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Tetracycline Resistant Campylobacter jejuni Subtypes Emanating from Beef Cattle Administered Non-Therapeutic Chlortetracycline are Longitudinally Transmitted within the Production Continuum but are Not Detected in Ground Beef.

ABSTRACT: The impacts of the antimicrobial growth promoter (AGP), chlortetracycline with sulfamethazine (AS700), on the development of antimicrobial resistance and longitudinal transmission of Campylobacter jejuni within the beef production continuum were empirically determined. Carriage of tetracycline resistance determinants in the enteric bacterial community increased at a greater rate for AS700-treatment cattle. The majority of the bacteria from animals administered AS700 carried tetW. Densities of C. jejuni shed in feces increased over the confined feeding period, and the administration of AS700 did not conspicuously reduce C. jejuni densities in feces or within the intestine. The majority of C. jejuni isolates recovered were resistant to tetracycline, but the resistance rates to other antibiotics was low (?20.1%). The richness of C. jejuni subtypes recovered from AS700-treated animals that were either resistant or susceptible to tetracycline was reduced, indicating selection pressure due to AGP administration. Moreover, a degree of subtype-specific resistance to tetracycline was observed. tetO was the primary tetracycline resistance determinant conferring resistance in C. jejuni isolates recovered from cattle and people. Clinically-relevant C. jejuni subtypes (subtypes that represent a risk to human health) that were resistant to tetracycline were isolated from cattle feces, digesta, hides, the abattoir environment, and carcasses, but not from ground beef. Thus, study findings indicate that clinically-relevant C. jejuni subtypes associated with beef cattle, including those resistant to antibiotics, do not represent a significant foodborne risk.

SUBMITTER: Inglis GD

PROVIDER: S-EPMC7022225 | biostudies-literature | 2019 Dec

REPOSITORIES: biostudies-literature

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Tetracycline Resistant Campylobacter jejuni Subtypes Emanating from Beef Cattle Administered Non-Therapeutic Chlortetracycline are Longitudinally Transmitted within the Production Continuum but are Not Detected in Ground Beef.

Inglis G Douglas GD Gusse Jenny F JF House Kathaleen E KE Shelton Tara G TG Taboada Eduardo N EN

Microorganisms 20191221 1

The impacts of the antimicrobial growth promoter (AGP), chlortetracycline with sulfamethazine (AS700), on the development of antimicrobial resistance and longitudinal transmission of Campylobacter jejuni within the beef production continuum were empirically determined. Carriage of tetracycline resistance determinants in the enteric bacterial community increased at a greater rate for AS700-treatment cattle. The majority of the bacteria from animals administered AS700 carried tetW. D ...[more]

PMID: 31877744

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Project description:Increasing evidence exists for the role that cattle play in the epidemiology of campylobacteriosis. In this study, the prevalence and distribution of Campylobacter jejuni were longitudinally examined at the subspecies level in the beef cattle production continuum. Animals were subdivided into two groups: those that were not administered antibiotics and those that were administered the antimicrobial growth promoter chlortetracycline and sulfamethazine (AS700). Samples were longitudinally collected throughout the confined feeding operation (CFO) period and during the slaughter process, and C. jejuni was isolated and genotyped to assess subtype richness and to elucidate transmission dynamics from farm to fork. The bacterium was frequently isolated from cattle, and the bacterial densities shed in feces increased over the CFO period. Campylobacter jejuni was also isolated from digesta, hides, the abattoir environment, and carcasses. The administration of AS700 did not conspicuously reduce the C. jejuni densities in feces or within the intestine but significantly reduced the bacterial densities and the diversity of subtypes on abattoir samples. All cattle carried multiple subtypes, including clinically relevant subtypes known to represent a risk to human health. Instances of intra-animal longitudinal transmission were observed. Although clinically relevant subtypes were transmitted to carcasses via direct contact and aerosols, the bacterium could not be isolated nor could its DNA be detected in ground beef regardless of treatment. Although the evidence indicated that beef cattle represent a significant reservoir for C. jejuni, including high-risk subtypes strongly associated with the bovine host, they do not appear to represent a significant risk for direct foodborne transmission. This implicates alternate routes of human transmission.IMPORTANCE Limited information is available on the transmission of Campylobacter jejuni subtypes in the beef production continuum and the foodborne risk posed to humans. Cattle were colonized by diverse subtypes of C. jejuni, and the densities of the bacterium shed in feces increased during the confined feeding period. Campylobacter jejuni was readily associated with the digesta, feces, and hides of cattle entering the abattoir, as well as the local environment. Moreover, C. jejuni cells were deposited on carcasses via direct contact and aerosols, but the bacterium was not detected in the ground beef generated from contaminated carcasses. We conclude that C. jejuni bacterial cells associated with beef cattle do not represent a significant risk through food consumption and suggest that clinically relevant subtypes are transmitted through alternate routes of exposure.

Project description:Concerns have been raised that in-feed chlortetracycline (CTC) may increase antimicrobial resistance (AMR), specifically tetracycline-resistant (TETr) Escherichia coli and third-generation cephalosporin-resistant (3GCr) E. coli We evaluated the impact of a 5-day in-feed CTC prophylaxis on animal health, TETr E. coli, and 3GCr E. coli A control group of cattle (n = 150) received no CTC, while a CTC group (n = 150) received in-feed CTC (10 mg/lb of body weight/day) from the 5th to the 9th day after feedlot arrival. Over 25% (38/150) of the animals in the control group developed illnesses requiring therapeutic treatment with antimicrobials critically important to human medicine. Only two animals (1.3%) in the CTC group required such treatments. Fecal swab and pen surface occurrences of generic E. coli (isolated on media that did not contain antimicrobials of interest and were not isolated based on any specific resistance), TETr E. coli, and 3GCr E. coli were determined on five sampling occasions: arrival at the feedlot, 5 days posttreatment (5 dpt), 27 dpt, 75 dpt, and 117 dpt. On 5 dpt, TETr E. coli concentrations were higher for the CTC group than the control group (P < 0.01). On 27 dpt, 75 dpt, and 117 dpt, TETr E. coli concentrations did not differ between groups. 3GCr E. coli occurrences did not differ between control and CTC groups on any sampling occasion. For both groups, generic, TETr, and 3GCr E. coli occurrences were highest on 75 dpt and 117 dpt, suggesting that factors other than in-feed CTC contributed more significantly to antimicrobial-resistant E. coli occurrence.ImportanceThe occurrence of human bacterial infections resistant to antimicrobial therapy has been increasing. It has been postulated that antimicrobial resistance was inevitable, but the life span of the antimicrobial era has been prematurely compromised due to the misuse of antimicrobials in clinical and agricultural practices. Direct evidence relating the use of antimicrobials in livestock production to diminished human health outcomes due to antimicrobial resistance is lacking, and the U.S. Food and Drug Administration has taken an approach to maximize therapeutic efficacy and minimize the selection of resistant microorganisms through judicious use of antimicrobials. This study demonstrated that prophylactic in-feed treatment of chlortetracycline administered for 5 days to calves entering feedlots is judicious, as this therapy reduced animal morbidity, reduced the use of antimicrobials more critical to human health, and had no long-term impact on the occurrence of antimicrobial-resistant E. coli.

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Dataset Information

Tetracycline Resistant Campylobacter jejuni Subtypes Emanating from Beef Cattle Administered Non-Therapeutic Chlortetracycline are Longitudinally Transmitted within the Production Continuum but are Not Detected in Ground Beef.

Publications

Tetracycline Resistant <i>Campylobacter jejuni</i> Subtypes Emanating from Beef Cattle Administered Non-Therapeutic Chlortetracycline are Longitudinally Transmitted within the Production Continuum but are Not Detected in Ground Beef.

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