The Challenge of Regulating Agricultural Ceftiofur Use To Slow the Emergence of Resistance to Extended-Spectrum Cephalosporins

Wittum, Thomas E.

doi:10.1128/aem.01967-12

Cited by 19 publications

(14 citation statements)

References 17 publications

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“…It might be assumed that clinical strains of E. coli O157, changing their natural habitat and entering into the human food chain, would be exposed to significant stress conditions for extended periods prior to human infection, which might result in rapid loss of the mobile DNA elements that harbor antibiotic resistance genes. Taken together, these results support the hypothesis that the mass application of AGPs to food animals housed in population-dense environments most likely has a significant effect on the emergence and dissemination of antimicrobial resistance phenotypes (34,43). During the past decade, population genetics-based studies have increasingly shaped our understanding of the diversity and complexity of E. coli O157 populations.…”

Section: Discussionsupporting

confidence: 69%

Molecular and Antimicrobial Susceptibility Analyses Distinguish Clinical from Bovine Escherichia coli O157 Strains

Vidović

Tsoi²,

Medihala³

et al. 2013

J Clin Microbiol

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A population-based study combining (i) antimicrobial, (ii) genetic, and (iii) virulence analyses with molecular evolutionary analyses revealed segregative characteristics distinguishing human clinical and bovine Escherichia coli O157 strains from western Canada. Human (n ‫؍‬ 50) and bovine (n ‫؍‬ 50) strains of E. coli O157 were collected from Saskatchewan and Manitoba in 2006 and were analyzed by using the six-marker lineage-specific polymorphism assay (LSPA6), antimicrobial susceptibility analysis, the colicin assay, plasmid and virulence profiling including the eae, ehxA, espA, iha, stx 1 , stx 2 , stx 2c , stx 2d , stx 2d-activatable , stx 2e , and stx 2f virulence-associated genes, and structure analyses. Multivariate logistic regression and Fisher's exact test strongly suggested that antimicrobial susceptibility was the most distinctive characteristic (P ‫؍‬ 0.00487) associated with human strains. Among all genetic, virulence, and antimicrobial determinants, resistance to tetracycline (P < 0.000) and to sulfisoxazole (P < 0.009) were the most strongly associated segregative characteristics of bovine E. coli O157 strains. Among 11 virulence-associated genes, stx 2c showed the strongest association with E. coli O157 strains of bovine origin. LSPA6 genotyping showed the dominance of the lineage I genotype among clinical (90%) and bovine (70%) strains, indicating the importance of lineage I in O157 epidemiology and ecology. Population structure analysis revealed that the more-diverse bovine strains came from a unique group of strains characterized by a high degree of antimicrobial resistance and high frequencies of lineage II genotypes and stx 2c variants. These findings imply that antimicrobial resistance generated among bovine strains of E. coli O157 has a large impact on the population of this human pathogen.

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Section: Discussionsupporting

confidence: 69%

Molecular and Antimicrobial Susceptibility Analyses Distinguish Clinical from Bovine Escherichia coli O157 Strains

Vidović

Tsoi²,

Medihala³

et al. 2013

J Clin Microbiol

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“…n-feed and in-water uses of medically important antimicrobials for the control and prevention of diseases have become controversial, because it is argued that they unnecessarily expose healthy animals to medically important antimicrobials and possibly increase the spread of antimicrobial resistance (AMR) (1)(2)(3). Restricting the use of medically important antimicrobials in food animal production has been suggested as a means to reduce AMR (1,(3)(4)(5).…”

mentioning

confidence: 99%

“…Restricting the use of medically important antimicrobials in food animal production has been suggested as a means to reduce AMR (1,(3)(4)(5). Conversely, studies have reported only small quantitative risks of human-pathogenic bacteria acquiring AMR due the use of antimicrobials in food animal production (6)(7)(8)(9).…”

mentioning

confidence: 99%

Effects of In-Feed Chlortetracycline Prophylaxis in Beef Cattle on Animal Health and Antimicrobial-Resistant Escherichia coli

Agga

Schmidt

Arthur

2016

Appl Environ Microbiol

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Concerns have been raised that in-feed chlortetracycline (CTC) may increase antimicrobial resistance (AMR), specifically tetracycline-resistant (TET r ) Escherichia coli and third-generation cephalosporin-resistant (3GC r ) E. coli. We evaluated the impact of a 5-day in-feed CTC prophylaxis on animal health, TET r E. coli, and 3GC r 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), TET r E. coli, and 3GC r 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, TET r E. coli concentrations were higher for the CTC group than the control group (P < 0.01). On 27 dpt, 75 dpt, and 117 dpt, TET r E. coli concentrations did not differ between groups. 3GC r E. coli occurrences did not differ between control and CTC groups on any sampling occasion. For both groups, generic, TET r , and 3GC r 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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“…A few other reports document varied antibiotic resistance acquisition during Salmonella infections from nosocomial (63) or inpatient isolates of other Gram-negative pathogens (64)(65)(66). Most drugresistant Salmonella isolates are suggested to arise from foods of animal origin, potentially from the use of antimicrobial agents in livestock (13,67,68). However, the development of antibiotic resistance within Salmonella strains as part of human fecal carriage has also been observed.…”

Section: Discussionmentioning

confidence: 99%

Whole-Genome Sequencing Identifies In Vivo Acquisition of a bla _CTX-M-27 -Carrying IncFII Transmissible Plasmid as the Cause of Ceftriaxone Treatment Failure for an Invasive Salmonella enterica Serovar Typhimurium Infection

McCollister

Kotter

Frank

et al. 2016

Antimicrob Agents Chemother

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bWe report a case of ceftriaxone treatment failure for bacteremia caused by Salmonella enterica subsp. enterica serovar Typhimurium, due to the in vivo acquisition of a bla CTX-M-27 -encoding IncFII group transmissible plasmid. The original ␤-lactamasesusceptible isolate ST882S was replaced by the resistant isolate ST931R during ceftriaxone treatment. After relapse, treatment was changed to ciprofloxacin, and the patient recovered. Isolate ST931R could transfer resistance to Escherichia coli at 37°C. We used whole-genome sequencing of ST882S and ST931R, the E. coli transconjugant, and isolated plasmid DNA to unequivocally show that ST882S and ST931R had identical chromosomes, both having 206 identical single-nucleotide polymorphisms (SNPs) versus S. Typhimurium 14028s. We assembled a complete circular genome for ST931R, to which ST882S reads mapped with no SNPs. ST882S and ST931R were isogenic except for the presence of three additional plasmids in ST931R. ST931R and the E. coli transconjugant were ceftriaxone resistant due to the presence of a 60.5-kb IS26-flanked, bla CTX-M-27 -encoding IncFII plasmid. Compared to 14082s, ST931R has almost identical Gifsy-1, Gifsy-2, and ST64B prophages, lacks Gifsy-3, and instead carries a unique Fels-2 prophage related to that found in LT2. ST882S and ST931R both had a 94-kb virulence plasmid showing >99% identity with pSLT14028s and a cryptic 3,904-bp replicon; ST931R also has cryptic 93-kb IncI1 and 62-kb IncI2 group plasmids. To the best of our knowledge, in vivo acquisition of extended-spectrum ␤-lactamase resistance by S. Typhimurium and bla CTX-M-27 genes in U.S. isolates of Salmonella have not previously been reported. G reater than 1.4 million cases of nontyphoidal salmonellosis are estimated to occur each year in the United States, with approximately 95% of cases resulting from foodborne transmission (1). Although most infections result in mild to moderate gastroenteritis that usually resolves with or without treatment, concurrent bacteremia is observed in approximately 6% of patients and can be associated with serious disease, especially in infants aged Ͻ1 year, the elderly, and those with immunocompromised states such as HIV infection (2-5). Although routine use of antimicrobial therapy is not generally recommended for the treatment of most Salmonella infections, such therapy may be lifesaving in persons with invasive disease.Treatment of invasive salmonellosis has been compromised in recent years due to the emergence of Salmonella isolates with single or multidrug resistance to a number of first-line agents (6, 7). Antimicrobial resistance in strains of nontyphoidal Salmonella (NTS) has been linked to the use of antimicrobial agents in livestock (8-11). Consequently, agents such as fluoroquinolones and third generation cephalosporins, such as ceftriaxone, have become treatment modalities of choice for therapy against severe Salmonella infections. In the United States before 1996, all reported cases of infection with ceftriaxone-resistant NTS isolates were known o...

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The Challenge of Regulating Agricultural Ceftiofur Use To Slow the Emergence of Resistance to Extended-Spectrum Cephalosporins

Cited by 19 publications

References 17 publications

Molecular and Antimicrobial Susceptibility Analyses Distinguish Clinical from Bovine Escherichia coli O157 Strains

Molecular and Antimicrobial Susceptibility Analyses Distinguish Clinical from Bovine Escherichia coli O157 Strains

Effects of In-Feed Chlortetracycline Prophylaxis in Beef Cattle on Animal Health and Antimicrobial-Resistant Escherichia coli

Whole-Genome Sequencing Identifies In Vivo Acquisition of a bla _CTX-M-27 -Carrying IncFII Transmissible Plasmid as the Cause of Ceftriaxone Treatment Failure for an Invasive Salmonella enterica Serovar Typhimurium Infection

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The Challenge of Regulating Agricultural Ceftiofur Use To Slow the Emergence of Resistance to Extended-Spectrum Cephalosporins

Cited by 19 publications

References 17 publications

Molecular and Antimicrobial Susceptibility Analyses Distinguish Clinical from Bovine Escherichia coli O157 Strains

Molecular and Antimicrobial Susceptibility Analyses Distinguish Clinical from Bovine Escherichia coli O157 Strains

Effects of In-Feed Chlortetracycline Prophylaxis in Beef Cattle on Animal Health and Antimicrobial-Resistant Escherichia coli

Whole-Genome Sequencing Identifies In Vivo Acquisition of a bla CTX-M-27 -Carrying IncFII Transmissible Plasmid as the Cause of Ceftriaxone Treatment Failure for an Invasive Salmonella enterica Serovar Typhimurium Infection

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Whole-Genome Sequencing Identifies In Vivo Acquisition of a bla _CTX-M-27 -Carrying IncFII Transmissible Plasmid as the Cause of Ceftriaxone Treatment Failure for an Invasive Salmonella enterica Serovar Typhimurium Infection