Presence of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in bulk-tank milk of bovine dairy farms in Antioquia, Colombia
DOI:
https://doi.org/10.17533/udea.rccp.v30n2a01Keywords:
antibiotic resistance, CTX-M-12a, livestock, public health, raw milkAbstract
Background: antibiotic resistance is spreading worldwide. It is important to evaluate whether foods of animal origin constitute a reservoir of resistance genes. Objective: the aim of the present study was to assess the occurrence and characterize extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae from bulk-tank milk samples of dairy farms located in Entrerríos, Antioquia (Colombia). Methods: a total of 120 randomly selected raw milk samples (one bulk-tank milk sample per dairy farm) were collected between September and October, 2013. A commercial chromogenic agar was used for screening presumptive ESBL-E. Identification of genus and species of isolates was performed with a commercial biochemical identification kit. The ESBL production was confirmed using the double disc synergy test. An antimicrobial susceptibility test was performed by the agar disc diffusion method and the automatized broth microdilution method. The ESBL-positive isolates were analyzed for the presence of bla genes by polymerase chain reaction (PCR) and sequencing. For the exploration of risk factors, information on dairy farm management practices was recorded using a questionnaire and the associations of predictors and results were tested with a logistic regression analysis. Results: the ESBL-E were isolated from 3.3% (4/120; CI 95%: 3-3.5%) of the samples. Farm size was the only factor associated with the presence of ESBL-E (OR = 11.5; CI 95%: 1.14-115.54; p = 0.038). All isolates were resistant to several antibiotics and harbored blaCTX-M-96 (alternate name CTX-M-12a) enzymes. Conclusion: although apparent frequency of ESBL-E was low, the presence of these resistant bacteria in milk may constitute a public health risk and should be further investigated.
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Resumo
Palavras chave: CTX-M-12A, gado, leite crua, resistência aos antibióticos, saúde pública.
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Adler A, Sturlesi N, Fallach N, Zilberman-Barzilai D, Hussein O, Blum SE, Klement E, Schwaber MJ, Carmeli Y. Prevalence, risk factors and transmission dynamics of ESBL-producing Enterobacteriaceae: a national survey of cattle farms in Israel, 2013. J Clin Microbiol 2015; 53(11):3515-3521.
Aljorayid A, Viau R, Castellino L, Jump R. Serratia fonticola, pathogen or bystander? A case series and review of the literature. ID Cases 2016; 5:6-8.
Amado NY, Fajardo HD, Ramírez Rueda RY, González GI. Prevalencia de betalactamasas de espectro extendido en bacilos gramnegativos de una institución de salud de Tunja (Colombia) en el año 2013. Salud Soc Uptc 2014; 1(2):54-60.
Archivo Secretaría de Asistencia Técnica Agropecuaria y Desarrollo Comunitario Municipio de Entrerríos, Antioquia, Colombia. Ciclo de vacunación contra fiebre aftosa, Federación Colombiana de Ganaderos (FEDEGAN) 2013-2.
Aust V, Knappstein K, Kunz HJ, Kaspar H, Wallmann J, Kaske M. Feeding untreated and pasteurized waste milk and bulk milk to calves: effects on calf performance, health status and antibiotic resistance of faecal bacteria. J Anim Physiol Anim Nutr (Berl) 2013; 97(6):1091-1103.
Batchelor M, Hopkins K, Threlfall EJ, Clifton-Hadley FA, Stallwood AD, Davies RH, Liebana E. blaCTX-M genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003. Antimicrob Agents Chemother 2005; 49:1319-1322.
Blanco VM, Maya Juan J, Correa Adriana, Perenguez Marcela, Muñoz Juan S, Motoa Gabriel, Pallares Christian, Rosso Fernando, Matta Lorena, Celis Yamile, Garzón Martha, Villegas María V. Prevalencia y factores de riesgo para infecciones del tracto urinario de inicio en la comunidad causadas por Escherichia coli productor de betalactamasas de espectro extendido en Colombia. Enferm Infecc Microbiol Clin 2016; 34:559-565.
Berge AC, Champagne SC, Finger RM, Sischo WM. The use of bulk tank milk samples to monitor trends in antimicrobial resistanceon dairy farms. Foodborne Pathog Dis 2007; 4(4):397-407.
Betancourt O, Scarpa C, Villagrán K. Estudio de resistencia de cepas de Staphylococcus aureus aisladas de mastitis subclínica bovina frente a cinco antibióticos en tres sectores de la IX región de Chile. Revista Científica FCV-LUZ 2003, 13(5):413-417.
Biomerieux, 2015. Una combinación ganadora para detectar resistencias. [Access date: January 13th, 2017). URL:http://www.biomerieux.com.ar/servlet/srt/bio/argentina/dynPage?doc=ARG_CLN_PRD_G_PRD_CLN_37.
Brunton LA, Reeves HE, Snow LC, Jones JR. A longitudinal field trial the impact of feeding waste milk containing antibiotic residues on the prevalence of ESBL-producing Escherichia coliin calves. Prev Vet Med 2014; 117(2):403-412.
Bush K. Proliferation and significance of clinically relevantβ-lactamases. Ann N Y Acad Sci 2013; 1277:84-90. Bush K. Bench-to-bedside review: the role of β-lactamases in antibiotic-resistant Gram-negative infections. Crit Care 2010;14(3):224.
Carattoli A. Animal reservoirs for extended spectrum betalactamase producers. Clin Micro biol Infect 2008; 14(1):117-123.
Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; nineteenth informational supplement M100-S18. Wayne, PA: Clinical and Laboratory Standards Institute; 2008.
Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; nineteenth informational supplement M100-S24. Wayne, PA: Clinical and Laboratory Standards Institute; 2014.
Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing; nineteenth informational supplement M100-S25. Wayne, PA: Clinical and Laboratory Standards Institute; 2015.
Dahmen S, Métayer V, Gay E, Madec JY, Haenni M. Characterization of ESBL-carrying plasmids and clones of Enterobacteriaceae causing cattle mastitis in France. Vet Microbiol 2013; 162:793-799.
Donado Godoy P, Castellanos R, León M, Arevalo A, Clavijo V, Bernal J, León D, Tafur MA, Byrne BA, Smith WA, Perez Gutierrez E. The establishment of the Colombian integrated program for antimicrobial resistance surveillance (COIPARS): a pilot project on poultry farms, slaughterhouses and retail market. Zoonoses and Public Health 2015; 62(1):56-58.
European Food Safety Authority (EFSA). Scientific opinion on the public health risks of bacterial strains producing extended-spectrum beta-lactamases and/or AmpCbeta-lactamases in food and food-producing animals. EFSA J 2011; 9:2322.
Ferens WA, Hovde CJ. Escherichia coliO157:H7: animal reservoir and sources of human infection. Foodborne Pathog Dis 2011; 8(4): 465-487.
Food and Drug Administration (FDA). Center for Veterinary Medicine. The judicious use of medically important antimicrobial drug in food-producing animals. Guidance for industry. April 13th, 2012.
González L, Cortés JA. Revisión sistemática de la farmacorresistencia en enterobacterias de aislamientos hospitalarios en Colombia. Biomédica 2014; 34(2):180-197.
Gerst J. Detección de la resistencia a los antibióticos con los sistemas vitek y vitek 2 de biomerieux. In: Resistencia antimicrobiana en las Américas: magnitud del problema y su contención. Organización Panamericana de la Salud. 2000.
Geser N, Stephan R, Hächler H. Occurrence and characteristics of extended-spectrum beta-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet Res 2012; 8:12.
Ghiglione B, Rodríguez MM, Herman R, Curto L, Dropa M, Bouillenne F, Kerff F, Galleni M, Charlier P, Gutkind G, SauvageE, Power P. Structural and kinetic insights into the “ceftazidimase” behavior of the extended-spectrum β-lactamase CTX-M-96.Biochem 2015; 54(32):5072-5082.
Gniadkowski M. Evolution and epidemiology of extended-spectrum beta-lactamases (ESBLs) and ESBL-producing microorganisms. Clin Microbiol Infect 2001; 7(11):597-608.
Gobernación de Antioquia, 2013. Economía. Municipio de Entrerríos. [Access date: December 1st, 2016]. URL: http://entrerrios-antioquia.gov.co/nuestromunicipio.shtml?apc=mfVereda-1-&m=f#economia
Gobernación de Antioquia, 2007. Perfil subregional norte antioqueño. [Access date: December 21st, 2016]. URL: http://www.antioquia.gov.co/antioquiav1/organismos/planeacion/descargas/perfiles/Perfil%20Subregional_Norte.pdf
Jiménez Velásquez S, Torres Higuera LD, Rodríguez Bautista JL, García Castro FE, Patiño Burbano RE. Identificación de aislamientos meticilino resistentes de Staphylococcus sp provenientes de hatos lecheros del Departamento de Cundinamarca. Rev Colomb Cienc Pecu 2013; 26(Supl).
Kreausukon K. Usage of antimicrobials on 60 dairy farms in Northern Germany and characterization of methicillin-resistant Staphylococcus aureus (MRSA) and extended spectrum betalactamases producing Escherichia coli (ESBLs-producingE. coli) isolated from bulk tank milk samples. PhD Diss Freie, Universität Berlin, Berlin, Germany. 2011.
Langford F, Burstyn U, Fisher L, Shelford J, Weary D. Feeding waste milk to calves and antibiotic resistance. 21st Annual Western Canadian Dairy Seminar, Red Deer, AB March 11-14, 2003.
Leal AL, Cortés JA, Arias G, Ovalle MV, Saavedra SY, Buitrago G, Escobar JA. Emergencia de fenotipos resistentes a cefalosporinas de tercera generación en Enterobacteriaceae causantes de infección del tracto urinario de inicio comunitario en hospitales de Colombia. Enferm Infecc Microbiol Clin 2013; 31(5):298-303.
Leedom J. Comparing the food safety record of pasteurized and raw milk products. [Access date: December 21st, 2016]. URL: http://www.foodpoisonjournal.com/food-poisoning-information/comparing-the-food-safety-record-of-pasteurized-and-raw-milk-products/#.V7Yrfyh97IW
Lejeune JT, Rajala Schultz PJ. Food safety: unpasteurized milk: a continued public health threat. Clin Infect Dis 2009; 48(1):93-100.
Leverstein van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect 2011; 17(6):873-880.
Locatelli C, Scaccabarozzi L, Pisoni G. CTX-M1 ESBL-Producing Klebsiella pneumoniae subsp pneumoniae Isolated from Cases of Bovine Mastitis. Clin Microbiol 2010; 48(10):3822-3823.
Machado Alba JE, González Santos DM. Dispensing antibiotics to outpatients in a Colombian population. Rev salud pública 2009; 11(5):734-744.
Mantilla Anaya JR, Barreto Hernández E, Reguero Reza MT, Velandia Rodríguez DA. Identifying cefotaximase genes in Enterobacteriaceae hospital isolates by PCR-SSCP. Rev Colomb Biotecnol 2009; 11(2):57-65.
Mesa RJ, Blanc V, Blanch AR, Cortés P, González JJ, Lavilla S, Miró E, Muniesa M, Saco M, Tórtola MT, Mirelis B, Coll P, Llagostera M, Prats G, Navarro FJ. Extended-spectrum b-lactamase-producing Enterobacteriaceae in different environments (humans, food, animal farms and sewage). Antimicrob Chemothe 2006; 58:211-215.
Ministerio de Agricultura y Desarrollo Rural de Colombia. Resolución 000017: Sistema de pago de leche cruda al productor. Bogotá, Colombia. 2012.
Ministerio de la Protección Social. Decreto 1880 del 27 de mayo de 2011. Bogotá, Colombia. Ministerio de la Protección Social. Decreto 616 del 28 de febrero de 2006. Bogotá, Colombia.
NCBI (National Center for Biotechnology Information) (2005). CTX-M-12a enzyme Klebsiella pneumoniae. GenBank:CAG28417.1. [Access date: December 1st, 2016]. URL: http://www.ncbi.nlm.nih.gov/protein/47109376.
NCBI (National Center for Biotechnology Information) (2015). Klebsiella pneumonia estrain K-837 beta-lactamase CTX-M-96 (blaCTX-M) gene, blaCTX-M-96 allele, complete cds. GenBank:KR811026.1. [Access date: April 20th, 2016]. URL: http://www.ncbi.nlm.nih.gov/nucleotide/940376853?report=genbank&log$=nucltop&blast_rank=1&RID=C1WP1YKG01R
Nóbrega DB, Guiduce MVS, Guimarães FF, Ribol DF. Molecular epidemiology and extended-spectrum β-lactamases production of Klebsiella pneumoniae isolated from three dairy herds. Pesq Vet Bras 2013 ; 33(7):855-859.
Odenthal S, Akineden Ö, Usleber E. Extended-spectrum betalactamase (ESBL)-produzierende Enterobacteriaceaein Anlieferungsmiclh aus hessischen Milchviehbetrieben. In: 54. Arbeitstagung der Deutsche Veterinärmedizinische Gesellschaft (DVG) Arbeitsgebiet Lebensmittelhygiene,Garmisch-Partenkirchen (Alemania), Septimebre 24-27 de 2013.
Odenthal S, Akineden Ö, Usleber E. Extended spectrumβ-lactamase producing Enterobacteriaceae in bulk tank milk from German dairy farms. Int J Food Microbiol 2016; 5:238:278.
Ohnishi AT, Okatani H, Esaki K, Harada T, Sawada M, Murakami K, Marumo Y, Kato R, Sato K, Shimura N, Hatanaka, Takahashi T. Herd prevalence of Enterobacteriaceae producing CTX-M type and CMY-2 b-lactamases among Japanese dairy farms. J App Microbiol 2013; 115:288-289.
Ohnishi M, Okatani A T, Harada K, Sawada T, Marumo K, Murakami M, Sato R, Esaki H, Shimura K, Kato H, Uchida N, Takahashid T. Genetic characteristics of CTX-M-type extended-spectrum-β-lactamase (ESBL)-producing Enterobacteriaceae involved in mastitis cases on Japanese dairy farms, 2007 to 2011. J Clin Microbiol 2013; 51(9): 3117-3122.
Oliver SP, Murinda SE. Antimicrobial resistance of mastitis pathogens. Vet Clin North Am Food Anim Pract 2012; 28(2):165-185.Paterson DL, Bonomo RA. Extended-spectrum beta-lactamases: a clinical update. Clin Microbiol Rev 2005; 18:657-686.
Pitout JDD, Thomson KS, Hanson ND, Ehrhardt AF, Moland ES, Sanders CC. B-lactamases responsible for resistance to expanded spectrum cephalosporins in Klebsiella pneumoniae, Escherichia coli, and Proteus mirabilis isolates recovered in South Africa. Antimicrob Agents Chemother 1998; 42:1350-1354.
Puerta García A, Mateos Rodríguez F. Enterobacterias. Medicine 2010; 10(51):3426-3431.
Randall L, Heinrich K, Horton R, Brunton L, Sharman M, Bailey Horne V, Sharma M, McLaren I, Coldham N, Teale C, Jones J. Detection of antibiotic residues and association of cefquinome residues with the occurrence of Extended-Spectrum β-Lactamase(ESBL)-producing bacteria in waste milk samples from dairy farms in England and Wales in 2011. Res Vet Sci 2014; 96:15-24.
Rasheed MU, Thajuddin N, Ahamed P, Teklemariam Z, Jamil K. Antimicrobial drug resistance in strains of escherichia coli isolated from food sources. Rev Inst Med Trop Sao Paulo 2014; 56(4):341-346.
Reist M, Geser N, Hachler H, Scharrer S, Stephan R. ESBL-producing Enterobacteriaceae: occurrence, risk factors for fecal carriage and strain traits in the Swiss slaughter cattle population younger than 2 years sampled at abattoir level. PLOS ONE 2013;8(8):71725.
Ruiz Romero RA. Mastitis bacteriana en ganado bovino: etiología y técnicas de diagnóstico en el laboratorio. [Access date: November 22nd, 2015]. URL: Disponible en: http://www.ammveb.net/articulos/Mastitis_bacteriana.pdf.
Ruiz SJ, Montealegre MC, Ruiz Garbajosa P, Correa A, Briceño DF, Martinez E, Rosso F, Muñoz M, Quinn JP, Canton R, Villegas MV. First characterization of CTX-M-15-producing Escherichia coli ST131 and ST405 clones causing community-onset infections in South America. J Clin Microbiol 2011; 49(5):1993-1996.
Randall L, Heinrich K, Horton R, Brunton L, Sharman M, Bailey-Horne V, Sharma M, McLaren I, Coldham N, Teale C, Jones J. Detection of antibiotic residues and association of cefquinome residues with the occurrence of extended- spectrum b-lactamase (ESBL)-producing bacteria in waste milk samples from dairy farms in England and Wales in 2011. Res Vet Sci 2014; 96:15-24.
Rybak MJ, Pharm D. Resistance to antimicrobial agents: an update. Sup Pharmacotherapy 2004; 24(12).
Sánchez L, Ríos R, Máttar S. Detection of extended spectrum beta-lactamases(ESBL) in Escherichia coli and Klebsiella pneumoniae isolated in a clinic in Villavicencio, Colombia. Infect 2008; 12(3): 193-200.
Sanders CC, Peyret M, Moland ES, Cavalieri SJ, Shubert C, Thomson KS, Boeufgras JM, Sanders WE. Potential impact of the VITEK 2 system and the advanced expert system on the clinical laboratory of a university-based hospital. J Clin Microbiol 2001; 39:2379-2385.
Schmid A, Hörmansdorfer S, Messelhäusser U, Käsbohrer A, Sauter-Louis C, Mansfeldc R. Prevalence of extended-spectrum -lactamase-producing Escherichia coli on bavarian dairy and beef cattle farms. App Environment Microbiol 2013; 79(9):3027-3032.
Schwaber MJ, Navon Venezia S, Chmelnitsky I, Leavitt A, Schwartz D, Carmeli Y. Utility of the VITEK 2 advanced expert system for identification of extended-spectrum β-lactamase production in Enterobacter spp. J Clin Microbiol 2006; 44(1):241-243.
Skočková A, Bogdanovičová K, Koláčková I, Karpíšková R. Antimicrobial-resistant and extended-spectrum β-lactamase-producing Escherichia coli in raw cow’s milk. J Food Protect 2015; 2(234):72-77(6).
Smet A, Martel A, Persoons D, Dewulf J, Heyndrickx M, Herman L, Haesebrouck F, Butaye P. Broad-spectrum b-lactamasesamong Enterobacteriaceae of animal origin: molecular aspects, mobility and impact on public health. FEMS Microbiol Rev 2010; 34:295-316.
Snow LC, Warner RG, Cheney T, Wearing H, Stokes M, Harris K, Teale CJ, Coldham NG. Risk factors associated with extended spectrum beta-lactamase E. coli(CTX-M) on dairy farms in North West England and North Wales. Prev Vet Med 2012;106(3,4):225-234.
StataCorp. 2011. Stata: Release 12. Statistical Software Release 12ed. StataCorp LP, College Station, Texas.
Sudarwanto M, Akineden Ö, Odenthal S, Gross M, Usleber E. Extended-spectrum b-Lactamase (ESBL)-producing Klebsiella pneumoniaein bulk tank milk from dairy farms in Indonesia. Foodborne Path Dis 2015; 12(7):585-590.
Timofte D, Maciuca IE, Evans NJ, Williams H, Wattret A, Fick JC, Williams NJ. Detection and molecular characterization of Escherichia coliCTX-M-15 and Klebsiella pneumoniaeSHV-12β-lactamases from bovine mastitis isolates in the United Kingdom. Antimicrob Agents Chemother 2014; 58(2):789-794.
Toro C. Protocolo de toma de muestras de leche: laboratorio de calidad e inocuidad de leche cruda. Facultad de Ciencias Agrarias, Universidad de Antioquia, Colombia. Versión 1 julio 10 de 2012.
Vacca CP, Niño CY, Reveiz L. Restricción de la venta de antibióticos en farmacias de Bogotá, Colombia: estudio descriptivo. Rev Panam Salud Pública 2011; 30(6):586-591.
Vanegas López MC, Moreno J E, Ramos Rueda V, Chirivi JS, Garzón A, Arévalo SA, Martínez MF, Gardeazábal PA, Baquero C. Methicillin-resistant Staphylococcus aureus (MRSA) isolated from Colombian foods. BIO 2012; 2:61-67.
Verraes C, Van Boxstael S, Van Meervenne E, Van Coillie E, Butaye P, Catry B, de Schaetzen MA, Van Huffel X, Imberechts H, Dierick K, Daube G, Saegerman C, De Block J, Dewulf J, Herman L. Antimicrobial resistance in the food chain: a review. Int J Environ Res Public Health 2013; 10(7): 2643-2669.
Villegas MV, Correa A, Perez F, Zuluaga T, Radice M, Gutkind G, Casellas JM, Ayala J, Lolans K, Quinn John P. CTX-M-12 β-Lactamase in a Klebsiella pneumoniae Clinical Isolate in Colombia. Antimicrob Agents Chemother 2004; 48(2):629-631.
Villegas MV; Guzmán Blanco M; Sifuentes Osornio J, Rossi F. Increasing prevalence of extended-spectrum-betalactamase among Gram-negative bacilli in Latin America – 2008 update from the study for monitoring antimicrobial resistance trends (SMART). Braz J Infect Dis 2011; 15(1):34-39.
Walsh C, Fanning S. Antimicrobial resistance in foodborne pathogens--a cause for concern Curr Drug Targets 2008; 9(9):808-815.
Wegener HC. Antibiotic resistance—linking human and animal health. In: Institute of Medicine (US). Improving food safetythrough a one health approach: workshop summary. Washington (DC): National Academies Press (US); 2012. A15. [Access date: December 1st, 2016]. URL: http://www.ncbi.nlm.nih.gov/books/NBK114485/
Woodford N, Fagan EJ, Ellington MJ. Multiplex PCR for rapid detection of genes encoding CTX-M extended spectrum B- lactamases. J Antimicrob Chemother 2006; 57:154-155.
Woodford N. Rapid characterization of beta lactamases by multiplex PCR. Methods Mol Biol 2010; 642:181-192.
Wooldridge M. Evidence for the circulation of antimicrobial-resistant strains and genes in nature and especially betweenhumans and animals. Rev Sci Tech 2008; 31(1):231-247.
World Health Organization –WHO (2001): Global Strategy for Containment of Antimicrobial Resistance. Rev Panam Salud Pública vol.10 n.4 Washington Oct. 2001
Xian-Zhi L, Manisha M, Shiva G, Lateef A. Β- lactam resistance and β- lactamases in bacteria of animal origin. Vet Microbiol 2007; 121:197-214.
Zhao WH, Hu ZQ. Epidemiology and genetics of CTX-Mextended-spectrum β-lactamases in Gram-negative bacteria. Critical Rev Microbiol 2013; 39(1):79-101.
Zeinhoma, Mohamed MA, Abdel-Latefb, Gihan K. Public health risk of some milk borne pathogens. Beni-Suef University J Basic App Scienc 2014; 3(3):209-215.
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