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PROCESSING, PRODUCTS, AND FOOD SAFETY |
Institute of Agricultural and Environmental Research, Tennessee State University, Nashville 37209-1561
1 Corresponding author: snahashon{at}tnstate.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: chicken • guinea fowl • antimicrobial resistance
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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There is growing scientific evidence that the use of antibiotics in food animals leads to the development of resistant pathogenic bacteria that can reach humans through the food chain (Van Looveren et al., 2001). Recent reports have shown that different types of food and environmental sources harbor bacteria that are resistant to one or more antimicrobial drugs used in human or veterinary medicine and in food-producing animals (Anderson et al., 2003; Schroeder et al., 2004).
Annual cost of treating infections caused by antibiotic-resistant bacteria is estimated to be $4 to $5 billion (McGowan, 2001). International and US public health agencies have targeted antibiotic resistance as an emerging public health concern (Barza and Travers, 2002) and one of the most pressing public health needs. Contaminated food of animal origin is one source of human bacterial infections; therefore, the presence of antibiotic-resistant strains in food animals such as poultry has raised concerns that the treatment of human infections will be compromised.
Antimicrobials Used in Poultry Management
Antibiotics are used for control and treatment of bacterial diseases in poultry. Common antibiotics are bacitracin, chlortetracycline, erythromycin, and penicillin. The fluoroquinolones are important members of the quinolone group of antibiotics licensed to treat diseases in humans and animals, and their use in livestock animals can contribute to increased resistance in foodborne bacteria (such as Campylobacter and Salmonella), which may infect humans. The fluoroquinolones are important for the treatment of invasive Salmonella and Campylobacter infections in humans, and an increase in the resistance in these bacteria is therefore of concern. In addition, when antibiotics are administered to birds over a long period, particularly at a low level, certain species of bacteria become resistant, and finally the resistance renders the antibiotic ineffective.
Antimicrobial Resistance in Chickens
Billions of chickens and millions of specialty poultry products enter the US market annually (McCrea et al., 2005). Consequently, poultry have been implicated as an important source of human infections (Stern and Robach, 2003). Although many of these pathogenic bacteria recovered from poultry have been monitored, several published studies have reported on antimicrobial resistance in pathogenic bacteria found in poultry, particularly Salmonella and Escherichia coli (Chung et al., 2004).
In the modern poultry industry, antibiotics are used for the treatment and prevention of infectious diseases in farm animals intended for food production and to protect public health from foodborne diseases. Mishandling of raw poultry and consumption of undercooked poultry are potential contamination sources of Campylobacter (Nadeau et al., 2002) and Salmonella. It is well documented that Campylobacter and Salmonella infections in humans have been associated with raw chicken (Harrison et al., 2001; Hernandez et al., 2005). Birds appear to be an important reservoir for Campylobacter lari, which has been isolated from gulls (Glunder and Petermann, 1989) and chickens (Tresierra-Ayala et al., 1995; Shih, 2000). Fresh chicken carcasses have been indicated to contain high numbers (approximately 105 cfu/g) of Campylobacter spp. (Cogan et al., 1999). Salmonella and Campylobacter have also been isolated in chicken feed and water (Padungtod and Kaneene, 2005).
Antimicrobial Resistance in Guinea Fowl
Guinea fowl does not comprise a large portion of the poultry meat market in the United States; however, it is sold year round in supermarkets and served as a special delicacy in some restaurants and hotels in large cities within the United States, Canada, Europe, Africa, and many other parts of the world. Although efforts to establish industrial production of guinea fowl in the United States are under way (Phillips and Ayensu, 1991), guinea fowl production is a viable enterprise in European markets. Recent reports indicate that guinea fowl are also raised commercially on farms in Canada (Nova Scotia Department of Agriculture, 1997) and Australia (Embury, 1998). In a commercial setting, guinea fowl are kept in confinement using methods similar to those for raising chickens (Phillips and Ayensu, 1991). These conditions predispose guinea fowl to microbial infection although previous reports have shown that they adapt well to harsh environmental conditions and are less susceptible to poultry diseases (Mathis and McDougald, 1987). However, there is a paucity of information pertaining to antimicrobial resistance in guinea fowl.
It has been observed that antibiotic usage over a long period can induce antibiotic resistance in bacteria (Gautier-Bouchardon et al., 2002). Although many pathogenic bacteria recovered from poultry have been monitored, few published studies have reported on antimicrobial resistance in poultry. Therefore, the objectives of this study were to 1) characterize pathogenic bacteria in the poultry housing environment; 2) investigate antibiotic resistance of pathogenic bacteria isolated from chicken and guinea fowl carcasses and the poultry housing environment; and 3) differentiate prevalence and antibiotic resistance of pathogenic bacteria between chickens and guinea fowls.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Eighty each of Pearl Grey guinea fowl obtained from Ideal Poultry Breeding Farms (Cameron, TX) and Hyline Single Comb White Leghorn (SCWL, Hyline International, Warren, IN) chickens were weighed and randomly assigned to electrically heated, temperature-controlled brood units (Petersime Brood Units, Model 2SD12, Petersime Incubator Company, Gettysburg, OH) equipped with raised wire floors for the first 3 wk of age (WOA). The battery cages measured 99 x 66 x 26 cm and each housed 10 birds. During the first WOA, the brooder temperature was maintained at 32.2°C and reduced gradually by 2.8°C every week until reaching 21.1°C; from this point on, no artificial heating was provided to the birds. At 4 WOA the birds were transferred onto floor pens covered with pine wood shavings where they were raised until 47 WOA. The concrete floor pens (240 x 150 cm) were covered with pine wood shavings litter to a depth of 10 cm. Each pen (which served as a replicate) housed 20 birds; each treatment was replicated twice and the experiment was repeated 2 times. Therefore, the total number of birds per treatment was 80. The birds were reared under standard conditions (Bell and Weaver, 2002a) and were fed standard Leghorn diets (NRC, 1994; Bell and Weaver, 2002a) and Pearl Grey guinea fowl diets (Nahashon et al., 2006) from hatch to 47 WOA. The diets were provided in mash form for ad libitum consumption. Water was provided in hanging bell water fountains for ad libitum consumption throughout the experimentation period. The birds received 23, 12, and 16 h of constant lighting from hatch to 8, 9 to 14, and 15 to 47 WOA, respectively. Ventilation within the battery holding room and the floor pens was maintained by thermostatically controlled exhaust fans.
The experimental house is part of Tennessee State University’s poultry research facilities, which include grower/breeder (floor) and layer (cage) houses. The poultry houses are about 100 feet apart and house chickens (layers, replacement pullets, and broilers) and sometimes guinea fowl. The floor house in which the experimental birds were reared is usually populated with breeder birds or replacement pullets. The house is usually depopulated, cleaned, and disinfected before repopulation with a new flock. This was the case before assigning the experimental birds in this study to their respective house. During the experimental period, antibiotics were not used in the experimental facilities and birds. However, before this study, antimicrobials such as erythromycin, chlortetracycline, and fluoroquinolones had been used to treat bacterial infections in poultry flocks that occupied these housing facilities. The anticoccidia drug amprolium (at 0.0125% of diet) was administered continuously through feed to the experimental birds.
Birds used in this study were not verified to be germ free. Furthermore, even with strict biosecurity measures that include cleaning and disinfecting, there are always some microorganisms present in the housing environment. On the other hand, microorganisms such as salmonella can be transmitted vertically and spread to other flocks horizontally. Birds also pick up microorganisms from litter and water because these are shared in the poultry house. It has been documented that air, water, supplies, and materials brought into the poultry houses can contribute to microbial levels (Bell and Weaver, 2002b). In the present study, the assumption was that the experimental birds would harbor or pick up pathogenic microorganisms from the housing environment even without inoculation of these microorganisms into individual birds.
Processing Procedures
At 47 WOA, 50% of experimental SCWL chickens (n = 40) and Pearl Grey guinea fowl (n = 40) were randomly selected and evaluated for presence of pathogenic microorganisms. Feed and water were withdrawn 12 h before slaughter. The birds were then manually caught and crated in plastic coops such that each coop contained 8 birds. All crates and equipment used in bird processing were cleaned in chlorinated water to ensure sanitized conditions. Crated birds were immediately transported and slaughtered. These birds were transported less than 100 m to the processing facility. While hanging by their feet, all 40 birds from each treatment group (bird type) were electrically stunned by passing their heads through 1% NaCl solution charged with electrical current (14V, 60 Hz) for 18 s. The birds were killed by hand using a conventional unilateral neck cut to sever the carotid artery and jugular vein and bled for 180 s. Birds were scalded for 120 s at 63°C in an air-agitated commercial scalder (Cantrell Model SS300CF, Cantrell Machine Co. Inc., Gainesville, GA) and picked for 30 s in a commercial in-line picker (Cantrell Model CPF-60, Cantrell Machine Co. Inc.). After the head, shanks, feet, and feathers were removed, the carcass was eviscerated manually by cutting around the vent to remove all of the viscera including the kidneys.
Sample Collection
The SCWL chicken (n = 40) and Pearl Grey guinea fowl (n = 40) carcasses were aseptically collected immediately after processing, refrigerated and transported to the laboratory for analysis. The samples were kept chilled (<4°C) and assayed within 1 h of collection. Each carcass was placed separately in a sterile bag containing 300 mL of buffered peptone water (BPW) and manually rinsed for 2 min, ensuring that all surfaces, internal and external, had contact with the rinse. Environmental samples from the farm included drinking water (10 mL; n = 40) and litter (10 g; n = 40). For environmental samples, 90 mL of BPW was added and pummeled in a stomacher 400 circulator (Seward Limited, London, UK) at 230 rpm for 2 min. The carcass rinse and the environmental homogenate from the samples were analyzed for the presence of Campylobacter, Salmonella, and other enteric bacteria. Drinking water samples were evaluated immediately after the bell water fountains were cleaned (fresh drinking water) and after 7 d (7 d-old drinking water). All samples were collected between December 2005 and August 2006, and between October and December 2007. All bird carcasses passed inspection and appeared healthy.
Isolation of Campylobacter spp.
Campylobacter spp. isolation and identification was achieved using selective media and biochemical tests. Carcass rinses (20 mL) and homogenate from litter and drinking water were placed in 20 mL of blood-free Bolton broth base (CM983, Oxoid, Basingstoke, UK), which had selective supplement (CR208E, Oxoid). The culture tubes were incubated at 42°C for 48 h. Microaerophilic conditions were generated by using Campygen sachets (CampyGen, Oxoid). After incubation, enrichment cultures were subcultured directly to Campylobacter blood-free selective agar plates (CM739, Oxoid) containing selective supplement (SR 155E, Oxoid). The plates were incubated microaerobically at 42°C for 48 h. Each suspected isolate was examined for catalase and oxidase production (Food and Drug Administration, 2005). The catalase- and oxidase-positive isolates were confirmed by API-Campy (BioMerieux, Durham, NC).
Isolation of Salmonella spp.
Salmonella spp. were also isolated using selective media and biochemical tests. Carcass rinses (BPW, 20 mL) and 20-mL homogenates from litter and drinking water were incubated at 37°C for 24 h. After incubation, 1.0 mL of enrichment broth was transferred into 9.0 mL of tetrathionate broth and incubated at 42°C for 24 h. A loopful of tetrathionate broth was streaked onto xylose-lysine-tergitol 4 agar (Difco) and incubated at 37°C for 24 h. Presumptive Salmonella colonies on xylose-lysine-tergitol 4 agar plates were further tested. The identities of Salmonella isolates were confirmed by use of the oxidase test and biochemical strips (API20E, BioMerieux).
Enumeration of Other Enterobacteriaceae
Carcass rinses (BPW) were enriched at 37°C for 20 h and 200 µL was streaked onto MacConkey agar (Oxoid) with incubation at 37°C for 24 h. Isolates were identified by oxidase tests and biochemical strips (API20E, BioMerieux) following the manufacturer’s recommendations. For each of the samples, typical colonies were selected to make a bacterial suspension, which was used to inoculate the strips. Biochemical tests were used to identify these isolates to the species or genus level.
Testing for Antimicrobial Susceptibility
The disk diffusion assay was performed according to the method described by the National Committee for Clinical Laboratory Standards [NCCLS, now Clinical and Laboratory Standards Institute] (CLSI, 2000). Cultures were tested for sensitivity to 10 antimicrobials (Table 1
). Staphylococcus aureus ATCC 29212 and Escherichia coli ATCC 25922 were used as quality control strains.
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Statistical Analysis
The experimental design was a completely randomized assignment of birds onto floor pens. Data were analyzed using the SAS/STAT software (SAS Institute, 1999). Differences in prevalence of Campylobacter and Salmonella among chickens, guinea fowl, and environmental samples were analyzed using the chi-square method. Significance implied P < 0.05 unless specified otherwise.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Campylobacter spp. and Salmonella spp. were isolated from 28 and 35% of whole chicken carcass rinses, respectively (Table 2). However, the number of Campylobacter spp. and Salmonella spp. isolated from guinea fowl (18 and 23%, respectively) was significantly lower (P < 0.05) when compared with those isolated from chickens. The litter (floor covering) material on which the birds were reared was also contaminated with Campylobacter. Campylobacter spp. and Salmonella spp. were isolated in 13 and 23% of the litter samples collected from the floor pens housing both chickens and guinea fowl. Apparently, the numbers of positive isolates of these pathogens obtained from pens that housed chickens were not different (P > 0.05) from those obtained from pens that housed the guinea fowl. Although Campylobacter was not recovered from the drinking water, about 13% of the samples tested were positive for Salmonella spp. The Salmonella spp. were isolated from 7-d-old drinking water but not from fresh water. Although Campylobacter jejuni and C. lari were the 2 common Campylobacter species isolated from chickens and guinea fowls carcasses and litter materials, Campylobacter upsaliensis was recovered only in the guinea fowl carcasses (Table 3). Overall, Salmonella were present in chickens and guinea fowl carcasses, and in the environmental samples.
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. Klebsiella pneumoniae were isolated from carcasses of chickens and guinea fowl and from all environmental samples evaluated. Klebsiella oxytoca and Enterobacter sakazakii were isolated only in chicken carcasses and not in guinea fowl carcasses or environmental samples. On the other hand, E. coli was found in carcasses of broilers and guinea fowls and in environmental samples, whereas Pseudomonas aeruginosa was found only in the chicken carcasses. Enterobacter aerogenes and Citrobacter youngue were only recovered in chickens and guinea fowl carcasses, but not in environmental samples. Antibiotic Resistance of Pathogenic Bacteria in Chickens and Guinea Fowls
Expressions of antibiotic resistance by microorganisms isolated from chickens and guinea fowls carcasses are presented in Tables 4 and 5, respectively. Campylobacter jejuni isolated from chickens and guinea fowl were resistant to ampicillin, ciprofloxacin, erythromycin, and nalidixic acid. Campylobacter lari was only resistant to ampicillin, kanamycin, and nalidixic acid. However, isolates of C. upsaliensis from guinea fowls were not resistant to any of the antibiotics evaluated. Salmonella isolates were resistant to ampicillin, streptomycin, and tetracycline, whereas E. coli isolates were resistant to ampicillin and nalidixic acid. Klebsiella pneumoniae was resistant to ampicillin, erythromycin, cefoxitin, streptomycin, and nalidixic acid. On the other hand, K. oxytoca isolated from chickens were resistant to ampicillin and erythromycin (Table 4). Enterobacter sakazakii also isolated from chicken was resistant to ampicillin and gentamicin. Pseudomonas aeruginosa isolated from chicken was not resistant to any of the antibiotics tested. Out of 80 isolates, from environmental samples, chicken, and guinea fowl, only 30 of the isolates (37.5%) were resistant to antibiotics.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Several pathogenic bacteria including C. jejuni, C. lari, Salmonella spp., and K. pneumoniae were isolated from carcasses of both chickens and guinea fowl. Although C. jejuni and C. lari were the 2 common Campylobacter species isolated in chicken and guinea fowl carcasses as well as litter materials, C. upsaliensis was recovered only in guinea fowls (Table 3). On the other hand, Salmonella were present in chickens and guinea fowl carcasses and in the environmental samples. Previous reports show that chickens are an important reservoir for C. lari (Shih, 2000). Fresh chicken carcasses have been indicated to contain high numbers (approximately 105 cfu/g) of Campylobacter spp. (Cogan et al., 1999). Salmonella and Campylobacter have also been isolated in chicken feed and water (Pedungtod and Kaneene, 2005).
Multidrug-resistance (ampicillin, ciprofloxacin, erythromycin, kanamycin, and nalidixic acid) was observed in Campylobacter spp. that were isolated from chickens and guinea fowl (Tables 4 and 5, respectively). Findings of significance in this study include the confirmation of the existence of antimicrobial resistance of Campylobacter to ciprofloxacin and erythromycin, antibiotics commonly used for treatment of campylobacteriosis in humans. Recent reports (Larkin et al., 2006; Threlfall et al., 2006) have cited evidence for an increase in the incidence of ciprofloxacin-resistant Campylobacter throughout the world. A recent survey of Campylobacter from raw poultry products indicated that 35% of isolates were resistant to ciprofloxacin (Ge et al., 2003). In this study, antimicrobial drugs for which Salmonella isolates exhibited resistance were ampicillin, streptomycin, and tetracycline. Salmonella spp. isolated from chickens have also been reported to be resistant to ampicillin, tetracycline, and gentamycin (Wilson, 2004). The antibiotic resistance in Salmonella from chickens should be considered a great risk for treatment of human salmonellosis. Escherichia coli isolates from chicken carcasses were only resistant to ampicillin and nalidixic acid (Table 4), whereas similar isolates from guinea fowl were only resistant to ampicillin (Table 5). Recent reports (Schroeder et al., 2004) have shown that E. coli isolated from meat and poultry demonstrated resistance to at least one antimicrobial drug. The housing environment in which the experimental birds were housed was previously populated with flocks that were treated with antibiotics. However, antibiotics were not fed to experimental birds in this study. Therefore, any microorganisms, antibiotic resistant or not, that were isolated from the housing environment and carcasses may have been introduced through the birds, air, supplies, and objects brought into the poultry house.
Resistance to the multidrugs ampicillin, cefoxitin, nalidixic acid, and streptomycin were observed in K. pneumoniae isolates (Tables 4 and 5, respectively). This observation was consistent with previous reports (Kim et al., 2005) that multidrug-resistant K. pneumoniae was isolated in farm environments and retail poultry and beef products. Klebsiella pneumoniae is resistant to several antibiotics such as ampicillin, streptomycin, gentamicin, chlorolphenicol, tetracycline, and ofloxacin (Rasool et al., 2003). Klebsiella pneumoniae is therefore an increasing problem in hospitals because of the evolution of antibiotic-resistant strains. In the present study, K. oxytoca isolates from chickens were resistant to ampicillin and erythromycin (Table 4). The E. sakazakii isolates recovered from chickens were resistant to ampicillin and gentamycin (Table 4). These findings are consistent with previous reports that E. sakazakii was resistant to multiple antibiotics, including ampicillin, gentamicin, and cefotaxime (Dennison and Morris, 2002). Enterobacter sakazakii is considered a food-borne pathogen that can cause severe illness and death in newborns, particularly in premature newborns or infants with weakened immune systems (Lai, 2001).
In conclusion, these data indicate that chicken and guinea fowl are reservoirs of antibiotic-resistant Salmonella, C. jejuni, C. lari, E. coli, and Klebsiella spp. There is potential for these antibiotic-resistant bacteria to be transferred to humans through contaminated poultry. Multidrug resistance of foodborne pathogens is certainly a public health concern and reinforces the need for more prudent use of antibiotics by farmers, veterinarians, and physicians. Therefore, a continued development of methods to reduce risk of foodborne pathogens in poultry is critical.
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ACKNOWLEDGMENTS |
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Received for publication April 13, 2007. Accepted for publication May 11, 2008.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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