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Antimicrobial (ESBL) resistance genes in faecal E. coli of calves fed waste milk with antimicrobial residues

Published online by Cambridge University Press:  30 August 2022

Manuel Cardoso ,
Inês Prata ,
Inês Rebelo ,
Telmo Nunes ,
Ana Pires ,
Carla Carneiro  and
Ricardo Bexiga
Manuel Cardoso
Affiliation:
Faculty of Veterinary Medicine, CIISA – Centre for Interdisciplinary Research in Animal Health, University of Lisbon, Lisbon, Portugal Faculty of Veterinary Medicine, Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), University of Lisbon, Lisbon, Portugal
Inês Prata
Affiliation:
Faculty of Veterinary Medicine, CIISA – Centre for Interdisciplinary Research in Animal Health, University of Lisbon, Lisbon, Portugal Faculty of Veterinary Medicine, Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), University of Lisbon, Lisbon, Portugal HVME – Hospital Veterinário Muralha de Évora, Évora, Portugal
Inês Rebelo
Affiliation:
Faculty of Veterinary Medicine, CIISA – Centre for Interdisciplinary Research in Animal Health, University of Lisbon, Lisbon, Portugal Faculty of Veterinary Medicine, Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), University of Lisbon, Lisbon, Portugal
Telmo Nunes
Affiliation:
Faculty of Veterinary Medicine, CIISA – Centre for Interdisciplinary Research in Animal Health, University of Lisbon, Lisbon, Portugal Faculty of Veterinary Medicine, Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), University of Lisbon, Lisbon, Portugal
Ana Pires
Affiliation:
Faculty of Veterinary Medicine, CIISA – Centre for Interdisciplinary Research in Animal Health, University of Lisbon, Lisbon, Portugal Faculty of Veterinary Medicine, Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), University of Lisbon, Lisbon, Portugal
Carla Carneiro
Affiliation:
Faculty of Veterinary Medicine, CIISA – Centre for Interdisciplinary Research in Animal Health, University of Lisbon, Lisbon, Portugal Faculty of Veterinary Medicine, Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), University of Lisbon, Lisbon, Portugal
Ricardo Bexiga*
Affiliation:
Faculty of Veterinary Medicine, CIISA – Centre for Interdisciplinary Research in Animal Health, University of Lisbon, Lisbon, Portugal Faculty of Veterinary Medicine, Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), University of Lisbon, Lisbon, Portugal
*
Author for correspondence: Ricardo Bexiga, Email: [email protected]
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Abstract

This research paper aimed to evaluate the association between feeding waste milk to calves and the occurrence of antimicrobial multi-resistance by extended spectrum β-lactamase (ESBL) enzymes through determining their production by E. coli isolates from 32 dairy farms. Among β-lactamase enzymes, ESBL provide resistance to a wide variety of β-lactam antimicrobials including penicillin and 2nd, 3rd and 4th generation cephalosporins. Feeding waste milk to calves has been observed to lead to increased antimicrobial resistance in faecal isolates of calves. In each farm included in this study, faecal samples were collected from the rectum of five healthy calves in the first month of life and pooled into a single container. Five isolates from each pool were selected and confirmed to be E. coli by amplification of the 16S rRNA gene. ESBL production was confirmed phenotypically on 148 isolates from 31 farms by use of the double-disk synergy test. Genotypic confirmation of ESBL production was performed by PCR for the genes blaCTX-M-1, −2, −8, −9 and blaCMY-2. A questionnaire was also performed and a mixed logistic regression model was used to identify risk factors for the occurrence of antimicrobial resistance. A negative binomial regression model was also used, in order to assess whether there was any association between certain farm management practices and the number of ESBL-producing E. coli isolates from each farm. Phenotypic confirmation of ESBL production was obtained on 40 E. coli isolates from 15 farms (48.4%), whereas genotypic confirmation was obtained on 55 isolates from 20 farms (64.5%). The use of three or more different intramammary antimicrobials to treat mastitis within the previous year significantly impacted the number of ESBL-producing E. coli isolates; on farms that did so, there were more isolates in which ESBL-producing E. coli was present, when compared to farms that had used less formulations within the same time span.

Keywords

AntimicrobialcalvesE. coliESBLwaste milk
Type
Research Article
Information
Journal of Dairy Research , Volume 89 , Issue 3 , August 2022 , pp. 259 - 264
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of Hannah Dairy Research Foundation

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References

Ali, T, Rahman, S, Zhang, L, Shahid, M, Zhang, S, Liu, G, Gao, J and Han, B (2016) ESBL-producing Escherichia coli from cows suffering mastitis in China contain clinical class 1 integrons with CTX-M linked to IS CR1. Frontiers in Microbiology 7, 1931.CrossRefGoogle Scholar
Aust, V, Knappstein, K, Kunz, H-J, Kaspar, H, Wallmann, J and Kaske, M (2013) Feeding untreated and pasteurized waste milk and bulk milk to calves: effects on calf performance, health status and antibiotic resistance of faecal bacteria. Journal of Animal Physiology and Animal Nutrition 97, 1091–1103.CrossRefGoogle ScholarPubMed
Beneragama, N, Iwasaki, M, Lateef, SA, Yamashiro, T, Ihara, I and Umetsu, K (2013) The survival of multidrug-resistant bacteria in thermophilic and mesophilic anaerobic co-digestion of dairy manure and waste milk. Animal Science Journal 84, 426–433.CrossRefGoogle ScholarPubMed
Bevan, ER, Jones, AM and Hawkey, PM (2017) Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. Journal of Antimicrobial Chemotherapy 72, 2145–2155.Google ScholarPubMed
Brunton, LA, Duncan, D, Coldham, NG, Snow, LC and Jones, JR (2012) A survey of antimicrobial usage on dairy farms and waste milk feeding practices in England and Wales. Veterinary Record 171, 296.CrossRefGoogle ScholarPubMed
Brunton, LA, Reeves, HE, Snow, LC and Jones, JR (2014) A longitudinal field trial assessing the impact of feeding waste milk containing antibiotic residues on the prevalence of ESBL-producing Escherichia coli in calves. Preventive Veterinary Medicine 117, 403–412.CrossRefGoogle ScholarPubMed
Chen, YMM, Wright, PJ, Lee, CS and Browning, GF (2003) Uropathogenic virulence factors in isolates of Escherichia coli from clinical cases of canine pyometra and feces of healthy bitches. Veterinary Microbiology 94, 57–69.CrossRefGoogle ScholarPubMed
Clinical and Laboratory Standards Institute (CLSI) (2017) Performance Standards for Antimicrobial Susceptibility Testing, 27th Edn., Pennsylvania, USA: Clinical and Laboratory Standards Institute.Google Scholar
D'Andrea, MM, Arena, F, Pallecchi, L and Rossolini, GM (2013) CTX-M-type β-lactamases: a successful story of antibiotic resistance. International Journal of Medical Microbiology 303, 305–317.CrossRefGoogle ScholarPubMed
Davis, MA, Sischo, WM, Jones, LP, Moore, DA, Ahmed, S, Short, DM and Besser, TE (2015) Recent emergence of Escherichia coli with cephalosporin resistance conferred by bla CTX−M on Washington state dairy farms. Applied and Environmental Microbiology 81, 4403–4410.CrossRefGoogle Scholar
Duse, A, Waller, KP, Emanuelson, U, Unnerstad, HE, Persson, Y and Bengtsson, B (2013) Farming practices in Sweden related to feeding milk and colostrum from cows treated with antimicrobials to dairy calves. Acta Veterinaria Scandinavica 55, 49.CrossRefGoogle ScholarPubMed
EFSA Panel on Biological Hazards (BIOHAZ) (2017) Risk for the development of Antimicrobial Resistance (AMR) due to feeding of calves with milk containing residues of antibiotics. EFSA Journal 15, 4665.Google Scholar
Geser, N, Stephan, R and Hächler, H (2012) Occurrence and characteristics of extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Veterinary Research 8, 21. doi: 10.1186/1746-6148-8-2.CrossRefGoogle ScholarPubMed
Gullberg, E, Cao, S, Berg, OG, Ilbäck, C, Sandegren, L, Hughes, D and Andersson, DI (2011) Selection of resistant bacteria at very Low antibiotic concentrations. PLoS Pathogens 7, e1002158.CrossRefGoogle ScholarPubMed
Jorgensen, MA, Hoffman, PC and Nytes, AJ (2006) A field survey of on-farm milk pasteurization efficacy. The Professional Animal Scientist 22, 472–476.CrossRefGoogle Scholar
Kuipers, A, Koops, WJ and Wemmenhove, H (2016) Antibiotic use in dairy herds in the Netherlands from 2005 to 2012. Journal of Dairy Science 99, 1632–1648.CrossRefGoogle ScholarPubMed
Lago, A, Godden, SM, Bey, R, Ruegg, PL and Leslie, K (2011) The selective treatment of clinical mastitis based on on-farm culture results: I. Effects on antibiotic use, milk withholding time, and short-term clinical and bacteriological outcomes. Journal of Dairy Science 94, 4441–4456.CrossRefGoogle ScholarPubMed
Leão, C, Botelho, A, Martins, E, Aguiar, C, Rebelo, I, Nunes, T and Bexiga, R (2017) Presence of Mycobacterium avium subs. paratuberculosis DNA in milk used to feed calves in Portugal. Journal of Dairy Research 84, 124–127.CrossRefGoogle ScholarPubMed
Lee, HJ, Khan, MA, Lee, WS, Yang, SH, Kim, SB, Ki, KS, Kim, HS, Ha, JK and Choi, YJ (2009) Influence of equalizing the gross composition of milk replacer to that of whole milk on the performance of Holstein calves. Journal of Animal Science 87, 1129–1137.CrossRefGoogle ScholarPubMed
Madec, J-Y, Haenni, M, Nordmann, P and Poirel, L (2017) Extended-spectrum β-lactamase/AmpC- and carbapenemase-producing Enterobacteriaceae in animals: a threat for humans? Clinical Microbiology and Infection 23, 826–833.CrossRefGoogle ScholarPubMed
Maynou, G, Migura-Garcia, L, Chester-Jones, H, Ziegler, D, Bach, A and Terré, M (2017) Effects of feeding pasteurized waste milk to dairy calves on phenotypes and genotypes of antimicrobial resistance in fecal Escherichia coli isolates before and after weaning. Journal of Dairy Science 100, 7967–7979.CrossRefGoogle ScholarPubMed
McDanel, J, Schweizer, M, Crabb, V, Nelson, R, Samore, M, Khader, K, Blevins, AE, Diekema, D, Chiang, H-Y, Nair, R and Perencevich, E (2017) Incidence of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli and Klebsiella infections in the United States: a systematic literature review. Infection Control & Hospital Epidemiology 38, 1209–1215.CrossRefGoogle ScholarPubMed
Odenthal, S, Akineden, Ö and Usleber, E (2016) Extended-spectrum β-lactamase producing Enterobacteriaceae in bulk tank milk from German dairy farms. International Journal of Food Microbiology 238, 72–78.CrossRefGoogle ScholarPubMed
Pereira, RVV, Siler, JD, Bicalho, RC and Warnick, LD (2014) In vivo selection of resistant E. coli after ingestion of milk with added drug residues. PLoS ONE 9, e115223.CrossRefGoogle ScholarPubMed
Quinn, PJ, Carter, ME, Carter, GR and Ricketts, SW (1994) Enterobacteriaceae. Clinical Veterinary Microbiology, 1st Edn. Maryland Heights, USA: Mosby, pp. 209–236.Google Scholar
Seiffert, SN, Hilty, M, Perreten, V and Endimiani, A (2013) Extended-spectrum cephalosporin-resistant Gram-negative organisms in livestock: an emerging problem for human health? Drug Resistance Updates 16, 22–45.CrossRefGoogle ScholarPubMed
Shahid, M, Al-Mahmeed, A, Murtadha, MM, Qareeballa, A, Eltahir, MA, Tabbara, KS, Ismaeel, AY, Dar, FK, Giha, HA, Bindayna, KM and Bindayna, KM (2014) Characterization of cephalosporin-resistant clinical Enterobacteriaceae for CTX-M ESBLs in Bahrain. Asian Pacific Journal of Tropical Medicine 7, S212–S216.CrossRefGoogle Scholar
Shin, SW, Jung, M, Won, HG, Belaynehe, KM, Yoon, IJ and Yoo, HS (2017) Characteristics of transmissible CTX-M- and CMY-type β-lactamase-producing Escherichia coli isolates collected from pig and chicken farms in South Korea. Journal of Microbiology and Biotechnology 27, 1716–1723.CrossRefGoogle ScholarPubMed
Vasseur, E, Borderas, F, Cue, RI, Lefebvre, D, Pellerin, D, Rushen, J, Wade, KM and de Passillé, AM (2010) A survey of dairy calf management practices in Canada that affect animal welfare. Journal of Dairy Science 93, 1307–1316.CrossRefGoogle ScholarPubMed
Winokur, PL, Vonstein, DL, Hoffman, LJ, Uhlenhopp, EK and Doern, GV (2001) Evidence for transfer of CMY-2 AmpC β-lactamase plasmids between Escherichia coli and Salmonella isolates from food animals and humans. Antimicrobial Agents and Chemotherapy 45, 2716–2722.CrossRefGoogle ScholarPubMed
Xia, S, Fan, X, Huang, Z, Xia, L, Xiao, M, Chen, R, Xu, Y and Zhuo, C (2014) Dominance of CTX-M-type extended-spectrum β-lactamase (ESBL)-producing Escherichia coli isolated from patients with community-onset and hospital-onset infection in China. PLoS ONE 9, 100707.CrossRefGoogle ScholarPubMed
Yan, J-J, Hong, C-Y, Ko, W-C, Chen, Y-J, Tsai, S-H, Chuang, C-L and Wu, J-J (2004) Dissemination of blaCMY-2 among Escherichia coli isolates from food animals, retail ground meats, and humans in southern Taiwan. Antimicrobial Agents and Chemotherapy 48, 1353–1356.CrossRefGoogle ScholarPubMed
Youngquist, CP, Mitchell, SM and Cogger, CG (2016) Fate of antibiotics and antibiotic resistance during digestion and composting: a review. Journal of Environmental Quality 45, 537–545.CrossRefGoogle ScholarPubMed
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