environmental conditions imposed on feedborne Salmonella during feed processing needs to be addressed. It is possible that feed processing may contribute selective pressure on resident Salmonella that in turn inuences virulence and subsequent infectivity dosage. There is also a concern with thermal processing and the risk of recontamination. Consequently, using HACCP approaches to identify critical areas where the feed mill environment may harbor Salmonella spp. needs to be considered. Limiting Salmonella contamination in feeds remains elusive partially because the uncertainty of sources and origins of Salmonella and the subsequent infrequent nature of the contamination levels. To be cost effective the treatment of feed will probably need to be selectively applied in conjunction with a HACCP program. The future for minimizing the impact of Salmonella contaminated feed as a potential contributor to foodborne disease would be to develop more efcient monitoring and sampling approaches for individual feed batches and sources as well applying more rapid and sensitive detection methodologies. Acknowledgments This review was supported by the Texas Higher Education Coordinating Boards Advanced Technology Program (Grant #999902-165) by Hatch grant H8311 administered by the Texas Agriculture Experiment Station. K.G.M. was supported by an Endowed Graduate Fellowship from Pilgrims Pride Inc., Pittsburg, TX, and Heep Foundation Internship. P.H. is supported by USDA-NRI grant #2004-04571.

8.2 Feed additives to eliminate colonized Salmonella spp. Antibiotics have been routinely added to feeds as therapeutic growth promoters for over a half century (Dibner and Richards, 2005). Antibiotics have also been used to eliminate colonized S. Enteritidis in molted laying hens and young chicks (Seo et al., 2000; Asakura et al., 2001; Holt, 2003). However, the potential spread of antibiotic resistance arising from agricultural sources and spreading to humans has become a controversial issue in the public sector (Donoghue, 2003; Jones and Ricke, 2003; Roe and Pillai, 2003; Bywater, 2005). Consequently, there has been more interest in alternative chemicals and biologicals that can accomplish the same outcome without the potential for transmissible resistance. Recently, Anderson et al. (2005) summarized their research on chlorate and nitro-based feed supplements demonstrating that they could reduce experimental infections of several foodborne pathogens in swine, cattle, sheep, and chickens. Bacteriocins which originate from bacteria and elicit antimicrobial properties against other bacteria have been examined for use in foods (Joerger, 2003). However, the production cost for bacteriocins may be prohibitive for large scale use in feeds. Bacteriophages which are viruses that infect and replicate in bacteria, have received renewed interest as biological agents to eliminate pathogen infections in food animals (Joerger, 2003; Huff et al., 2005). Bacteriophages have the advantage over broad spectrum antibacterial agents because of their specicity for particular strains of bacteria. Consequently, phage can lyse susceptible pathogenic bacteria such as Salmonella spp. while leaving benecial microora unharmed. This,

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