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FOOD SAFETY |
* National Farm Medicine Center, Marshfield Clinic Research Foundation, Marshfield, WI 54449; and
Division of Microbiology, National Center for Toxicological Research, US Food and Drug Administration, Jefferson, AR 72211
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Abstract |
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 Top Abstract INTRODUCTIONBACKGROUNDSALMONELLA IN SWINESALMONELLA IN CHICKENSSALMONELLA IN TURKEYSMAJOR SEROVARS OF SWINE,...CONCLUSIONSLITERATURE CITED |
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Key Words: chicken • pathogenicity • Salmonella • swine • turkey
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INTRODUCTION |
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TopAbstractINTRODUCTIONBACKGROUNDSALMONELLA IN SWINESALMONELLA IN CHICKENSSALMONELLA IN TURKEYSMAJOR SEROVARS OF SWINE,...CONCLUSIONSLITERATURE CITED |
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; Voetsch et al., 2004). An estimated 95% of these salmonellosis cases are associated with the consumption of contaminated of food products (Mead et al., 1999). Salmonellosis is most often attributed to the consumption of contaminated foods such as poultry, beef, pork, eggs, and fresh produce. Direct contact with infected animals may also serve as a source for Salmonella infections (Tauxe, 1991; Benenson et al., 1995). The dynamics of Salmonella infections have proven to be quite variable and are affected by changes in human demographics and lifestyles, human behavior, changes in industry and technology, changes in travel and commerce, the shift toward global economy, microbial adaptation, breakdown in the public health infrastructure, and the lack of knowledge on food safety and handling practices among consumers (Knabel, 1995; Altekruse et al., 1997; Hall, 1997). An improved understanding of how the populations of Salmonella associated with food animals have changed over time due to changes in selection pressure and management practices will aid in planning for future strategies to limit the human health impact of Salmonella. A primary focus of this review is the factors associated with serotypes that are common to swine, poultry, and human infections. Major topics that are reviewed herein include a retrospective assessment of the predominant Salmonella serovars that have been commonly detected among each of the food animal species, an examination of Salmonella contamination of food animals and their products along the production and processing continuum, and a look at some of the serovars that are commonly detected in swine and poultry and are a significant cause of human salmonellosis. |
BACKGROUND |
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TopAbstractINTRODUCTIONBACKGROUNDSALMONELLA IN SWINESALMONELLA IN CHICKENSSALMONELLA IN TURKEYSMAJOR SEROVARS OF SWINE,...CONCLUSIONSLITERATURE CITED |
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). With the increased consumption of pork and poultry, also comes increased potential for exposure to Salmonella through these food commodities. Due to this risk of pathogen exposure through the food supply, food producers and the US government have implemented food safety programs to reduce pathogens entering the food supply and to respond following a potential contamination of the food supply (Swaminathan et al., 2001; Rose et al., 2002).
Contamination of swine and poultry with Salmonella can occur prior to entry into the processing facility and by cross contamination in processing plants. There have been a number of advancements that have taken place to improve the microbiological quality of meat and poultry in the processing areas. Several physical and chemical decontamination procedures have been applied to carcasses in an attempt to reduce or eliminate Salmonella contamination. However, these procedures have not been completely successful in eliminating Salmonella. One area that could contribute significantly toward a reduction in the level of Salmonella contamination of meat and poultry is the development of on-farm practices that reduce the number of Salmonella-contaminated animals arriving at the processing plants. This reduction necessitates comprehensive control at the farm where the animals are born or hatched and raised before shipment to processing plants. Breeder herds and flocks, hatcheries, contaminated feed and water, and environmental sources and vectors, such as litter, animal caretakers, and insects, are potential preharvest sources of Salmonella contamination in swine and poultry (Bailey, 1993; Nayak et al., 2003). A combination of pre- and postharvest intervention strategies should ultimately provide consumers with safer meat and poultry products, which would significantly reduce the medical and productivity costs associated with salmonellosis. Because of the increase of consumption and the significant overlap of foodborne pathogens commonly associated with swine and poultry, a review of the relevant literature and related data is important to further our understanding of Salmonella associated with food animals.
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SALMONELLA IN SWINE |
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TopAbstractINTRODUCTIONBACKGROUNDSALMONELLA IN SWINESALMONELLA IN CHICKENSSALMONELLA IN TURKEYSMAJOR SEROVARS OF SWINE,...CONCLUSIONSLITERATURE CITED |
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). Much of the Salmonella serotyping on veterinary isolates in the United States is conducted by the USDA National Veterinary Services Laboratory (NVSL) in Ames, IA. The serotyping performed at NVSL includes isolates collected from nonclinical sources as part of flock and slaughter surveillance and research efforts and from clinical sources, such as those from veterinary diagnostic laboratories (CDC, 2006c). Examining the number of isolates of a particular serovar that are identified by NVSL for different food animal species provides a good view of the trends that various serotypes contribute to the overall Salmonella carriage in different animal species. However, the data from NVSL need to be viewed with a certain understanding that due to the means of collection, there may some bias in the data. The great majority of swine isolates are from clinical sources, compared with isolates from chickens and turkeys, which are more heavily weighted to surveillance sources (Table 1). That being said, a review of the serotypes numbers for isolates from swine over the last 20 yr identified some interesting trends (Ferris et al., 1987, 1999, 2000, 2001, 2002, 2003; Ferris and Frerichs, 1988a,b; Ferris and Miller, 1989, 1990, 1991, 1992, 1996, 1997, 1998; Ferris and Thomas, 1993, 1994, 1995; CDC, 2004, 2005, 2006c). From 1986 to 1995, the predominant serovar identified was S. Choleraesuis (Figure 1). In 1996, Derby was the most commonly identified serovar. Derby was subsequently replaced in 1997 by S. Typhimurium, which has remained the most commonly identified serovar from swine. In 2005, the most commonly detected Salmonella serovars were S. Typhimurium (n = 784), Derby (n = 386), S. Heidelberg (n = 164), S. Choleraesuis (n = 153), and Agona (n = 91), among the 2,175 total isolates (Table 1). When the results of isolates from clinical sources were compared with those from nonclinical sources, differences were evident. Among the non-clinical isolates, Derby was the most commonly detected serovar, compared with S. Typhimurium for the clinical isolates. There were also no S. Choleraesuis isolates detected among the nonclinical isolates (CDC, 2006c). These results appear to indicate that S. Typhimurium and S. Choleraesuis may be more pathogenic to swine than other serovars.
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As mentioned above, data from the NVSL indicated that S. Choleraesuis was replaced as the predominant serovar detected in swine following 1995, and this could be attributable to a number of factors. The first is that overall numbers of S. Typhimurium identified increased throughout much of the 1990s, whereas the number of S. Choleraesuis isolates identified decreased or remained steady. Secondly, NVSL started to charge fees for serotyping services for part of 1993, which may have led to a decrease in the number of isolates submitted for typing. In contrast to isolates from most other serovars, S. Choleraesuis isolates can be identified by biochemical testing and serogrouping without sending isolates to NVSL for the full serotyping (Ferris and Thomas, 1994). If diagnostic laboratories performed much of the S. Choleraesuis testing in-house, this likely would have led to an under-representation of the true contribution of S. Choleraesuis to swine in the NVSL numbers.
Salmonella Choleraesuis is an important serovar for human health due to its highly invasive nature in human. The pathogen is a relatively rare cause of illness in the United States, with an average of approximately only 40 cases per year over the last decade, whereas it remains a predominant problem in many Asian countries, including Thailand and Taiwan (Chiu et al., 2004; CDC, 2006c). For example, it was the second most identified serovar in Taiwan after S. Typhimurium (Chiu et al., 2004). Analysis of the S. Choleraesuis genome found a large number of pseudogenes associated with mutations in genes implicated in virulence and chemotaxis that has likely contributed to the increased invasiveness of these strains in humans (Chiu et al., 2005). Thus, the control of S. Choleraesuis remains an important veterinary and human public health concern.
Salmonella Prevalence in Swine
In the United States there are approximately 185 million hogs raised and sold each year from approximately 82,000 farms (USDA, 2004). The prevalence of Salmonella positive animals from these farms appears to quite variable depending on the farms surveyed. A study by Barber et al. (2002) found that 1.4 to 3.1% of swine on the farms that they sampled were positive for Salmonella. These results were less than for other multifarm studies, which found that between 3.4 and 33% of animals and fecal samples were positive for Salmonella (Davies et al., 1998; Rodriguez et al., 2006). The type of farm also may factor into the prevalence of Salmonella-positive animals. Davies and colleagues (1998) found that the prevalence on gilt developmental farms was 3.4%, whereas on breeder farms the prevalence was between 18 and 22%.
At the slaughter plant, there is also significant variability among herds for Salmonella carriage. Gebreyes et al. (2004) examined pigs from 5 farms and followed the animals through the slaughter process. The percentage of Salmonella-positive fecal samples on the farm and mesenteric lymph node and cecal samples at the slaughter plant was highly variable. The percentage of on-farm positive fecal samples ranged form 0 to 42%, whereas the percentage of positive samples at the slaughter plant ranged from 0 to 77%. The herds with the highest percentage of fecal positive isolates on the farms also had the highest rates of contamination at the slaughter facility. In a review of federal testing results of inspected abattoirs for 1998 through 2000, it was found that the annual percentage of positive carcasses ranged from 5.8 to 9.8% for A set samples collected at the facilities. The A sets are the samples collected during the initial round of testing at a particular facility. Facilities that fail the initial testing are subjected to further testing and the collection of B (and potentially C and D sets) are collected if corrective actions are not successful (Rose et al., 2002). These numbers were greater than the USDA inspection testing results obtained for market hogs from 2003 to 2006, which ranged from 2.5 to 4.0% positive per year (USDA, 2007c). Therefore, it appears that the pathogen reduction: hazard analysis and critical control point (PR-HACCP) programs implemented by USDA and meat processors have had a positive effect on reducing Salmonella contamination at the slaughter plant. There was also variability in retail meat samples, with the percentage of positive samples for Salmonella ranging from 1 to 16%. The lowest positive levels were in pork chops (1 to 3.3%) and the highest in ground pork (16%), which could reflect comingling of tissue from multiple animals into the ground product (Zhao et al., 2001, 2006).
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SALMONELLA IN CHICKENS |
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TopAbstractINTRODUCTIONBACKGROUNDSALMONELLA IN SWINESALMONELLA IN CHICKENSSALMONELLA IN TURKEYSMAJOR SEROVARS OF SWINE,...CONCLUSIONSLITERATURE CITED |
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). Contaminated poultry meat and eggs, particularly when the bacterium is present in the egg contents, are important vehicles of Salmonella infections. Several factors can affect the susceptibility of poultry to Salmonella colonization (Bailey, 1988). These include 1) age of birds; 2) Salmonella serotype and initial challenge dose level; 3) stress, including environmental, transport, and overt or subclinical disease; 4) presence of feed additives, such as antimicrobials and anticoccidials; 5) survival through low pH of the stomach; 6) competition with gut microflora; 7) presence of a compatible colonization site, and 8) host genetic background. There are several potential sources of Salmonella contamination in an integrated poultry operation. Chicks are very susceptible to Salmonella infection and gut colonization from hatching to 96 h of age (Bailey, 1988). These chicks can be infected by vertical transmission through infected parents or by horizontal transmission through hatcheries, sexing in contaminated hatcheries, cloacal infection, transportation equipment, and feed (Lahellec and Colin, 1985; Opitz et al., 1993). Environmental factors such as air, litter and unclean facilities, and vectors, such as insects, humans, and rodents, are responsible for Salmonella contamination in poultry farms (Jones et al., 1991; Hoover et al., 1997; Amick-Morris, 1998).
Chickens can be infected with many different serovars of Salmonella. Some serovars, such as S. Pullorum and S. Gallinarum, are host specific for chickens, whereas other serovars, such as S. Typhimurium, S. Enteritidis, and S. Heidelberg, are able to infect a wide range of hosts. There are a number of commonly identified serotypes of Salmonella associated with chickens in the United States (Table 2), with the most common serovars being S. Enteritidis, S. Kentucky, S. Heidelberg, S. Typhimurium, and S. I 4,[5],12:1- for clinical isolates and S. Heidelberg, S. Kentucky, S. Typhimurium, S. Senftenberg, and S. Enteritidis for nonclinical isolates (CDC, 2006c). The trends for the most common Salmonella serovars over the last 20 yr are summarized in Figure 2 (Ferris et al., 1987; 1999, 2000, 2001, 2002, 2003; Ferris and Frerichs, 1988a,b; Ferris and Miller, 1989, 1990, 1991, 1992, 1996, 1997, 1998; Ferris and Thomas, 1993, 1994, 1995; CDC, 2004, 2005, 2006c). Since 1997, S. Heidelberg has been the most prevalent serovar reported, with a peak in 2000 of just over 50% of all isolates reported being S. Heidelberg (Figure 2). In the early to mid 1990s, S. Enteritidis was the most frequently reported serotype in the United States, as well as in Europe (Velge et al., 2005).
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In the early 1900s, pullorum disease and fowl typhoid, caused by S. Pullorum and S. Gallinarum, respectively, were widespread in the United States (Shivaprasad, 2003). The National Poultry Improvement Plan (NPIP), established in 1935, was partly designed to help control and eradicate pullorum disease and fowl typhoid (USDA, 1997). Pullorum disease and fowl typhoid were eradicated from commercial flocks largely through control programs, such as NPIP, by the mid 1960s (Baumler et al., 2000). It has been proposed that the emergence of S. Enteritidis infections in the 1990s may correspond with the eradication of S. Gallinarum in poultry. Prior to the 1960s, S. Enteritidis was rare among poultry; however, with the reduction and elimination of S. Gallinarum and S. Pullorum, the prevalence of S. Enteritidis in chickens increased. Before the increase in S. Enteritidis infections in chickens, the serovar was commonly detected in rodents and potentially made the jump to birds as immunity to S. Pullorum waned in the flocks (Baumler et al., 2000). Strains from S. Enteritidis, and S. Gallinarum displayed the same O antigen (O9) of the lipopolysaccaride on their cell surfaces, which likely contributed to competition between the 2 serovars in poultry (Gupta et al., 1996; Velge et al., 2005). Mathematical models suggest that S. Gallinarum competitively excluded S. Enteritidis from poultry (Rabsch et al., 2000). Therefore, it appears likely that S. Enteritidis filled an ecologic niche that was created by the eradication of S. Gallinarum and S. Pullorum in poultry (Rabsch et al., 2001; Velge et al., 2005).
Since the mid 1990s, the prevalence of S. Enteritidis has been declining in chickens, whereas that of S. Heidelberg has been rising. The decline of S. Enteritidis can be attributed to many factors. One major factor is that the NPIP added S. Enteritidis to its improvement plan for eggs and meat in 1989 and 1994, respectively, which targeted flocks with S. Enteritidis contamination problems (USDA, 1997). The decline could also be aided by an increase in the natural flock immunity of the poultry population. As the frequency of bird populations becoming infected with or vaccinated against a serotype increases, the frequency of the population becoming immune to serotypes containing similar antigens also increases. With increased flock immunity, there is a likelihood that there will be a reduction in the number of cases of disease until the number of cases gets too small that the majority of the flock loses the immunity and again is susceptible to infection (Cogan and Humphrey, 2003). Vaccines directed toward S. Enteritidis are often employed to maintain a high level of immunity in flocks to prevent potential widespread infection (Cogan and Humphrey, 2003). The emergence of S. Heidelberg as the most commonly detected serovar in chickens following the implementation of NPIP and the corresponding decline in S. Enteritidis infections could signify that S. Heidelberg is occupying the ecological niche left by the decline of S. Enteritidis. Salmonella Heidelberg has been shown to colonize the reproductive tract and enter eggs, similar to what is observed with S. Enteritidis (Gast et al., 2004, 2005b, 2007).
Salmonella Prevalence in Chickens
In studies that have examined the prevalence of Salmonella on chicken farms and colonizing birds, there has also been large interflock variability. The percentage of Salmonella-positive birds and fecal samples on farms has ranged from 5 to 100% (Carraminana et al., 1997; Bailey et al., 2002). In a study by Bailey et al. (2002), samples taken from hatcheries had the greatest percentage of positive samples and those taken from breeding stock had the least. At the slaughter plant, Salmonella-positive samples ranged from 8 to 34%. These samples include carcass samples and rinse water sampling (Bailey et al., 2002). The results of USDA PR-HACCP inspection testing of A set samples for broiler carcasses from 1998–2006 ranged from 10.9 to 16.3% positive per year (Rose et al., 2002; USDA, 2007c). The percentage of positive samples increased yearly from 2002 through 2005, which was opposite the desired trend; thus, the USDA Food Safety and Inspection Services (FSIS) instituted new sampling criteria to focus testing on the plants with the highest levels of Salmonella from serotypes that are most associated with human disease. Results from 2006 indicated that 11.4% of broilers were positive for Salmonella, which was down from 16.3% in 2005 (USDA, 2007c). When PR-HACCP testing of ground chicken meat was carried out in processing plants, 44.6% of the raw product was found to be contaminated with Salmonella in 1996 (McNamara and Levine, 1998). The percentage of USDA A samples positive for Salmonella for ground chicken decreased to a low of 13.8% in 1999 before increasing significantly to the point where 45.0% of samples were positive in 2006 (Rose et al., 2002; USDA, 2007c). Indeed, this percentage of positive samples in 2006 was greater than the 1996 baseline for PR-HAACP testing in chicken processing facilities (McNamara and Levine, 1998; USDA, 2007c). On the retail end, up to 35% of meat samples tested positive for Salmonella. The greatest variability was among ground chicken samples (4.2 to 35% positive; CDC, 2002; Rose et al., 2002). Whole bird and chicken breasts generally had a lower percentage of positive samples (4.2 to 10%; Zhao et al., 2001).
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SALMONELLA IN TURKEYS |
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TopAbstractINTRODUCTIONBACKGROUNDSALMONELLA IN SWINESALMONELLA IN CHICKENSSALMONELLA IN TURKEYSMAJOR SEROVARS OF SWINE,...CONCLUSIONSLITERATURE CITED |
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; CDC, 1996; Grein et al., 1999). Several different serovars of Salmonella have been isolated from preharvest turkey environment. A comprehensive list of serovars isolated from turkeys is described by Hafez and Jodas (2000). These include, but are not limited to, S. Heidelberg, S. Hadar, S. Senftenberg, S. Newport, S. Reading, S. Bredeney, S. Agona, S. Anatum, S. Enteritidis S. Meleagridis, and S. Saintpaul (Baker et al., 1966; Hafez and Jodas, 2000).
Of the top 20 most common serotypes associated with human Salmonella infections, 5 are commonly isolated from turkeys (within the 10 most commonly detected in 2005). These common serotypes are S. Typhimurium, S. Heidelberg, S. Montevideo, S. Saintpaul, and S. Agona (CDC, 2006c). The great majority of turkey isolates are from nonclinical sources, compared with isolates from cattle and swine which are more heavily weighed to clinical sources (Table 3). A review of the serotypes numbers for isolates from turkeys over the last 20 yr demonstrated a great deal of diversity in the predominant serovars in each of the years (Ferris et al., 1987, 1999, 2000, 2001, 2002, 2003; Ferris and Frerichs, 1988a,b; Ferris and Miller, 1989, 1990, 1991, 1992, 1996, 1997, 1998; Ferris and Thomas, 1993, 1994, 1995; CDC, 2004, 2005, 2006c). Isolates from serovar S. Heidelberg were most commonly detected from 1986 to 1989, 1992, and 1999 to 2001. The predominant serovar in 1990, 1991, and 1994 was Reading; in 1995 and 1996 it was Brandenburg; in 1997, 2002, 2003, and 2004, it was S. Senftenberg; in 1998 it was S. Bredeney; and in 2005 the predominant serovar was S. Hadar (Figure 3). In 2005, there were 2,110 Salmonella from turkeys servotyped at NVSL, the most commonly detected serovars were S. Hadar (n = 643), S. Senftenberg (n = 387), S. Heidelberg (n = 154), S. Saintpaul (n = 110), and S. Typhimurium (n = 88). When the results of isolates from clinical sources were compared with those from nonclinical sources, there was some difference. Among the nonclinical isolates, S. Hadar was the most commonly detected serovar, compared with S. Senftenberg for the clinical isolates (CDC, 2006c). Isolates from serovars S. Heidelberg and S. Montevideo were also detected at greater percentages in Salmonella from clinical than nonclinical sources; interestingly, these were also more common human pathogens than isolates from serovar S. Hadar.
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During the past 20 yr, there have been 6 different serovars that have predominated. These include S. Heidelberg, S. Reading, S. Brandenburg, S. Senftenberg, S. Bredeney, and S. Hadar (Figure 3
). The majority of isolates tested are from nonclinical sources including routine flock and slaughter surveillance and food testing. Therefore, variability in sampling of isolates from different sources could confound the data from year to year. With some USDA surveillance sampling, producers or processors that have known contamination issues are targeted for more comprehensive testing, which could bias the numbers of the particular serovars common at certain locations (USDA, 2007a). Also, the turkey industry is highly integrated and has a limited number of large producers. The 2002 Census of Agriculture indicated that over 65% of turkeys raised in the United States were produced from 800 farms that reared greater that 100,000 birds (USDA, 2004). In these large production environments, turkeys are reared in high densities that increase the potential of disease spread among the animals being raised. If a particular serovar of Salmonella spread through one or more of these large farms in a particular region, it could skew the numbers for a particular year. For example from 1997 to 1998, the number of S. Bredeney isolates increased from 110 to 475, with much of the increase coming from isolates originating in North Carolina. The number of S. Bredeney isolates from North Carolina increased by 305 over this time (Ferris and Miller, 1997, 1998). The following year, 1999, the number of S. Bredeney isolates in turkeys from the entire United States decreased significantly to 119 (Ferris et al., 1999). The results indicate how a spike in isolates from one location can significantly affect the overall US prevalence. Therefore, looking at the trends over a number of years may provide a better picture of the trends in serotype numbers. Salmonella Heidelberg, S. Senftenberg, and S. Hadar have been the predominant serovars over the past decade (Ferris et al., 1999, 2000, 2003; CDC, 2004, 2005, 2006c).
Salmonella Prevalence in Turkeys
The detection of Salmonella among flocks and farms can be quite variable. In a study by Nayak et al. (2003), the frequency of detection in 4 turkey flocks raised on the same farm ranged from 0 to 21%. Furthermore, Salmonella was isolated from 13% of litter, 11% of turkey ceca, 10% of drinker, 5% of environmental swabs, 3% of feed, and 1% of feeder samples (Nayak et al., 2003). In another study, Salmonella was isolated from 13.6% of poult box liners, 25% of yolk sac samples, 53.8% of ceca, 14.8% of feed shipments, 39.1% of feeder contents, 51.1% of litter samples, 63.8% of drinkers, and 22.8% of air samples (Hoover et al., 1997).
A study of 6 commercial turkey flocks scheduled to be loaded and shipped to the abattoir found that about 33% of on-farm and slaughter turkey samples were positive for Salmonella, mostly originating from the cecal contents of the bird (Rostagno et al., 2006). The authors demonstrated that preslaughter practices such as feed withdrawal, catching, loading, and transportation do not significantly affect the prevalence of Salmonella in turkeys shipped to the processing plants. Additionally, a national survey of 276 Canadian registered commercial turkey flocks indicated that approximately 87 and 9% of litter and feed samples, respectively, were contaminated with Salmonella (Irwin et al., 1993). Of the 48 different serovars isolated from the study, S. Anatum, S. Hadar, S. Agona, S. Heidelberg, and S. Saintpaul were the most prevalent. Historically, there has also been large in-flock variability as well. McBride et al. (1978) reported considerable variation (0 to 72%) in the prevalence of Salmonella in 25 turkey flocks; serovars S. Agona (47%), S. Saintpaul (26%), and S. Reading (16%) were the major serovars isolated from these flocks.
The prevalence of USDA-tested Salmonella-positive birds arriving at slaughter facilities in 2006 was 7.1% (USDA, 2007c), which was down from 18.6% in 1997 (Eblen et al., 2006; Naugle et al., 2006; Wesley et al., 2006). Additionally, 49.9% of raw ground turkey meat was found to be contaminated with Salmonella from federally inspected plants in 1996 (McNamara and Levine, 1998). The percentage of USDA A samples positive for Salmonella for ground turkey decreased to 36.5% in 1998 and continued to decline until 2004 when 19.9% of samples were positive (Rose et al., 2002; USDA, 2007c). The percentages of positive samples in 2005 and 2006 were 23.2 and 20.3%, respectively. The percentage of Salmonella-positive ground turkey samples collected at the processing facilities decreased by nearly 60% from 1996 to 2006 following the implementation of the PR-HACCP program (McNamara and Levine, 1998; USDA, 2007c). Another study showed that the overall incidence of Salmonella in turkey processing plants was 16.7%, with greater prevalence of this pathogen observed in prechilled than postchill carcasses (Logue et al., 2003). Salmonella Agona, S. Hadar, S. Heidelberg, and S. Senftenberg were the major serovars isolated from these processing plants. Along the processing line, the percentage of positive isolates ranged from 6.4% for birds following postevisceration chilling to 30.7% in chill water samples (Logue et al., 2003). In the processing plants, the defeathering and scalding operations have been identified as being the major sources of Salmonella cross contamination (Nde et al., 2007). On the retail end, the highest percentage of positive samples were found in ground turkey (11 to 36.5%; Rose et al., 2002), whereas 2.6% of breast meat samples were positive (Zhao et al., 2001). In another study, S. Newport, S. Hadar, S. Heidelberg, S. 4:12:nonmotile, and S. Reading were isolated from turkey meat retail samples in Fargo, North Dakota (Fakhr et al., 2006). The authors found that of the 74 retail turkey meats samples collected, 30 were positive for Salmonella.
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MAJOR SEROVARS OF SWINE, POULTRY, AND HUMAN INFECTION |
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TopAbstractINTRODUCTIONBACKGROUNDSALMONELLA IN SWINESALMONELLA IN CHICKENSSALMONELLA IN TURKEYSMAJOR SEROVARS OF SWINE,...CONCLUSIONSLITERATURE CITED |
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Salmonella Typhimurium is the most common source of human salmonellosis in the United States and is in the top 5 most detected for each major food animal species (CDC, 2006c). Serologically, S. Typhimurium is a member of serogroup B, with serovars such as S. Heidelberg, S. Derby, and S. Agona (CDC, 2006c). Multiple virulence factors are present in the S. Typhimurium genome that allow for efficient colonization and invasion of the gastrointestinal tract (reviewed by Foley and Lynne, 2008). The genome contains at least 5 different pathogenicity islands: 1) SPI-1 encoding a type 3 secretion system (T3SS) associated with invasion; 2) SPI-2 encoding a T3SS associated with intracellular survival; 3) SPI-3 encoding genes associated with intra-cellular proliferation and Mg2+ uptake; 4) SPI-4, which contains genes for toxin secretion and apoptosis or host cell death, and 5) SPI-5, which encodes a number of different T3SS-associated proteins (Amavisit et al., 2003; van Asten and van Dijk, 2005). Most S. Typhimurium isolates also contain a virulence plasmid encoded fimbriae (pef genes) and Salmonella plasmid virulence (spv genes) factors, which are important for replication in extraintestinal sites such as the liver and spleen (Ahmer et al., 1999).
A 4-yr review of FoodNet data indicated that S. Typhimurium is 1 of the top 2 most commonly isolated serotypes from humans with salmonellosis and accounts for nearly 50% of patients who died from salmonellosis (Kennedy et al., 2004; Perch et al., 2004). Even though it is one of the most common serotypes associated with salmonellosis, S. Typhimurium has a disproportionately high mortality rate for the proportion of infections it causes (less than 20% of infections and 50% of deaths due to Salmonella). Additionally, many isolates are multidrug resistant. The National Antimicrobial Resistance Monitoring System (NARMS) reported that in 2003 for Salmonella isolated from humans, 45% of S. Typhimurium isolates were resistant to greater than or equal to 2 antibiotics. Of these, two-thirds were resistant to at least 5 antibiotics (CDC, 2006a).
Among the S. Typhimurium strains, there are a number of different divisions that can be made using different typing methods, such as phage typing (Baggesen and Aarestrup, 1998). One of these phage typing groups is Definitive Type 104 (DT104), which is a typically multidrug resistant group of S. Typhimurium that was first detected in the United Kingdom in the late 1980s (Cloeckaert and Schwarz, 2001; Humphrey, 2001). These DT104 isolates are an important cause of human disease, and many have the typical penta-resistance profile of resistance to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline (Glynn et al., 1998; Poppe et al., 1998). The resistance genes encoding the penta-resistance are located on the chromosome of DT104 strains, with the genes encoding ampicillin (blaPSE-1), streptomycin (aadA2), and sulfonamide (sul1) located in 2 separate integrons. The genes associated with resistance for chloramphenicol (floR) and tetracycline (tetR and tetA) are located between the 2 integrons, making up a 12.5-kb resistance locus in the chromosome. This locus sits within a larger genetic structure referred to as the Salmonella genomic island 1 (Cloeckaert and Schwarz, 2001). The DT104 isolates have spread throughout much of the world and reached the United States in the mid 1990s. The DT104 isolates were originally detected in cattle but now are widespread in swine and poultry as well (Humphrey, 2001). Many of the DT104 isolates have a relatively high level of genetic similarity based on pulsed field gel electrophoresis (PFGE) patterns; this similarity is often associated with more recently evolved biotypes or due to the clonal spread of pathogen. However, there are some DT104 strains that have distinct PFGE profiles (Markogiannakis et al., 2000). The data from NARMS indicates that from 1996 to 2003, that between 21 and 35% of S. Typhimurium isolates from humans tested were resistant to at least 5 drugs (ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline) associated with DT104 resistance phenotype (FDA, 2006).
Salmonella enterica Serovar Enteritidis
Salmonella Enteritidis is a serovar that can infect and cause disease in a broad range of hosts including poultry and a number of mammalian species (Baumler et al., 2000). Currently, S. Enteritidis is the most common serotype reported in human cases of salmonellosis in the European Union and the second most common serotype (behind S. Typhimurium) reported in the United States (CDC, 2006c; de Jong and Ekdahl, 2006). Like most Salmonella serotypes, S. Enteritidis has a variety of virulence factors that contribute to its pathogenicity. Salmonella employ a wide variety of fimbriae that aid in attachment of the bacterium to host tissue. Salmonella Enteritidis utilizes many of the different types of fimbriae, including SEF14, SEF17, SEF18, SEF21, long polar fimbriae, and plasmid encoded fimbriae (Thorns, 1995). Of these, SEF14 is limited to group D1 serovars, which includes S. Enteritidis and S. Gallinarum, and appears to be important for bacterial adhesion to tissues of the reproductive tract (Turcotte and Woodward, 1993). The effective colonization of the reproductive tract in poultry allows S. Enteritidis to be transmitted vertically to eggs and subsequently chicks following hatching. This efficient colonization and transmission likely aided in its rapid spread S. Enteritidis in poultry following the eradication of S. Gallinarum.
Salmonella Enteritidis isolates can also be distinguished further by phage typing. In the North America, the predominant phage types (PT) are PT8 and PT13, whereas PT4 is predominant phage type in Western Europe and Japan (Cogan and Humphrey, 2003; White et al., 2007). Although PT4 is still the most common phage type reported in Western Europe, its overall prevalence is starting to decline, whereas PT14b and PT21 are on the rise. In fact, from 1998 to 2003, the percentage of S. Enteritidis isolates identified as PT4 decreased from 61.8 to 32.1%, whereas PT14b and PT21 increased by 276 and 137%, respectively (Fisher, 2004). Although PT4 is not the most commonly identified phage type in the United States, it has been the cause of a number of outbreaks of S. Enteritidis (Passaro et al., 1996; Sobel et al., 2000; Burr et al., 2005).
Salmonella enterica Serovar Heidelberg
Salmonella Heidelberg is the fourth most common source of human salmonellosis in the United States and in the top 3 most detected serotypes for swine and poultry (CDC, 2006c). Salmonella Heidelberg was also the most common serovar detected by the retail meat wing of NARMS. The isolates of the serovar were typically associated with chicken breasts and ground turkey (Zhao et al., 2006). According to the most recent Food-Net data, the incidence of human infections by S. Heidelberg has increased by 25% over the last 10 yr, even while the overall number of cases of salmonellosis decreased by 9% (CDC, 2006b). Annually, infections with S. Heidelberg lead to approximately 84,000 cases of salmonellosis and contribute to approximately 7% of the Salmonella-related deaths in the United States, the second highest percentage after S. Typhimurium (Kennedy et al., 2004). The relatively high level of mortality associated with S. Heidelberg may indicate that members of the serovar have enhanced virulence in humans. Additionally, when disease outbreaks associated with Salmonella were examined from 1973 to 2001, it was found that there were 2,260 outbreaks, with 184 (8%) being attributed to S. Heidelberg (Chittick et al., 2006). Poultry, eggs, and egg-containing products were the primary identified vehicles of infection in the outbreaks.
Like S. Enteritidis, S. Heidelberg has been shown to be able to colonize the reproductive tract of layers and contaminate eggs (Gast et al., 2005a). The route of infection for the reproductive tract appears to be associated with the gastrointestinal route. Invasive Salmonella are transmitted systemically and subsequently colonize the ovary and oviduct (Gast et al., 2005a). Salmonella Heidelberg strains are capable of penetrating and growing in the interior of a hen’s egg, which could contribute to the spread to humans (Mammina et al., 2003; Gast et al., 2005b, 2007). In fact, a review of FoodNet data found that the consumption of undercooked eggs has been identified as a primary risk factor for the development of S. Heidelberg-associated salmonellosis (Aarestrup et al., 2004; FDA, 2006). Additionally, a number of strains have been also been reported to be resistant to multiple antimicrobial agents (Hennessy et al., 2004). Some strains have been found that are resistant to greater than 10 drugs, including third generation cephalosporins, and a number of the genes encoding the resistance are located on plasmids that have been shown to be conjugative, indicating the possibility for transfer to susceptible strains (Aarestrup et al., 2004). This potential for resistance spread is especially concerning because the organisms are known to cause severe disease that often requires antimicrobial therapy.
Salmonella enterica Serovar I 4,[5],12:i:-
Salmonella I 4,[5],12:i:- is a new serovar that appears to be emerging in poultry and humans. It is currently the sixth most common serovar reported in human and poultry isolates (CDC, 2006c). Salmonella I 4,[5],12:i:-is an atypical strain that emerged and spread in Spain in the mid 1990s (Echeita et al., 2001). When first serotyped using the Kauffman-White scheme, it was found that the strain could be a S. Typhimurium strain, a Lagos strain, a monophasic variant, or a new serovar. Much work has been done to further characterize the strain using serological, lysogenic, and genetic testing. Results showed that S. I 4,[5],12:i:- is a member of serogroup B, along with S. Typhimurium (Echeita et al., 1999). Further characterization showed that Enterica serovar S. I 4,[5],12:i:- was closely related to S. Typhimurium DT U302 based upon serotyping, PFGE, plasmid profiles, and antimicrobial resistance profiles (de la Torre et al., 2003). Salmonella I 4,[5],12:i:- is a different serovar due to the lack of a flagellar antigen (fljB) (Echeita et al., 2001). Also noteworthy is that many of these strains are resistant to multiple antimicrobials, including ampicillin, chloramphenicol, streptomycin, sulfonamide, tetracycline, gentamicin, and trimethoprim-sulfamethoxazole (Echeita et al., 2001).
Salmonella enterica Serovar Montevideo
Human infections associated with S. Montevideo are most often associated with the consumption of contaminated produce, prepared food, beef, and poultry. There have been some more recent outbreaks associated with sesame seeds, chocolate, and tomatoes (Zhuang et al., 1995; Hedberg et al., 1999; Unicomb et al., 2005; Health Protection Agency, 2006a). In food animals, the serovar is most often associated with sheep, cattle, and poultry (Guerin et al., 2005; Health Protection Agency, 2006b). In chickens, S. Montevideo strains are able to enter the yolk of eggs, which may make the consumption of undercooked eggs a potential risk for contracting S. Montevideo-associated salmonellosis (Murase et al., 2006). Animal handling has also been associated with disease outbreaks, including numerous outbreaks reported in children following the handling of young chicks and ducks around Easter time (CDC, 1997, 2007). This practice of purchasing live baby poultry has begun to be more regulated in some states, including setting minimum numbers of birds to purchase, in part, to discourage the purchasing the birds as short-term pets (CDC, 2007). Salmonella Montevideo is a member of serogroup C1, with serovars such as S. Choleraesuis and S. Infantis (Brenner and McWhorter-Murlin, 1998).
Salmonella enterica Serovar Saintpaul
Human infection with S. Saintpaul is one of the top serovars associated with disease in the United States, as well as in other countries, including Japan (Hata et al., 2003; CDC, 2006c). Salmonella Saintpaul was the second most commonly identified serovar detected by the retail meat portion of NARMS (Zhao et al., 2006). The majority of positive samples originated from ground turkey; therefore, turkey products are likely to be one of the more common sources of infection. The data from NVSL and CDC indicated that among the nonclinical isolates of S. Saintpaul from all nonhuman animal sources, 85% were associated with turkey samples (CDC, 2006c). In contrast, with clinical isolates of S. Saintpaul, only 20% were associated with turkeys as a source. The majority of clinical isolates were associated with mammalian hosts and "other birds and wild animals" (CDC, 2006c). This disequilibrium between clinical and nonclinical sources could potentially indicate that the serovar is less pathogenic to turkeys and displays a higher level of virulence in mammalian hosts, including humans. Salmonella Saintpaul is also member of serogroup B, along with serovars such as S. Heidelberg and S. Typhimurium (Brenner and McWhorter-Murlin, 1998).
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TopAbstractINTRODUCTIONBACKGROUNDSALMONELLA IN SWINESALMONELLA IN CHICKENSSALMONELLA IN TURKEYSMAJOR SEROVARS OF SWINE,...CONCLUSIONSLITERATURE CITED |
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When we look more specifically at food animal species, we saw that for each of the species examined, there was a change over the past 2 decades in the predominant serovars associated with the animal species. In swine, the shift appears to be a longer-term trend where S. Choleraesuis was replaced by S. Typhimurium in the mid 1990s, and S. Typhimurium remains the predominant serovar. In chickens, historically S. Pullorum and S. Gallinarum were significant problems to the poultry industry, which led in part to the development of NPIP. Following the implementation of control strategies, these serovars were eliminated from commercial flocks in the 1960s, allowing S. Enteritidis to predominate. Following the elimination S. Pullorum and S. Gallinarum, S. Enteritidis became the predominant serovar associated with chickens. Beginning in the late 1980s, the NPIP targeted S. Enteritidis, and by the mid 1990s S. Heidelberg became the predominant serovar associated with chickens. In turkeys, there has been a high level of variability in the predominant serovars over the past 20 yr. This variability is potentially due to the nature of the industry in which there are relatively few farms that raise the majority of birds in the United States. The presence of a particular serotype in a limited number of farms could, in all likelihood, allow the serovar to ascend to the top of the most detected serovar for the year. The trend over the past decade has been that serovars including S. Heidelberg, S. Senftenberg, and S. Hadar have consistently been among the top serovars detected in turkeys, which likely indicates their importance. Overall, Salmonella associated with swine and poultry industry remains a problem; however, strategies to target particular serovars appears to work to reduce pathogen numbers and human infections associated with those serovars. Unfortunately, it appears that when one serovar is targeted and the numbers reduced, other serovars fill the void created. Therefore a holistic management approach may be needed to significantly reduce the overall burden of Salmonella on human health.
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2 Disclaimer: The views expressed herein do not necessarily reflect those of the US Food and Drug Administration or the US Department of Health and Human Services.
3 Corresponding author: foley.steven{at}mcrf.mfldclin.edu
Received for publication July 26, 2007. Accepted for publication September 2, 2007.
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TopAbstractINTRODUCTIONBACKGROUNDSALMONELLA IN SWINESALMONELLA IN CHICKENSSALMONELLA IN TURKEYSMAJOR SEROVARS OF SWINE,...CONCLUSIONSLITERATURE CITED |
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