Skip to main content
Top
Published in: Comparative Clinical Pathology 2/2017

01-03-2017 | Original Article

Farm-level evaluation of enrofloxacin resistance in Escherichia coli isolated from broiler chickens during a rearing period

Authors: Bahman Abdi-Hachesoo, Keramat Asasi, Hassan Sharifiyazdi

Published in: Comparative Clinical Pathology | Issue 2/2017

Login to get access

Abstract

In this study, enrofloxacin resistance was investigated in commensal Escherichia coli isolated from broiler chickens using phenotypic and genotypic assays. Five E. coli isolates were recovered from the cloacal swabs of 15 broiler chickens in the farms at the ages of 1 day (stage 1), 30 days (stage 2), and 1 day before slaughter (stage 3). Minimum inhibitory concentration results for enrofloxacin showed that the prevalence of resistance significantly increased (P < 0.05) during the rearing period (43, 80, and 86%, respectively, for stages 1, 2, and 3, respectively). Relation of enrofloxacin resistance with gyrA and parC mutations was evaluated by sequencing and PCR-RFLP. Wild-type isolates (without mutations in gyrA and parC) and isolates with a single mutation in Ser-83 were higher in early days of the rearing period of chickens in comparison with the second and third stages. Mutations at both Ser-83 and Asp-87 of gyrA and at Ser-80 of parC were higher in the second and third stages of rearing period. No qnrA, qnrB, and qnrS determinants were detected among these E. coli isolates. Evaluation of different risk factors showed that factors related to antimicrobial exposure such as antibiotic consumption in previous stocking, occurrence of colibacillosis and respiratory viral infections, and antibiotic usage in recent stocking significantly increased the rate of enrofloxacin resistance (P < 0.05).
Literature
go back to reference Abdi-Hachesoo B, Asasi K, Sharifiyazdi H (2013) Rapid detection of Escherichia coli gyrA and parC mutants in one-day-old broiler chicks in Iran. Vet Ital 49:291–297PubMed Abdi-Hachesoo B, Asasi K, Sharifiyazdi H (2013) Rapid detection of Escherichia coli gyrA and parC mutants in one-day-old broiler chicks in Iran. Vet Ital 49:291–297PubMed
go back to reference Belloc C, Lam D, Pellerin JL, Beaudeau F, Laval A (2005) Effect of quinolone treatment on selection and persistence of quinolone-resistant Escherichia coli in swine faecal flora. J Appl Microbiol 99:954–959CrossRefPubMed Belloc C, Lam D, Pellerin JL, Beaudeau F, Laval A (2005) Effect of quinolone treatment on selection and persistence of quinolone-resistant Escherichia coli in swine faecal flora. J Appl Microbiol 99:954–959CrossRefPubMed
go back to reference Bergeron CR, Prussing C, Boerlin P, Daignault D, Dutil L, Reid-Smith RJ, Zhanel GG, Manges AR (2012) Chicken as reservoir for extraintestinal pathogenic Escherichia coli in humans, Canada. Emerg Infect Dis 18:415–421CrossRefPubMedPubMedCentral Bergeron CR, Prussing C, Boerlin P, Daignault D, Dutil L, Reid-Smith RJ, Zhanel GG, Manges AR (2012) Chicken as reservoir for extraintestinal pathogenic Escherichia coli in humans, Canada. Emerg Infect Dis 18:415–421CrossRefPubMedPubMedCentral
go back to reference Blanco JE, Blanco M, Mora A, Blanco J (1997) Prevalence of bacterial resistance to quinolones and other antimicrobials among avian Escherichia coli strains isolated from septicemic and healthy chickens in Spain. J Clin Microbiol 35:2184–2185PubMedPubMedCentral Blanco JE, Blanco M, Mora A, Blanco J (1997) Prevalence of bacterial resistance to quinolones and other antimicrobials among avian Escherichia coli strains isolated from septicemic and healthy chickens in Spain. J Clin Microbiol 35:2184–2185PubMedPubMedCentral
go back to reference Cattoir V, Poirel L, Rotimi V, Soussy C-J, Nordmann P (2007) Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 60(2):394–397 Cattoir V, Poirel L, Rotimi V, Soussy C-J, Nordmann P (2007) Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 60(2):394–397
go back to reference Clinical and Laboratory Standards Institute (2013) Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Approved Standard – 4rd Ed. CLSI, Wayne, Pennsylvania, Vet01-A4 Clinical and Laboratory Standards Institute (2013) Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Approved Standard – 4rd Ed. CLSI, Wayne, Pennsylvania, Vet01-A4
go back to reference Cohen SP, McMurry L, Hooper D, Wolfson J, Levy S (1989) Cross-resistance to fluoroquinolones in multiple-antibiotic-resistant (Mar) Escherichia coli selected by tetracycline or chloramphenicol: decreased drug accumulation associated with membrane changes in addition to OmpF reduction. Antimicrob Agents Chemother 33:1318–1325CrossRefPubMedPubMedCentral Cohen SP, McMurry L, Hooper D, Wolfson J, Levy S (1989) Cross-resistance to fluoroquinolones in multiple-antibiotic-resistant (Mar) Escherichia coli selected by tetracycline or chloramphenicol: decreased drug accumulation associated with membrane changes in addition to OmpF reduction. Antimicrob Agents Chemother 33:1318–1325CrossRefPubMedPubMedCentral
go back to reference Da Costa PM, Oliveira M, Ramos B, Bernardo F (2011) The impact of antimicrobial use in broiler chickens on growth performance and on the occurrence of antimicrobial-resistant Escherichia coli. Livest Sci 136:262–269CrossRef Da Costa PM, Oliveira M, Ramos B, Bernardo F (2011) The impact of antimicrobial use in broiler chickens on growth performance and on the occurrence of antimicrobial-resistant Escherichia coli. Livest Sci 136:262–269CrossRef
go back to reference Everett MJ, Jin YF, Ricci V, Piddock L (1996) Contributions of individual mechanisms to fluoroquinolone resistance in 36 Escherichia coli strains isolated from humans and animals. Antimicrob Agents Chemother 40:2380–2386PubMedPubMedCentral Everett MJ, Jin YF, Ricci V, Piddock L (1996) Contributions of individual mechanisms to fluoroquinolone resistance in 36 Escherichia coli strains isolated from humans and animals. Antimicrob Agents Chemother 40:2380–2386PubMedPubMedCentral
go back to reference Fàbrega A, Madurga S, Giralt E, Vila J (2009) Mechanism of action of and resistance to quinolones. Microb Biotechnol 2:40–61CrossRefPubMed Fàbrega A, Madurga S, Giralt E, Vila J (2009) Mechanism of action of and resistance to quinolones. Microb Biotechnol 2:40–61CrossRefPubMed
go back to reference Giovanardi D, Campagnari E, Ruffoni LS, Pesente P, Ortali G, Furlattini V (2005) Avian pathogenic Escherichia coli transmission from broiler breeders to their progeny in an integrated poultry production chain. Avian Pathol 34:313–318CrossRefPubMed Giovanardi D, Campagnari E, Ruffoni LS, Pesente P, Ortali G, Furlattini V (2005) Avian pathogenic Escherichia coli transmission from broiler breeders to their progeny in an integrated poultry production chain. Avian Pathol 34:313–318CrossRefPubMed
go back to reference Hofacre CL, Rene’de Cotret A, Maurer JJ, Garritty A, Thayer SG (2000) Presence of fluoroquinolone-resistant coliforms in poultry litter. Avian Dis 44:963–967CrossRefPubMed Hofacre CL, Rene’de Cotret A, Maurer JJ, Garritty A, Thayer SG (2000) Presence of fluoroquinolone-resistant coliforms in poultry litter. Avian Dis 44:963–967CrossRefPubMed
go back to reference Huff W, Huff G, Rath N, Balog J, Donoghue A (2004) Therapeutic efficacy of bacteriophage and Baytril (enrofloxacin) individually and in combination to treat colibacillosis in broilers. Poult Sci 83:1944–1947CrossRefPubMed Huff W, Huff G, Rath N, Balog J, Donoghue A (2004) Therapeutic efficacy of bacteriophage and Baytril (enrofloxacin) individually and in combination to treat colibacillosis in broilers. Poult Sci 83:1944–1947CrossRefPubMed
go back to reference Johnson JR, Kuskowski MA, Menard M, Gajewski A, Xercavins M, Garau J (2006) Similarity between human and chicken Escherichia coli isolates in relation to ciprofloxacin resistance status. J Infect Dis 194:71–78CrossRefPubMed Johnson JR, Kuskowski MA, Menard M, Gajewski A, Xercavins M, Garau J (2006) Similarity between human and chicken Escherichia coli isolates in relation to ciprofloxacin resistance status. J Infect Dis 194:71–78CrossRefPubMed
go back to reference Jones E, Snow L, Carrique-Mas J, Gosling R, Clouting C, Davies R (2013) Risk factors for antimicrobial resistance in Escherichia coli found in GB turkey flocks. Vet Rec 173:422–422CrossRefPubMed Jones E, Snow L, Carrique-Mas J, Gosling R, Clouting C, Davies R (2013) Risk factors for antimicrobial resistance in Escherichia coli found in GB turkey flocks. Vet Rec 173:422–422CrossRefPubMed
go back to reference Leal RMP, Figueira RF, Tornisielo VL, Regitano JB (2012) Occurrence and sorption of fluoroquinolones in poultry litters and soils from São Paulo State, Brazil. Sci Total Environ 432:344–349CrossRefPubMed Leal RMP, Figueira RF, Tornisielo VL, Regitano JB (2012) Occurrence and sorption of fluoroquinolones in poultry litters and soils from São Paulo State, Brazil. Sci Total Environ 432:344–349CrossRefPubMed
go back to reference Moniri R, Dastehgoli K (2005) Fluoroquinolone-resistant Escherichia coli isolated from healthy broilers with previous exposure to fluoroquinolones: is there a link? Microb Ecol Health Dis 17:69–74CrossRef Moniri R, Dastehgoli K (2005) Fluoroquinolone-resistant Escherichia coli isolated from healthy broilers with previous exposure to fluoroquinolones: is there a link? Microb Ecol Health Dis 17:69–74CrossRef
go back to reference Morales-Gutiérrez F, Barbosa J, Barrón D (2015) Metabolic study of enrofloxacin and metabolic profile modifications in broiler chicken tissues after drug administration. Food Chem 172:30–39CrossRefPubMed Morales-Gutiérrez F, Barbosa J, Barrón D (2015) Metabolic study of enrofloxacin and metabolic profile modifications in broiler chicken tissues after drug administration. Food Chem 172:30–39CrossRefPubMed
go back to reference Nelson JM, Chiller TM, Powers JH, Angulo FJ (2007) Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a public health success story. Clin Infect Dis 44:977–980CrossRefPubMed Nelson JM, Chiller TM, Powers JH, Angulo FJ (2007) Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a public health success story. Clin Infect Dis 44:977–980CrossRefPubMed
go back to reference Nolan LK, Barnes JH, Vaillancourt JP, Abdul-Aziz T, Logue CM (2013) Colibacillosis. In: Swayne DE (ed) Disease of poultry, 13th edn. Iowa State University Press, Ames, pp 751–805 Nolan LK, Barnes JH, Vaillancourt JP, Abdul-Aziz T, Logue CM (2013) Colibacillosis. In: Swayne DE (ed) Disease of poultry, 13th edn. Iowa State University Press, Ames, pp 751–805
go back to reference Ozeki S, Deguchi T, Yasuda M, Nakano M, Kawamura T, Nishino Y, Kawada Y (1997) Development of a rapid assay for detecting gyrA mutations in Escherichia coli and determination of incidence of gyrA mutations in clinical strains isolated from patients with complicated urinary tract infections. J Clin Microbiol 35:2315–2319PubMedPubMedCentral Ozeki S, Deguchi T, Yasuda M, Nakano M, Kawamura T, Nishino Y, Kawada Y (1997) Development of a rapid assay for detecting gyrA mutations in Escherichia coli and determination of incidence of gyrA mutations in clinical strains isolated from patients with complicated urinary tract infections. J Clin Microbiol 35:2315–2319PubMedPubMedCentral
go back to reference Petersen A, Christensen JP, Kuhnert P, Bisgaard M, Olsen JE (2006) Vertical transmission of a fluoroquinolone-resistant Escherichia coli within an integrated broiler operation. Vet Microbiol 116:120–128CrossRefPubMed Petersen A, Christensen JP, Kuhnert P, Bisgaard M, Olsen JE (2006) Vertical transmission of a fluoroquinolone-resistant Escherichia coli within an integrated broiler operation. Vet Microbiol 116:120–128CrossRefPubMed
go back to reference Rad M, Kooshan M, Mesgarani H (2012) Quinolone resistance among Salmonella enterica and Escherichia coli of animal origin. Comp Clin Path 21:161–165CrossRef Rad M, Kooshan M, Mesgarani H (2012) Quinolone resistance among Salmonella enterica and Escherichia coli of animal origin. Comp Clin Path 21:161–165CrossRef
go back to reference Redgrave LS, Sutton SB, Webber MA, Piddock LJ (2014) Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 22:438–445CrossRefPubMed Redgrave LS, Sutton SB, Webber MA, Piddock LJ (2014) Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 22:438–445CrossRefPubMed
go back to reference Rodríguez-Martínez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual Á (2011) Plasmid-mediated quinolone resistance: an update. J Infect Chemother 17:149–182CrossRefPubMed Rodríguez-Martínez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual Á (2011) Plasmid-mediated quinolone resistance: an update. J Infect Chemother 17:149–182CrossRefPubMed
go back to reference Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
go back to reference Shams F, Hasani A, Pormohammad A (2014) The first report of the qnr, aac (6′)-Ib-cr and qepA genes in quinolone resistant Escherichia coli and Klebsiella pneumoniae in Iran. Iran J Public Health 43:99 Shams F, Hasani A, Pormohammad A (2014) The first report of the qnr, aac (6′)-Ib-cr and qepA genes in quinolone resistant Escherichia coli and Klebsiella pneumoniae in Iran. Iran J Public Health 43:99
go back to reference Taylor NM, Clifton-Hadley FA, Wales AD, Ridley A, Davies RH (2009) Farm-level risk factors for fluoroquinolone resistance in E. coli and thermophilic Campylobacter spp. on finisher pig farms. Epidemiol Infect 137(08):1121 Taylor NM, Clifton-Hadley FA, Wales AD, Ridley A, Davies RH (2009) Farm-level risk factors for fluoroquinolone resistance in E. coli and thermophilic Campylobacter spp. on finisher pig farms. Epidemiol Infect 137(08):1121
go back to reference Witte W (2000) Selective pressure by antibiotic use in livestock. Int J Antimicrob Agents 16:19–24CrossRef Witte W (2000) Selective pressure by antibiotic use in livestock. Int J Antimicrob Agents 16:19–24CrossRef
go back to reference Yang H, Chen S, White DG, Zhao S, McDermott P, Walker R, Meng J (2004) Characterization of multiple-antimicrobial-resistant Escherichia coli isolates from diseased chickens and swine in China. J Clin Microbiol 42:3483–3489CrossRefPubMedPubMedCentral Yang H, Chen S, White DG, Zhao S, McDermott P, Walker R, Meng J (2004) Characterization of multiple-antimicrobial-resistant Escherichia coli isolates from diseased chickens and swine in China. J Clin Microbiol 42:3483–3489CrossRefPubMedPubMedCentral
go back to reference Zibandeh S, Sharifiyazdi H, Asasi K, Abdi-Hachesoo B (2016) Investigation of tetracycline resistance genes in Escherichia coli isolates from broiler chickens during a rearing period in Iran. Vet Arhiv 86:565–572 Zibandeh S, Sharifiyazdi H, Asasi K, Abdi-Hachesoo B (2016) Investigation of tetracycline resistance genes in Escherichia coli isolates from broiler chickens during a rearing period in Iran. Vet Arhiv 86:565–572
Metadata
Title
Farm-level evaluation of enrofloxacin resistance in Escherichia coli isolated from broiler chickens during a rearing period
Authors
Bahman Abdi-Hachesoo
Keramat Asasi
Hassan Sharifiyazdi
Publication date
01-03-2017
Publisher
Springer London
Published in
Comparative Clinical Pathology / Issue 2/2017
Print ISSN: 1618-5641
Electronic ISSN: 1618-565X
DOI
https://doi.org/10.1007/s00580-017-2402-x

Other articles of this Issue 2/2017

Comparative Clinical Pathology 2/2017 Go to the issue