Salmonella Contamination and Antibiotic Resistance on Pastured Poultry and Conventional Poultry Farms

Final Report for OS05-025

Project Type: On-Farm Research
Funds awarded in 2005: $9,542.00
Projected End Date: 12/31/2005
Region: Southern
State: North Carolina
Principal Investigator:
Cedarose Siemon
Independent Research Scientist
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Project Information

Abstract:

Antimicrobials have been used in low-dose amounts throughout the food animal production industry for over thirty years. The World Health Organization has identified several unfavorable consequences to the low-level, long-term exposure to antimicrobials that livestock undergo in commercial production systems (WHO 1997):
• Increased prevalence of antimicrobial resistant bacteria in food animals, which can be transferred to humans through consumption
• Resistance genes of bacteria in food animals can be transferred to human pathogens
• Increased occurrence of infection by resistant pathogens
• Possible loss of antimicrobial effectiveness for both animals and humans
Salmonella is a widespread food-borne pathogen that causes gastrointestinal infection. An estimated 1.4 million people per year in the US are infected with Salmonella (Voetsch et al. 2004). Contaminated poultry is a common source that causes Salmonella infection in humans. On-farm control of Salmonella has been shown to directly decrease the level of contamination of poultry meat at retail (Wegener et al. 2003). Interestingly, Salmonella develop resistance quickly to antimicrobials and are perhaps the most widely studied bacteria for its severity in multi-drug resistance development.
Pasture poultry farms are a new way of raising poultry intensively on the pasture and doesn’t employ the use of antimicrobials. Being a new form of raising poultry without antimicrobials, pasture poultry farms are of importance in the effort to raise poultry without increasing the antimicrobial resistant bacteria population. However, one main reason antimicrobials are used in commercial poultry farming is to control the on-farm levels of Salmonella prevalence, therefore, we must study Salmonella prevalence on pasture poultry farms to know if poultry can be raised without antimicrobials and not have significantly higher levels of Salmonella prevalence.

There are two objectives to this study:
1. To see if Salmonella prevalence is significantly different on pasture poultry farms than on commercial poultry farms.
2. To see if antimicrobial resistance is different between the pasture and commercial poultry farms.
This study was conducted in Wisconsin in 2004 and in North Carolina in 2005, a total of 17 pasture and 14 commercial farms were studied. From each farm thirty fecal samples were collected and analyzed for Salmonella contamination and antimicrobial resistance.
Commercial and pasture poultry farms were found to not be significantly different in Salmonella contamination (p-value 0.4928). Samples collected from commercial farms were found to be 2.6 times more likely to be contaminated with Salmonella (<0.0001). In NC, significantly more Salmonella isolates from commercial farms were resistant to: amoxicillin/clavulanic acid (<0.005), ampicillin (<0.005), chloramphenicol (<0.005), streptomycin (<0.005), sulfisoxazole (<0.005), and tetracycline (<0.005). In NC, significantly more Salmonella isolates from pasture farms were resistant to (Graph 1.): ceftriaxone (<0.05) and cephalothin (<0.005). Multi-drug resistance (resistance to ?5 antimicrobials) within the Salmonella isolates was found to be 85 times more likely in commercial poultry farms than in pasture poultry farms (<0.0001).
Pasture poultry farms didn’t use antimicrobials and wasn’t found to have a higher prevalence of Salmonella than the commercial farms. Multidrug resistance was only in NC and was in commercial farms exclusively. North Carolina had a great majority of the antimicrobial resistance. Why might pasture farms have any resistance? Resistant Salmonella could be transported onto the farm from the hatchery or the feed mill. Feed mills mill feed with low-dose antimicrobials in it for other farmers, feed mills could be an environment for antimicrobial resistant Salmonella to develop. Pasture poultry farming may be the way in which poultry can be raised without the use of antimicrobials and without the risk of higher Salmonella prevalence. However, more research is required to further verify these findings.

Bibliography:

World Health Organization-Emerging and other Communicable Diseases, Surveillance and Control. 1997. The Medical Impact of Antimicrobial Use in Food Animals. Berlin, Germany. 1-6

Voetsch A.C., Van Gilder T.J., Angulo F.J. et al. 2004. Emerging Infections Program FoodNet Working Group. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clinical Infectious Diseases 2004; 38 (Suppliment 3):S127-S134

Wegener C., Hald T., Wong D., Madsen M., Korsgaard H., Bager F., Gerner-Smidt P. and Molbak K. 2003. Salmonella Control Programs in Denmark. Emerging Infectious Diseases. 9: 774-779

Tables, figures or graphs mentioned in this report are on file in the Southern SARE office.

Contact Sue Blum at 770-229-3350 or
sueblum@southernsare.org for a hard copy.

Introduction

The World Health Organization has identified several unfavorable consequences to the low-level, long-term exposure to antimicrobials that livestock undergo in commercial production systems (WHO 1997): Increased prevalence of antimicrobial resistant bacteria in food animals, which can be transferred to humans through consumption; resistance genes of bacteria in food animals can be transferred to human pathogens; increased occurrence of infection by resistant pathogens; possible loss of antimicrobial effectiveness for both animals and humans. Commercial broiler farms typically implement low-dose feed-grade antimicrobials and have since the 1970’s.
An estimate of 1.4 million cases of illness, 15,000 hospitalizations, and 400 deaths in the U.S. per year are due to Salmonella infection (Voetsch et al. 2004). There are several reasons why Salmonella prevalence ought to be studied on poultry farms. Firstly, Salmonella are widespread food-borne pathogens. Secondly, Salmonella develop resistance quickly and have been found to be resistant to a wide variety of antimicrobials. Thirdly, Salmonella is common in poultry and is spread to humans by contaminated meat. In Denmark, a multi-year, nationwide study showed that the level of Salmonella contamination on the farm affects the level at retail (Wegener et al. 2003). If the prevalence of Salmonella on the farm is high then the prevalence at retail may be high, therefore it is important to measure Salmonella prevalence at the farm level. Measuring Salmonella after slaughter does not directly show the prevalence of Salmonella for a particular farming system because the carcass may have become contaminated with Salmonella from the slaughter facilities.
Generally, and for this study, no antimicrobials are used on the pasture poultry farms. On pasture poultry farms the broilers are raised in brooder houses until 3 weeks of age, then moved into small (around 10’x12’) pens on pasture. The pens have a roof (often a piece of tin), open air wiring for walls, and no flooring, giving the broilers direct access to the pasture. The pens are moved a minimum of once a day to a new area of pasture, which usually hadn’t had broilers on it in over a year. Pens have from 25 to 100 broilers inside and the broilers are slaughtered from 55-100 days old. On conventional farms the broilers are raised indoors in a large house for their entire life, an all-in-all-out system. Each batch of broilers enter the barn within a week of the last flock, often after the bedding on the floor has been mixed. Houses have from 15,000-75,000 broilers inside and the broilers are slaughtered from 40-55 days old. Feed grade antimicrobials were routinely used on the conventional farms.
Pasture poultry farms have not been thoroughly tested for Salmonella prevalence. Processed chickens from free-range poultry have been tested for Salmonella prevalence (Bailey and Cosby 2005). However, it is difficult to say if Salmonella prevalence is a direct result of how the broilers are reared without testing Salmonella prevalence on the farm.

Bibliography:

World Health Organization-Emerging and other Communicable Diseases, Surveillance and Control. 1997. The Medical Impact of Antimicrobial Use in Food Animals. Berlin, Germany. 1-6

Voetsch A.C., Van Gilder T.J., Angulo F.J. et al. 2004. Emerging Infections Program FoodNet Working Group. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clinical Infectious Diseases 2004; 38 (Suppliment 3):S127-S134

Wegener C., Hald T., Wong D., Madsen M., Korsgaard H., Bager F., Gerner-Smidt P. and Molbak K. 2003. Salmonella Control Programs in Denmark. Emerging Infectious Diseases. 9: 774-779

Bailey, J.S. and Cosby D.E. 2005. Research note: Salmonella Prevalence in Free-Range and Certified Organic Chickens. Journal of Food Protection. 68: 2451-2453

Project Objectives:

To compare pasture and commercial poultry farms in terms of:
-Farm and sample level Salmonella prevalence
-Antimicrobial resistance within the Salmonella found

Research

Materials and methods:

Farm Description:
On pasture poultry farms the birds were raised in brooder houses until 3 weeks of age, then moved into small (around 10’x12’) pens on pasture. The pens had a roof (often a piece of tin), open air wiring for walls, and no flooring, giving the birds direct access to the pasture. The pens were moved a minimum of once a day to a new area of pasture, which usually hadn’t had birds on it in over a year. Pens had from 25 to 100 birds inside and the birds were slaughtered from 55-100 days old. No antimicrobials were used on the pasture poultry farms. On conventional farms the birds were raised indoors in a large house for their entire life, an all-in-all-out system. Each batch of birds entered the barn within a week of the last flock, often after the bedding on the floor had been mixed. Houses had from 15,000-75,000 birds inside and the birds were slaughtered from 40-55 days old. Feed grade antimicrobials were routinely used on the conventional farms.

Sampling method:
During the summer of 2004 eight pasture and nine conventional broiler poultry farms were sampled in Wisconsin for the prevalence of Salmonella. During the summer of 2005 ten pasture and five conventional broiler poultry farms were sampled in North Carolina (three farms from Virginia and one from South Carolina, for simplicity reference to North Carolina is used for all south east states) for the prevalence of Salmonella. From each farm 30 (~5 gram) fecal specimens were collected from pasture poultry and conventional poultry farms in Wisconsin and North Carolina. The specimens were collected with plastic gloves and sealed in a sterile Whirl Pak© bag (Wisconsin) or collection cup (North Carolina). The specimens were put in coolers on ice and processed in the lab within eight hours of collection. Appropriate dress in a sterile suit, plastic shoe coverers, and lab-grade plastic gloves was used upon entry to the farm. When sampling a pasture poultry farm the thirty specimens collected were evenly distributed throughout the different pens. When sampling a conventional poultry house in North Carolina specimens were collected in a zig-zag pattern going from one end of the barn to another, sampling evenly throughout the house. In Wisconsin specimens from conventional poultry houses were collected throughout the middle third of the barn, the sampling method became more developed in North Carolina.

Salmonella isolation:
The Salmonella isolation laboratory method was based on the USDA Microbiology Laboratory Guidebook (USDA 2002) method for the Isolation and Identification of Salmonella from Meat, Poultry, and Egg Products. As well as, methods developed by DVM NCSU laboratory of Wondwossen Gebreyes. Using sterile methods the fecal specimens were weighed to five grams +/- one gram. Each specimen was added to tetrathionate broth to make a 1:10 mixture. Each bag or collection cup was shaken vigorously to ensure a well-mixed solution. At early to mid- and late to mid-points in processing the thirty specimens a negative control (sterile tetrathionate broth) and a positive control (a hydrogen sulfide producing Salmonella positive colony-from the laboratory of Peter Bahnson DVM UW 2004) were incorporated. One to three controls and positive controls were incorporated in each farm’s thirty specimens. The 1:10 fecal to tetrathionate broth mixes were incubated at 37°C for 24 hours.
One hundred microlitres of the suspension from the 1:10 fecal: tetrathionate broth were transferred using sterile pipette tips to a test tube containing 9.90 ml of Rappaport Vassilliadis R10 media and incubated at 42°C for 24 hours. Specimens were then streaked onto XLT4 selective plates. The XLT4 plates were then incubated at 37°C for 24 hours. After incubation the plates were allowed to sit at room temperature for 24 hours. Up to three colonies from every plate were tested for the appropriate biochemical reactions on triple iron sugar and urea slants, to confirm that the colony was Salmonella. The slants were incubated at 37°C for 24-48 hours. A portion of the growth from the TSI slants was transferred and streaked onto Luria Bertani agar slants and incubated at 37°C for 24 hours. These tubes were then stored at room temperature until used for antimicrobial susceptibility testing.

Antimicrobial susceptibility test:
The antimicrobials that were tested for are a modified National Antimicrobial Resistance Monitoring System list of antimicrobials that are important to veterinary and human use, as well as, important for antimicrobial resistance within Salmonella, antimicrobials used by the conventional farms tested in this study: ampicillin (Am), chloramphenicol (C), streptomycin (S), sulfasoxazole (Su), tetracycline (Te), amoxicillin/clavulanic acid (Ax), cephalothin (CF), ceftriaxone (CRO), ciprofloxacin (CIP), kanamycin (K), amikacin (AN), gentamicin (GM). Kirby-Bauer disc diffusion method on Mueller-Hinton agar plates using standard techniques (NCCLS 2002) was used for the testing of antimicrobial resistance in the Salmonella isolates.

Bibliography:

National Committee for Clinical Laboratory Standards. (2002). Performance Standards for Antimicrobial Disc and Dilution Susceptibility Tests for Bacteria Isolated from Animals-Second Edition:Approved Standard M31-A2. NCCLS, Villanova PA, USA

Research results and discussion:

Results

In this study, we compared the prevalence of Salmonella in broiler farms that were raised in conventional and pasture settings. We also compared antimicrobial resistance of the isolates detected in the two production systems. This study was conducted in a total of 31 farms in two states, Wisconsin (nine conventional and nine pasture) and North Carolina (five conventional and ten pasture).
On pasture poultry farms the birds were raised in brooder houses until 3 weeks of age, then moved into small (around 10’x12’) pens on pasture. The pens had a roof (often a piece of tin), open air wiring for walls, and no flooring, giving the birds direct access to the pasture. The pens were moved a minimum of once a day to a new area of pasture, which usually hadn’t had birds on it in over a year. Pens had from 25 to 100 birds inside and the birds were slaughtered from 55-100 days old. No antimicrobials were used on the pasture poultry farms. On conventional farms the birds were raised indoors in a large house for their entire life, an all-in-all-out system. Each batch of birds entered the barn within a week of the last flock, often after the bedding on the floor had been mixed. Houses had from 15,000-75,000 birds inside and the birds were slaughtered from 40-55 days old. Feed grade antimicrobials were routinely used on the conventional farms.
At the farm level, in Wisconsin 25% pasture and 44% conventional poultry farms were found to have Salmonella (each farm with at least one positive specimen). The difference was not statistically significant (p=0.6199) as shown in Table 1. In North Carolina, there was also no significant difference in Salmonella prevalence, 40% pasture and 40% conventional poultry farms were positive for Salmonella (p=1.0). Overall, no significant difference in Salmonella prevalence was found, 33% pasture and 47% conventional poultry farms (p= 0.4928).
On an individual specimen level, conventional farms were found to have a significantly higher percentage of positive specimens than pasture (p<0.0001). In Wisconsin, 18% of all specimens from pasture and 34% of all specimens from conventional poultry farms were found to have Salmonella (p-value <0.0001). In North Carolina 14% of all specimens from pasture and 23% of all specimens from conventional poultry farms were found to have Salmonella, resulting in a p-value of 0.0287. Overall, 16% of all specimens collected from pasture and 30% of all specimens collected from conventional poultry farms were Salmonella positive (p<0.0001) as shown on Table 1.
Antimicrobial resistance was found to 10 out of 12 antimicrobials tested. Among flocks sampled in North Carolina, 51% of the isolates were resistant to one or more of the 12 antimicrobials tested. The frequency of resistance, in North Carolina, to various classes of antimicrobials to which resistance was commonly detected include: ampicillin (48%), amoxicillin/clavulanic acid (46%), streptomycin (36%), sulfasoxazole (32%), tetracycline (32%), chloramphenicol (31%), and cephalothin (18%).
In general, Salmonella isolates showed antimicrobial resistance in a relatively lower frequency in Wisconsin than those isolated in North Carolina. Of all the isolates found to have resistance, 80% of them were from North Carolina. In Wisconsin on one pasture farm 90% of the isolates were resistant to streptomycin and tetracycline and one isolate was resistant ampicillin, amoxicillin, and ceftriaxone. Two more isolates from Wisconsin were found to be streptomycin resistant, each from different farming types (conventional and pasture).
Of all the pasture isolates tested for antimicrobial resistance 5% were resistant to ceftriaxone, a third generation cephalosporin. From one farm were isolated seven of the eight isolates with ceftriaxone resistance found, even though there was no report of antimicrobial use in the pasture farms. The predominant resistance pattern was ampicillin, amoxicillin/clauvanic acid, cephalothin, ceftriaxone; AmAxCFCRO (5% of all North Carolina pasture isolates). Two more isolates from pasture poultry farms showed resistance to ceftriaxone, one isolate from Wisconsin.
Multi-drug resistance (resistance to three or more classes of antimicrobials) was found in 69% of the isolates from conventional farms and 11% on pasture farms in North Carolina (Table 3.). Multi-drug resistance was found to be significantly higher in isolates from conventional than pasture poultry farms in North Carolina (p<0.0001). No multi-drug resistance was found in Wisconsin.
There were three predominant resistance patterns found in this study. In North Carolina 22% of the isolates from pasture poultry farms had a resistance pattern of AmAxCF. In Wisconsin 56% of the isolates from pasture poultry farms had a resistance pattern of STe. In North Carolina 62% of the isolates from conventional farms had a resistance pattern of AmCSGTeAx (Table 2.).

Discussion

In this study, we investigated Salmonella prevalence and compared antimicrobial resistance frequency between isolates from conventional and pasture-reared poultry. Salmonella prevalence wasn’t different between the two farming systems. A study conducted in the U.S. on Salmonella prevalence in free-range chicken carcasses found 31% (42/135) of the carcasses to have Salmonella and stated that free-range chickens are no less likely to have Salmonella (Bailey and Cosby 2005). In a study looking at Salmonella prevalence in hogs living on pasture and hogs living indoors no difference in Salmonella contamination was found (Callaway et al. 2005). In Broiler production it has been found that if the hatcheries are contaminated then the flock is likely to be contaminated (Bailey et al. 1998, Cox et al. 1990). Hatcheries affect Salmonella prevalence independent of various conventional practices and maybe even the pasture system.
There are many factors that may influence Salmonella contamination on either farming system, which may only apply to one farming system. Conventional broilers are raised indoors and pasture broilers are raised outdoors. Horizontal transfer of Salmonella from surfaces surrounding where the flock is being raised can be a significant influence on the contamination of a flock, even with uninfected hatcheries (Heyndrickx et al. 2002). In one study, Salmonella serotypes from the poultry house impacted the contamination of the broiler at slaughter more than the serotypes from the hatchery (Lahellec and Colin 1985). Conventional poultry are raised indoors and between flocks conventional producers in this study used the same cleaning procedure of turning the old litter within the house. By not removing the old litter between flocks horizontal transfer is very likely. In pasture poultry systems the broilers are in open-air frames, which are moved to new pasture daily, therefore, decreasing the likelihood of horizontal transfer.
Previously, it has also been shown that there are many risk factors associated with Salmonella contamination at the end of rearing in conventional poultry: Salmonella-positive delivered day-old chicks, feed trucks that parked in front of the change room to deliver the feed, if antimicrobial treatment occurred after a disease, and the duration between cleansing and longer disinfection period (Rose et al. 2003). Many of these factors may not apply to pasture poultry farms, more research is needed to evaluate which procedures could be important risk factors for contamination on pasture poultry farms. Most of the pastures that the flocks were reared on hadn’t had a production flock on them in a year or more. Salmonella has been found to survive on pasture in contaminated manure for a maximum of 64-77 days (Hutchison et al. 2005, Platz 1981). Consistent isolation of Salmonella was found to last only until ~28 days (Platz 1981). These findings support that Salmonella shed by pasture flocks may not be on the pasture after a year when the next flock comes through. Some farms did have cattle grazing on the farm, which could be a potential risk factor for the introduction of Salmonella into those flocks.
Both farming systems may have characteristics that may limit Salmonella prevalence. On conventional farms various classes of antimicrobials are used for therapeutic and production purposes. On pasture poultry farms, the broilers are moved frequently, leaving contaminated feces behind, perhaps lowering cross-contamination rates. Also, no antimicrobials or vaccines are used. Pasture farmers reported a low incidence of sick broilers. However, if a broiler is detected as sick it is moved to a pen that is separated from the flock and is treated using alternative medicine, such as: probiotics, yogurt, soluble vitamins, garlic, comfrey, chickweed, apple vinegar, etc… Understanding why the two farming systems didn’t have different Salmonella prevalence requires a detailed multivariate epidemiological study on ecological factors, and it is beyond the scope of this study.
We found that on conventional farms if Salmonella was found it was widespread throughout the specimens collected. In contrast, on pasture farms, if Salmonella was found it was less widespread in the specimens (Table 1.). The percentage of specimens from the conventional farms with Salmonella was 29.8%. The percentage of specimens form the pasture farms with Salmonella was 16.2%. Previously, a study was conducted in four states for the duration of a year examining the sources and movement of Salmonella; the mean for on-farm specimen contamination was 9.8% (Bailey et al. 2001). Salmonella may be so widespread in conventional flocks as a result of the short amount of time from one flock to the next in a house and because the houses have the old litter turned but not removed and the house not disinfected, strengthening the likelihood of horizontal contamination (Heyndrickx et al. 2002). Testing levels of Salmonella prevalence in the flocks right before slaughter, we were able to estimate the likelihood of contamination potentially going into the processing facilities. If the amount going into the facilities is very low or none, then a noteworthy decrease in contaminated poultry leaving the slaughter plant may be accomplished (Bailey 1993). Slightly more specimens per farm were found to be positive in Wisconsin than in North Carolina. We speculate that this is because the study was conducted in North Carolina during the peak of a summer drought that met temperatures of 105°F, which can be detrimental to the survival of Salmonella on pasture (Hutchison et al. 2005, Platz 1981). In Wisconsin and North Carolina the same percentage of conventional farms were found to have Salmonella. In North Carolina the percentage of pasture farms with Salmonella was almost twice that of the percentage of pasture farms with Salmonella in Wisconsin.
A higher frequency of antimicrobial resistance was found in North Carolina. This may be a result of the state being one of the major poultry producing states for several decades. It may thus be presumed that various classes of antimicrobials were used in houses sampled in this study, as well as, at feed-mills where feed was milled for either conventional or pasture poultry farm in this study. A previous study on antimicrobial resistance in Salmonella isolated from swine farms in North Carolina found 86% of 1314 isolates were resistant to one or more antimicrobials (Gebreyes et al. 2004), in this study on poultry in North Carolina we found 51% of 214 isolates were resistant to one or more antimicrobials.
In Wisconsin no antimicrobial resistance was found except on a pasture farm where antimicrobials weren’t reportedly used. In Wisconsin the poultry industry in the areas sampled was established more recently and nearly all the houses tested were just built that year, which may be why Salmonella from those houses hadn’t developed antimicrobial resistance. Whereas, the houses sampled in North Carolina were old poultry houses, having had both turkeys and chickens, some houses were over 15 years old. The long-term use of the houses to rear poultry with the regular use of feed grade antimicrobials may allow for the development of resistance to many antimicrobials and multi-drug resistance. Many of the houses in North Carolina were unused for two or more years due to less demand for turkeys before broilers were introduced.
Antimicrobial resistance is currently one of the major public health issue throughout the world. Recently, the food industry has begun to require the conventional poultry producers to use less antimicrobials, all as a result of consumer concern about antimicrobial resistance. Often, it is difficult to accurately document the amount of antimicrobials used in the food animal industry. The Union of Concerned Scientists calculated that 28 million pounds (93% of antimicrobials used on animals) are used for production purposes (Mellon et al. 2001). The Animal Health Institute, estimated that 23 million pounds of antimicrobials were sold for use in food and companion animals in the U.S. per year for 1999-2001 (AHI 2001). Infections occur in a larger number of cases when caused by Salmonella that has previously been exposed to an antimicrobial than Salmonella hasn’t been exposed to antimicrobials (Cohen and Tauxe 1986). Heightened antimicrobial resistance in Salmonella may bring failure in treatment if the Salmonella are resistant to the antimicrobials used (Anderson et al. 2003). Mitigation efforts on antimicrobial use in food animal and human medicine systems should be made by the farming, veterinary, medical and public health communities (Anderson et al. 2003, WHO 1997).
Overall, a higher frequency of resistance was seen in conventional farms. Conventional farms employ the regular use of feed grade antimicrobials, while pasture farms didn’t use any antimicrobials. Resistance seen in the conventional farms was to antimicrobials that Salmonella is commonly found to be resistant to in livestock settings, where antimicrobials are used (NARMS-EB 2000).
Salmonella isolates from pasture farms were found to be resistant to the common antimicrobials and ceftriaxone (figure 1.). Ceftriaxone is a front line therapeutic remedy for Salmonellosis (Cherubin et al. 1986) and resistant Salmonella was only recently found in chicken, 1% of 1,121 isolates (Gray et al. 2004). In this study 5% of the isolates from pasture poultry farms were resistant to ceftriaxone. Perhaps on pasture poultry farms the high level of farmer interaction affects the level of ceftriaxone resistant Salmonella. Humans in North Carolina were found to be a source of ceftriaxone resistant Salmonella (25). Resistance to ceftriaxone may also be a result of cattle being grazed on the same farm or a selective force different than antimicrobials. Previously, cattle were reported to act as a main reservoir for the Salmonella serovar Newport-MDRAmpC, which also carried ceftriaxone resistance (Gupta et al. 2003). The one pasture poultry farm where seven isolates were found with ceftriaxone resistance had cattle grazing on the same pasture near the flock. Antimicrobials hadn’t been used on the farm or by the farmer in thirteen years; therefore the ceftriaxone resistant Salmonella may have originated from sources other than the farm.
In this study multi-drug resistance is defined as resistance to three or more classes of antimicrobials. Multi-drug resistance was found almost only in conventional farms in North Carolina, which may be a result of the state being one of the major poultry producing states for several decades. During those decades it may be presumed that many classes of antimicrobials were used in the houses sampled in this study. Multi-drug resistance in Salmonella adds to the human health problem of Salmonella infection. Multi-drug resistance in Salmonella renders antimicrobial treatment ineffective, including third generation cephalosporins, like ceftriaxone (Rossiter et al. 2002). Multi-drug resistant Salmonella Typhimurium infections were found to exhibit a higher mortality than non multi-drug resistant S. Typhimurium infections (Helms et al. 2002). The National Antimicrobial Resistance Monitoring System reported 1.4-7.0% of Salmonella isolates that are resistant to 7-5 antimicrobials (NARMS-EB 2000) in this study 69% of conventional isolates in North Carolina were resistant to 7-5 antimicrobials and 3% of pasture isolates were resistant to 5 antimicrobials in North Carolina. In truth, very little can be concluded about the cause of more or less antimicrobial resistance because it is a multivariate issue.

Bibliography:

Bailey, J.S. and Cosby D.E. 2005. Research note: Salmonella Prevalence in Free-Range and Certified Organic Chickens. Journal of Food Protection. 68: 2451-2453

Callaway T.R., Morrow J.L., Johnson A.K., Dailey J.W., Wallace F.M., Wagstrom E.A., McGlone J.J., Lewis A.R., Dowd S.E., Poole T.L., Edrington T.S., Anderson R.C., Genovese K.J., Byrd J.A., Harvey R.B., Nisbet D.J. 2005. Environmental prevalence and persistence of Salmonella spp. In outdoor swine wallows. Foodborne Pathogenic Diseases 2(3): 263-273

Bailey J.S., Cason J.A., Cox N.A. 1998. Environment and Health: Effect of Salmonella in young chicks on competitive exclusion treatment. Poultry Science 77: 394-399

Cox N.A., Bailey J.S., Mauldin J.M., Blankenship L.C. 1990. Presence and impact of Salmonella contamination in commercial broiler hatcheries. Poultry Science. 69(9): 1606-1609

Heyndrickx M., Vandekerchove D., Herman L., Rollier I., Grijspeerdt, De Zutter L. 2002. Printed in the United Kingdom routes for Salmonella contamination of poultry meat: epidemiological study from hatchery to slaughterhouse. Epidemiological Infections. 129: 253-265

Lahellec, C., Colin P. 1985. Relationship between serotypes of Salmonella from hatcheries and rearing farms and those from processed poultry carcasses. British Poultry Science. 26:179-186

Rose N., Mariani J.P., Drouin P., Toux J.Y., Rose V., Colin P. 2003. A decision-support system for Salmonella in broiler-chicken flocks. Preventive Veterinary Medicine. 59: 27-42

Platz S. 1981. Studies on survival of Salmonella on agricultural areas. Zentralbl Bacteriol Mikrobiol Hygeine. 173 (6): 452-456

Hutchison M.L., Walters L.D., Moore T., Thomas D.J.I., Avery S.M. 2005. Fate of pathogens present in livestock wastes spread onto fescue plots. Applied and Environmental Microbiology. 71: 691-696

Bailey J.S., Stern N.J., Fedorka-Cray P., Craven S.E., Cox N.A., Cosby D.E., Ladely S., Musgrove M.T. 2001. Sources and movement of Salmonella through integrated poultry operations: a multistate epidemiological investigation. Journal of Food Protection. 64:1690-1697

Bailey J.S. 1993. Control of Salmonella and Campylobacter in poultry production. A summary of work at Russell Research Center. Poultry Science. 72(6): 1169-1173

Gebreyes W.A., Thakur S., Davies P.R., Funk J.A., Altier C. 2004. Trends in antimicrobial resistance, phage types and integrons among Salmonella serotypes from pigs, 1997-2000. Journal of Antimicrobial Chemotherapy. 53:997-1003

Mellon, M., Benbrook, C., Benbrook, K., 2001. Hogging It: estimates of antimicrobial abuse in livestock. Cambridge: Union of Concerned Scientists Publications.

AHI (Animal Health Institute). 2002. “Survey shows decline in antibiotic use in animals” Press release accessed September 29th. 2002
http://www.ahi.org/mediaCenter/pressReleases/surveyShowsDecline.asp

Cohen M.L., Tauxe R.V. 1986. Drug-resistant Salmonella in the United States: an epidemiological perspective. Science 234 (4779): p. 964-969

Anderson A.D., Nelson J.M., Rossiter S., Angulo F.J. 2003. Public health consequences of use of antimicrobial agents in food animals in the United States. Microbial Drug Resistance. 9 (4): 373-379

World Health Organization-Emerging and other Communicable Diseases, Surveillance and Control. 1997. The Medical Impact of Antimicrobial Use in Food Animals. Berlin, Germany. 1-6

National Antimicrobial Resistance-Enteric Bacteria (NARMS-EB). 2000. Veterinary isolates final report. FDA/USDA/CDC. http://www.ars-grin.gov/ars/SoAtlantic/Athens/arru/narms_2000/narms_toc00.html

Cherubin C.E., Eng R.H.K., Smith S.M., Goldstein E.J. 1986. Cephalosporin therapy for Salmonellosis: questions of efficacy and cross resistance with ampicillin. Archives of Internal Medicine. 46: 2149-2152

Gray J.T., Hungerford L.L., Fedorka-Cray P.J., Headrick M.L. 2004. Extended-spectrum-cephalosporin resistance in Salmonella enterica isolates of animal origin. Antimicrobial Agents and Chemotherapy. 48 (8): 3179-3181

Gupta A., Fontana J., Crowe C., Bolstorff B., Stout A., Van Duyne S., Hoekstra M.P., Whichard J.M., Barrett T.J., Angulo F.J. 2003. Emergence of multidrug-resistant Salmonella enterica serotype newport infections resistant to expanded-spectrum cephalosporins in the United States. Journal of Infectious Diseases. 88: 1707-1716

Rossiter S., Joyce K., Stevenso J., Barrett T., Anderson A. and NARMS Working Group. 2002. Multidrug-Resistance among Human Non-Typhoidal Salmonella Isolates in the United States: NARMS 1999-2000. www.cdc.gov/narms/publications/2002/Rossiter_2002.pdf

Helms M., Vastrup P., Gerner-Smidt P., Molbak K. 2002. Excess mortality associated with antimicrobial drug-resistant Salmonella typhimurium. Emerging Infectious Diseases. 8 (5): 490-495

Participation Summary

Educational & Outreach Activities

Participation Summary:

Education/outreach description:
Outreach

Poster presentation at the Carolina Sustainable Farmer’s Association Conference in Duram, NC on Nov. 4-5 2005

Poster presentation at the Small Family Farm Conference at the University of Virginia on Nov. 9 2005

In process still:

Scientific publication of research in the peer-reviewed journal Avian Diseases.

Publications in ATTRA and the APPPA website or newsletter

Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.