J APPL POULT RES 2006. 15:475-482
© 2006 Poultry Science Association
National Poultry Extension Workshop |
Microbial Safety of Chickens Raised Without Antibiotics
J. P. Griggs*,
J. B. Bender
and
J. P. Jacob*,1
* Department of Animal Science; and Department of Veterinary Population Medicine, University of Minnesota, 1354 Eckles Ave, St. Paul 55108
1 Corresponding author: jacob150{at}umn.edu
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SUMMARY
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The purpose of the current study was to verify whether there was any validity to the claim that consumers could reduce their exposure to antibiotic-resistant bacteria by purchasing poultry products that were produced without antibiotics. Rinse samples were taken from whole carcasses from chickens grown in small flocks and marketed as antibiotic-free. Salmonella bacteria were isolated from 18.7% of all the carcasses sampled. Campylobacter bacteria were found on 96.0% of the carcasses tested. More than two-thirds (69.4%) of the Salmonella isolates were resistant to at least 1 antibiotic. The antibiotic to which the Salmonella isolates were most commonly resistant was trimethoprim-sulfa, with almost two-thirds (62.9%) of the isolates being resistant to it. Almost three-fourths (73.4%) of the Campylobacter isolates were resistant to at least 1 antibiotic. The most common antibiotic to which Campylobacter isolates were resistant was tetracycline, with almost three-fourths (72.7%) of all Campylobacter isolates being resistant to it.
Key Words: broiler • antibiotic-free • food safety
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DESCRIPTION OF PROBLEM
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In December 2002, a report published jointly by the Sierra Club and the Institute for Agriculture and Trade Policy claimed that consumers could reduce their exposure to antibiotic-resistant microorganisms by purchasing poultry products that were raised without antibiotics [1]. However, they made this claim without collecting samples from poultry that were raised without antibiotics. Their failure to test products from poultry raised without antibiotics seriously weakens their assumption that these products would reduce an individual’s exposure to antibiotic-resistant bacteria. The purpose of the current research was to verify whether there was any validity to the claim made in the Institute for Agriculture and Trade Policy/Sierra Club report [1].
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MATERIALS AND METHODS
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Carcass rinse samples were taken from whole chickens after evisceration, but before entering the chill tank. The carcasses were from chickens grown in small flocks and marketed as antibiotic-free. The majority of the farms, however, were not certified organic. A total of 299 chickens were collected at custom processing plants and represented 20 farms located throughout Minnesota. The samples were obtained by state inspectors (Minnesota Department of Agriculture) and sent to their laboratories in St. Paul for processing. There, the rin-sates were cultured for Salmonella and Campylobacter bacteria. The isolates were then tested for antimicrobial susceptibility, and identified more specifically. The Campylobacter isolates were identified as Campylobacter jejuni or Campylobacter spp., and the Salmonella isolates were identified by serotype (e.g., Salmonella Kentucky).
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RESULTS AND DISCUSSION
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Table 1
shows the results from previously reported studies and the results from this study. The methods used in the other studies varied to some degree. Wallinga et al. [1] used whole refrigerated (not frozen) chicken carcasses that were purchased from supermarkets in or around Des Moines, IA, and Minneapolis, MN. They purchased 200 conventionally raised chickens and tested all of them for Salmonella, and half of them for Campylobacter. Salmonella and Campylobacter were isolated from 17.5 and 95.0% of the birds sampled in the study, respectively. Jorgensen et al. [2] conducted their research in England and purchased 241 whole, raw, chickens during successive winters. Some of these birds were purchased frozen. They used a variety of methods to collect samples to culture for Salmonella and Campylobacter. They isolated Campylobacter from 83% of the chickens sampled. Antibiotic resistance varied by species, with 56% of Campylobacter coli isolates and 1.8% of C. jejuni isolates being resistant to erythromycin.
Wilson [3] purchased 1,127 raw chickens over a 6-yr period. Samples were collected from a portion of the neck skin of each bird, rather than collecting a rinse from the entire carcass. Wilson found that 57% of the sampled chickens carried Campylobacter. Zhao et al. [4] tested 212 chicken carcasses. All were analyzed for Salmonella and 184 for Campylobacter. They obtained these samples over 1 yr from supermarkets in the Washington, DC, metropolitan area. They found Salmonella and Campylobacter on 4.2 and 70.7%, respectively, of the chickens tested.
Harrison et al. [5] tested chicken products from supermarkets and butcher shops that they collected monthly for 7 mo. They tested whole chickens as well as chicken breasts and pieces. One hundred seventy-five samples came from local supermarkets, and 125 came from local butcher shops. They found that 53% of the whole chickens, 33% of the breasts, and 15% of the pieces tested were positive for Salmonella. In addition, 77% of the whole chickens, 72% of the breasts, and 64% of the pieces were positive for Campylobacter. Only the data for the whole chickens are reported in Table 1
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For their study, Willis and Murray [6] obtained 30 chicken carcasses per month for 11 mo from local supermarkets. This group tested 330 raw carcasses, representing 2 different companies, for the presence of Campylobacter and found that 69.4% of the carcasses contained Campylobacter bacteria.
Berndtson et al. [7] conducted their research in Sweden and took swab samples of the neck skin of broilers before and after the carcasses were put through the chiller. They sampled 10 carcasses this way on 5 separate occasions. They detected Campylobacter on all the carcasses before the chill tank, whereas slightly fewer (95%) carcasses were contaminated after the chill tank.
In Northern Ireland, Flynn et al. [8] purchased 153 packages of fresh chicken wings and placed the entire contents of each package in enrichment broth to culture Campylobacter bacteria. They found that 64.7% of the packages contained Campylobacter.
Clearly, direct comparison between the various studies listed in Table 1 is not possible. The origins of the chicken carcasses differ in location, year, and season in which they were obtained. In each study, the cultures were grown at different laboratories using at least slightly different methods. However, Table 1 shows that despite these differences there is some similarity in the data. With the exception of 1 report, Salmonella was isolated from less than one-fourth of the birds tested, and was found in as few as 4.2% of the birds in 1 case [4]. In all 8 studies, Campylobacter was found in greater than half of the chickens tested, and in as many as 100%.
In the current study all producers claimed to be raising chickens without routine antibiotic use. However, in a couple of cases it was difficult to determine if producers had indeed added medication to the feed or water that could be classified as an antibiotic, or if perhaps their rations came with an added antibiotic. Most of this confusion was probably due to producers not knowing precisely what was in the ration or supplements they gave to their chickens. This was relevant in regards to meat and bone meal. In at least one case the producer did not think meat and bone meal was in their ration, but when we examined a label from a bag of feed we saw that their ration did in fact include animal by-products. Some of the confusion about the presence of antibiotics may have been caused by the producers not knowing that certain compounds in their feed were indeed antibiotics. A producer’s inability to recall the exact name of a compound that they gave their chickens could have also caused problems.
Antibiotic-resistant bacteria were isolated from the chicken rinsates collected. Resistance and susceptibility were determined based on the same standards used for the 2000 National Antimicrobial Resistance Monitoring System (NARMS) annual report [9]. Salmonella bacteria were isolated from chicken carcasses from 11 farms. On 6 of these farms, some of the isolates were resistant to at least 1 antibiotic. Campylobacter jejuni and non-jejuni species of Campylobacter were found on chickens from 17 and 13 farms, respectively. Chickens from 12 farms were found to be carrying both classifications of Campylobacter. Only chickens from 1 farm were found to be free of any type of Campylobacter. This farm also did not have any Salmonella. Campylobacter isolates resistant to at least 1 antibiotic were found on 18 farms. On only 1 farm were we unable to isolate any antibiotic-resistant bacteria from the carcass rinse samples.
Tables 2, 3, 4, and 5 summarize the antimicrobial susceptibility results obtained in the study. Sixty-three carcass rinse samples were contaminated with Salmonella (Table 2). Sixty-three Salmonella spp. isolates were tested for susceptibility against 11 antibiotics. Thirty-four (54%) of the isolates were resistant to at least 1 antibiotic. The antibiotics to which the greatest numbers of Salmonella spp. isolates were susceptible were ceftriaxone and ciprofloxacin. Two hundred eighty-seven carcass rinse samples were contaminated with Campylobacter (Tables 3, 4, and 5). A total of 630 Campylobacter isolates were tested for susceptibility to 7 antibiotics; almost three-fourths of the isolates (73.3%) were resistant to at least 1 antibiotic. The antibiotic to which most of the Campylobacter isolates (99.5%) were susceptible was ciprofloxacin.
Table 6 shows how many multiple antibiotic-resistant isolates of each type were identified in this study. The data from this study are presented with the data from NARMS for retail chicken products in Table 7.
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Table 7. National Antimicrobial Resistance Monitoring System (NARMS) data for retail chicken from 1999 for Campylobacter resistance1 compared with our data
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The data in Table 7 are interesting because they show that antimicrobial susceptibility of the isolates from our study did not differ greatly from those found in the NARMS survey [9], except in the case of ciprofloxacin. The Campylobacter isolated from the retail products in the NARMS survey [9] were much more likely to be resistant to ciprofloxacin than the isolates we tested in our study (24 vs. 4.8% for C. jejuni). This suggests that there was a selection pressure that favored the growth of ciprofloxacin-resistant bacteria in the NARMS study that was not present in the chickens from which we collected samples. The rest of the data comparisons in Table 7 show there may be a certain amount of background resistance that would be present in any poultry flock, whether they are raised with or without antibiotics. However, 2 points should be noted here: 1) the chickens in our study were not raised under tight biosecurity so they may have been exposed to antimicrobial resistance present in the environment or on the farm, and 2) we did not monitor closely the presence of antibiotics in feeds or supplements, which may have resulted in the producers unknowingly giving their broilers antibiotics, and possibly promoting the development of antibiotic-resistant bacteria.
The motivation for this study was to find evidence to support the claim of Wallinga et al. [1] that chickens raised without routine antibiotics would be less likely to be contaminated with bacteria that were resistant to antibiotics. Tables 8 and 9 display the results of our study with those of Wallinga et al. [1] for Salmonella spp. and Campylobacter spp., respectively.
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Table 8. Resistance findings for Salmonella spp. from the Institute for Agriculture and Trade Policy/Sierra Club report [1] compared with our data1
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Table 9. Resistance findings for Campylobacter from the Institute for Agriculture and Trade Policy/Sierra Club report [1] compared with our data1
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Unfortunately there were some idiosyncrasies in the sampling methods in our project that made it difficult to analyze the data and draw conclusions from it. First, in some cases multiple flocks from the same farm were sampled, but in others, a single flock was sampled. Sometimes, the multiple flocks were completely separate batches of chickens brought to processing months apart. Sometimes chickens from the same flock on the farm were split up and brought to processing 1 or 2 wk apart, and would thus appear to be 2 separate flocks in the data set. Producers who did this would usually bring the larger birds from the flock in first, and bring the remainder of the flock on a later date.
Another problem with the data is that we did not always test an equal number of isolates from each carcass for antimicrobial susceptibility. In some cases up to 3 isolates from a carcass were tested; in others, no isolates were tested for susceptibility, although they were present. This, and the sampling problems mentioned above, meant that some farms contributed more to the susceptibility data than others. These factors should be considered when examining these data.
To learn about the farms from which we sampled chickens, an on-farm interview was conducted with as many producers as we were able to contact and who were willing to participate. Twelve such on-farm interviews were conducted. The interview consisted of 127 questions that covered a variety of topics related to broiler production. Some of the topics covered were the hatchery from which they got their chicks, the type of feed fed to the broilers, the type of waterers used with their broiler flocks, and incidence of diseases in the flock. Questions pertaining to the type of housing used with the broiler flocks were also asked.
Four common types of housing systems were presented as options in the interview: indoor (no pasture/range access), movable pasture pens, free-range, and day-range. The farms where chickens were raised indoors were not keeping these enclosures sealed tight enough to keep out wild birds, so this housing method should not be considered a more biosecure method of raising broilers. Movable pasture pens are typically enclosed, bottomless pens that are moved daily to give the chickens inside access to new pasture. Free-range housing was defined as a method in which chickens were allowed to range on pasture day and night without any type of confining enclosure except a fence to enclose a generous range area. These chickens will likely have a building or some type of shelter to return to when they desire. Day-range housing is similar to free-range except that the chickens are enclosed in a building in the evening. This method of housing chickens can greatly reduce the loss caused by predation because the chickens are protected from nocturnal predators. The most common housing system found in the 12 farms that were visited was day-range (6), followed by free-range (3), indoors without pasture access (2), and movable pasture pens (1). Some of these producers were using systems that could be described as a hybrid of day-range with the movable pasture pen systems, but herein were categorized as having a day-range system. The producers using these hybrid systems enclosed the chickens in a bottomless enclosure at night, but opened it during the day to allow the chickens to roam. These pens were moved periodically to expose the chickens to new areas of pasture, thus providing them with new areas to forage, and minimizing the build-up of waste in any one area. Two producers interviewed in our study were raising chickens in this way.
During our interviews we encountered only 1 producer raising certified organic broilers. One other producer had recently dropped her certification, but was still feeding certified organic feed to her broilers. Two producers said their feed was made from transitional grains, and 7 others said the majority of the ingredients in their feed were conventionally grown grains. One producer thought he may have been feeding a feed made from transitional grains, but was not certain, so he was not counted with the above 2. None of the producers thought their feeds contained meat and bone meal, but as discussed above, in one case, a producer did not know that his feed contained animal protein products. In hindsight, that question on the survey could have been worded more clearly. Some producers might not have been familiar with the term ‘meat and bone meal’, and it is not as inclusive a term as we perhaps would have liked in that question; better terms would have been ‘animal by-products’ or ‘animal protein’.
The above example illustrates some of the difficulties in designing a comprehensive interview that a variety of people will be able to understand. It was easy for those of us involved in the project to understand the meaning of all the questions in the interview, but that was not necessarily the case for those whom we interviewed. It is likely that if somebody did not know what was meant by a question they simply guessed at an answer. It was also difficult to get concrete answers for some of the questions because of the variability that is inherent in farming. The daily temperature, humidity, precipitation, and farmer’s ambition can affect how frequently pens need to be moved, when litter needs to be changed, or when the birds get started on their next ration, and meant that there was often no simple answer to questions pertaining to topics like these.
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CONCLUSIONS AND APPLICATIONS
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- Research suggests that raising chickens without antibiotics, especially when the birds are kept outdoors, can result in higher levels of Campylobacter and Salmonella contamination than in conventionally raised chickens.
- Removal of antibiotics from chicken feed has not been shown to reduce the incidence of antibiotic resistance. In the samples collected from chickens raised without antibiotics, high levels of multiple antibiotic resistances were noted.
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ACKNOWLEDGMENTS
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The research was supported by the University of Minnesota’s Rapid Agricultural Response fund. Special thanks to the Minnesota Department of Agriculture (MDA) for doing the lab work and for the MDA poultry inspectors for collecting the carcass rinse samples.
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REFERENCES AND NOTES
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- Wallinga, D., N. Bermudez, and E. Hopkins. 2002. Poultry on Antibiotics: Hazards to Human Health. Report by Institute for Agriculture and Trade Policy, and the Sierra Club. Available online at www.sierraclub.org/factoryfarms/antibiotics/antibiotics_report.pdf Accessed June 9, 2005.
- Jorgensen, F., R. Bailey, S. Williams, P. Henderson, D. R. A. Wareing, F. J. Bolton, J. A. Frost, L. Ward, and T. J. Humphrey. 2002. Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. Int. J. Food Microbiol. 76:151–164.[Web of Science][Medline]
- Wilson, I. G. 2002. Salmonella and Campylobacter contamination of raw retail chickens from different producers: A six-year survey. Epidemiol. Infect. 129:635–645.[Medline]
- Zhao, C., B. Ge, J. De Villena, R. Sudler, E. Yeh, S. Zhao, D. G. White, D. Wagner, and J. Meng. 2001. Prevalence of Campylobacter spp., Escherichia coli, and Salmonella serovars in retail chicken, turkey, pork, and beef from the greater Washington, DC, area. Appl. Environ. Microbiol. 67:5431–5436.[Abstract/Free Full Text]
- Harrison, W. A., C. J. Griffith, D. Tennant, and A. C. Peters. 2001. Incidence of Campylobacter and Salmonella isolated from retail chicken and associated packaging in South Wales. Lett. Appl. Microbiol. 33:450–454.[Web of Science][Medline]
- Willis, W. L., and C. Murray. 1997. Campylobacter jejuni seasonal recovery observations of retail market broilers. Poult. Sci. 76:314–317.[Abstract/Free Full Text]
- Berndtson, E., M.-L. Danielsson-Tham, and A. Engvall. 1996. Campylobacter incidence on a chicken farm and the spread of Campylobacter during the slaughter process. Food Microbiol. 32:35–47.[Medline]
- Flynn, O. M. J., I. S. Blair, and D. A. McDowell. 1994. Prevalence of Campylobacter species on fresh retail chicken wings in Northern Ireland. J. Food Prot. 57:334–336.
- NARMS. 2000. National Antimicrobial Resistance Monitoring System: Enteric Bacteria—2000 Annual Report. www.cdc.gov/narms/annual/2000/NARMS_final_report_2000.pdf Accessed June 9, 2005.
- Gupta, A., J. M. Nelson, T. J. Barrett, R. V. Tauxe, S. P. Rossiter, C. R. Friedman, K. W. Joyce, K. E. Smith, T. F. Jones, M. A. Hawkins, B. Shiferaw, J. L. Beebe, D. J. Vugia, T. Rabatsky-Ehr, J. A. Benson, T. P. Root, and F. J. Angulo. 2004. Antibacterial resistance among Campylobacter strains, United States, 1997–2001. Emerg. Infect. Dis. 10:1102–1109.[Web of Science][Medline]
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J. P. Jacob, J. P. Griggs, and J. B. Bender
Characterization of Small-Scale Antibiotic-Free Broiler Production in Minnesota
J. Appl. Poult. Res.,
January 1, 2008;
17(3):
412 - 420.
[Abstract]
[Full Text]
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TOP
SUMMARY
DESCRIPTION OF PROBLEM
