Animal Feed Science and Technology 75 (1998) 75±79
Short communication
A pilot survey of Salmonella enterica contamination of cattle feeds in the Pacific northwestern USA Denise S. Krytenburga, Dale D. Hancocka,*, Daniel H. Ricea, Thomas E. Besserb, Clive C. Gaya, John M. Gaya a
Field Disease Investigation Unit, Washington State University, Pullman, WA 99164-7060, USA b Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, WA 99164-7040, USA Received 9 December 1997; accepted 10 May 1998
Abstract Commercially prepared cattle feeds collected from the delivery or storage area of 12 farms (six dairy and six beef feedlot) in the American states of Washington, Oregon and Idaho were cultured for Salmonella enterica. Of 295 feed samples examined, 29 (9.8%) collected from six of the 12 farms were found to contain S. enterica. # 1998 Elsevier Science B.V. Keywords: S. enterica; Salmonella; DT104; Cattle; Feeds
1. Introduction Salmonellosis is an important disease of cattle (Radostits et al., 1994), and salmonella infections in cattle potentially expose humans to the risk of food-borne salmonellosis (Hancock et al., 1997). Although the role that contaminated animal feeds play in salmonella infections of food animals is not well understood, bacteriological monitoring of feeds in some countries has repeatedly demonstrated a relatively high salmonella contamination rate (Durand et al., 1990; Malmqvist et al., 1995; Veldman et al., 1995). A survey of salmonella contamination in swine feeds from the USA was recently reported, (Harris et al., 1997); however, the most recently published study documenting the rate of salmonella contamination in cattle feeds in the USA was reported over 30 years ago (Allred et al., 1967). The purpose of the present study was to estimate the frequency of Salmonella enterica in cattle feeds delivered to farms in the northwestern US. * Corresponding author. Tel.: +1-509-335-0711; fax: +1-509-335-0880; e-mail
[email protected] 0377-8401/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved PII S 0 3 7 7 - 8 4 0 1 ( 9 8 ) 0 0 1 8 6 - 2
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2. Materials and methods Cattle feed samples were collected by State or Federal Veterinary Medical Officers and Animal Health Technicians from six dairies and six beef feedlots in Washington, Oregon and Idaho. On each farm, all available commercially prepared cattle feeds were collected on three separate farm visits between July and November 1995. Samples were obtained from either the sites on the farm where cattle feeds were delivered or from the feed storage area. The sampling methods were designed to minimize the potential of obtaining feeds that were contaminated with S. enterica on the farm. Each feed sample (approximately 50 g) was collected using a sterile disposable latex glove and placed into a sterile plastic bag, sealed, and shipped to the laboratory. All samples were stored at room temperature until the initiation of bacterial culturing which usually occurred within 1 week of sample collection. All cattle feed samples were cultured for S. enterica using previously described methods (Gray et al., 1995; Harris et al., 1997). All isolates of S. enterica were serotyped at the National Veterinary Services Laboratories in Ames, IA. Antimicrobial susceptibility testing was performed on selected isolates using the method of Bauer et al., 1966. Genetic subtyping was performed on selected isolates using pulsed field gel electrophoresis (PFGE) of XbaI digested chromosomal DNA as described by Barrett et al. (1994). 3. Results Salmonella enterica bacteria were isolated from 29 (9.8%) of 295 cattle feeds tested. Five serovars were represented (Table 1). Feeds obtained from six of the 12 farms (two feedlots and four dairies) were found to contain S. enterica. Salmonella enterica was found in all major categories of cattle feeds except those designated miscellaneous proteins (n7) and the group of unknown feeds (n6) (Table 2). The serovars Senftenberg, Thompson, Braenderup, and Lille were each found in at least four of the feed categories and collectively accounted for 93% of the isolates found in feeds (Table 2). One feed sample of cracked maize was found to contain the serovar Typhimurium, and another feed was found to contain an isolate belonging to the serogroup C1 that could not be further typed. The Typhimurium isolate had an antimicrobial susceptibility and pulse field gel electrophoresis pattern that were consistent with the epidemic clone that has been designated as definitive type (DT) 104 (Threlfall et al., 1994). Table 1 Salmonella enterica serovars present in 295 feed samples collected from northwestern U.S. cattle operations Number (%) of isolates
Serovar
7 9 7 4 1 1
Senftenberg Thompson Braenderup Lille Typhimurium Group C1 (untypable)
(24.1) (31.0) (24.1) (13.8) (3.5) (3.5)
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Table 2 Salmonella enterica contamination rates by feed category, and serovars isolated Feed category a
No. sampled
No. (%) positive
Dry forages Wet foragesb Dry byproductc Wet byproductd Grainse Oil seedsf
59 55 30 28 55 24
5 6 2 3 4 5
Minerals/add.g Misc. proteinsh Mixed feedsi Unknown
6 7 25 6
3 (50.5) 0 1 (4.0) 0
Total
295
(8.5) (10.9) (6.7) (10.7) (7.3) (20.8)
S enterica serovars Senftenberg, Thompson, Braenderup Senftenberg, Lille, Thompson Braenderup Thompson, Senftenberg, Lille Typhimurium, Braenderup, Thompson Braenderup, Thompson, Senftenberg, serogroup C1 (untypable) Thompson, Lille Braenderup
29 (9.8)
The feed categories consisted of the following: achopped alfalfa, alfalfa hay, chopped grass hay, grass hay; maize or grass silage (DM <70%); crye pellets, oat screenings/pellets; dwet potatoes, sweet maize, cannery waste, whey; erolled cracked maize, rolled barley, ground maize, maize dust; fcannola, cotton seed, cannola or rape seed meal; gShamrock vitamin and mineral, Aureomycin crumbles, Loper mineral; hunspecified protein; i feed bunk mix. b
4. Discussion The present study supports the conclusion that S. enterica bacteria are relatively common contaminants of cattle feeds in the northwestern US. These results are broadly consistent with animal feed surveillance data from Europe (Malmqvist et al., 1995; Veldman et al., 1995), South Africa (Durand et al., 1990), and U.S. feed mills (United State Animal Health Association, 1995) which found contamination rates ranging from 5.2% to 18.8%. The small sample size in the present study precludes making inferences about the relative frequencies of S. enterica in various categories of cattle feeds (Table 2). However, Salmonella were found in a wide spectrum of feeds including grain, wet and dry forages, byproducts, and miscellaneous protein supplements. This is in agreement with a recent study in which Escherichia coli were found in a similarly wide spectrum of cattle feeds (Lynn et al., 1998) indicating that fecal contamination of cattle feeds in the northwestern USA is common. A recent survey of swine feeds in the US found a substantially lower prevalence than the present study (2.8% vs. 9.8%) even though identical bacterial isolation methods were used. This may be a reflection of differences between swine and cattle feeds in the manufacture, handling, storage, and sources of feed materials used. For example, swine feeds are commonly held and transported in enclosed bins while cattle feeds are much more likely to be transported and stored in the open. The finding of Salmonella in 9.8% of feeds delivered to farms indicates that most cattle would be repeatedly exposed to Salmonella in feed during their lifetimes. This is because farm mixed feeds commonly contain several component feeds, and new loads of feeds are frequently received on farms. Most cattle operations reportedly contain animals that are
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seropositive to one or more serogroups of S. enterica (Smith et al., 1994), and the present study suggests that much of this exposure could occur from contaminated feed. Although clinical salmonellosis associated with S. enterica-contaminated feeds has been reported in cattle (Glickman et al., 1981; Anderson et al., 1997; Losinger et al., 1997), the most common serovars found in cattle feeds in the present study, and in animal feeds in other studies (Durand et al., 1990; Malmqvist et al., 1995; Veldman et al., 1995), are not the most common serovars reported from submissions to animal diagnostic laboratories (Ferris and Thomas, 1995). Widespread subclinical infection with S. enterica has been reported in three cattle herds consuming feed contaminated with the serovar Mbandaka,(Jones et al., 1982), and seroconversion in cattle to one or more serogroups appears to be much more widespread than reported clinical disease (Smith et al., 1994). These findings suggest that the S. enterica serovars common to feed may be relatively avirulent to cattle, or occur in feeds at infectious but subclinical doses. Even though Salmonella in feeds may have limited clinical significance for cattle, clinical disease in cattle may not be necessary for feed-borne infections of cattle to play an important role in beef-borne disease of humans (Bauer and Hormansdorfer, 1996) since all of the serovars isolated in this study have been associated with disease in humans (Hargrett-Bean et al., 1987; L'Ecuyer et al., 1996; Centers for Disease Control, 1997). The finding of a cattle feed contaminated with an isolate of Typhimurium fitting criteria consistent with the epidemic clone DT104 is of particular interest. This clone appears to have been disseminated nearly simultaneously in both the UK (Threlfall et al., 1994) and the US (Besser et al., 1997) beginning in the 1980s, becoming the most frequently isolated strain of Typhimurium in cattle, and a frequent cause of salmonellosis in humans. One possible explanation for the rapid expansion of this clone in cattle populations is through contaminated feeds in commerce. 5. Conclusion Commercially produced cattle feeds in the northwestern USA are frequently contaminated with Salmonella enterica. The importance of this in the epidemiology of cattle or human salmonellosis is not clear, however, the current study found one cattle feed that was contaminated with Typhimurium which is known to cause serious disease in both cattle and humans.
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