Antimicrobial resistance in ovine production: maternal-descendant similarities in Coliforms and Enterococcus spp.
DOI:
https://doi.org/10.1590/1809-6891v26e-80984EAbstract
Abstract: Reports are scarce on the increase of antimicrobial resistance and the transfer of resistance from progenitor to progeny in production animals. Given this scenario, it is essential to understand how bacterial resistance mechanisms spread in ovine culture. The aim of this study is to identify the occurrence of antimicrobial resistance in Coliforms and Presumptive (P.) Enterococcus spp. present in progenitors and their descendants during the birth and weaning periods. Twenty-six pregnant ewes (Ovis aries) with an average body weight of 40 ± 2.0 kg and a body condition score of 3.5 ± 0.3 were used. Blood and fecal samples were collected from both dams and offspring for complete blood count analysis and antimicrobial susceptibility testing (AST). The AST was performed against the antibiotics penicillin, tetracycline, enrofloxacin, ampicillin, streptomycin, erythromycin and ceftiofur, targeting the bacterial genera Coliforms and Enterococcus spp. The results have shown that in the birth and weaning period, the progenitor and progeny had similarity to the susceptibility tests. Antibiotics such as erythromycin and penicillin presented high resistance levels. Furthermore, ceftiofur, an antibiotic not used in sheep farming, showed isolated cases of resistance. Although these occurrences were low and not widespread, the findings highlight the potential impact of pre-existing bacterial resistance mechanisms on the effectiveness of newer antimicrobials. It is concluded that there is a maternal-descendant similarity between both bacteria. The antibiotics ceftiofur, tetracycline, streptomycin, ampicillin and enrofloxacin showed lower resistance; erythromycin and penicillin showed higher resistance. Specific studies are recommended for each ovine production to control the resistance offered by erythromycin and penicillin.
Key-words: Antibiotic; ewe; lamb; sensitivity; susceptibility.
Downloads
References
World Health Organization (WHO). Antimicrobial Resistance: Global Report on Surveillance. Geneva: World Health Organization; 2014. Available from: https://apps.who.int/iris/handle/10665/112642 [Accessed 10 July 2024]
Office International des Epizooties (OIE). Resistência antimicrobiana. Disponível em: https://www.woah.org/en/what-we-do/global-initiatives/antimicrobial-resistance/. [Accessed 01 July 2024].
Alcock BP, Raphenya AR., Lau TTY, et al. CARD: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 2020;48 (D1): D517-D525. https://doi.org/10.1093/nar/gkz935
Zhang T, Niu G, Boonyayatra S, Pichpol D. Antimicrobial resistance profiles and genes in Streptococcus uberis associated with bovine mTSAitis in Thailand. Front Vet Sci. 2021;8:705338. https://doi.org/10.3389/fvets.2021.705338
Melo MR, Almeida E, Hofer E, et al. Antibiotic resistance of Vibrio parahaemolyticus isolated from pond-reared Litopenaeus vannamei marketed in Natal, Brazil. Braz J Microbiol. 2011;42(4):1463-1469. https://doi.org/10.1590/S1517-83822011000400032
Grabowski Ł, Gaffke L, Pierzynowska K, et al. Enrofloxacin: the ruthless killer of eukaryotic cells or the lTSA hope in the fight against bacterial infections? Int J Mol Sci. 2022;23(7):3648. https://doi.org/10.3390/ijms23073648
Riboldi GP, Frazzon J, d'Azevedo PA, Frazzon AP. Antimicrobial resistance profile of Enterococcus spp. isolated from food in Southern Brazil. Braz J Microbiol. 2009;40(1):125-128. https://doi.org/10.1590/S1517-83822009000100021
Kaszanyitzky ÉJ, Tenk M, Ghidán Á, Fehérvári GY, Papp M. Antimicrobial susceptibility of enterococci strains isolated from slaughter animals on the data of Hungarian resistance monitoring system from 2001 to 2004. Int J Food Microbiol. 2007;115:119–123. https://doi.org/10.1016/j.ijfoodmicro.2006.10.004
López M, Sáenz Y, Rojo-Bezares B, et al. Detection of vanA and vanB2-containing enterococci from food samples in Spain, including Enterococcus faecium strains of CC17 and the new singleton ST425. Int J Food Microbiol. 2009;133:172-178. https://doi.org/10.1016/j.ijfoodmicro.2009.05.020
Acha PN, Szyfres B. Zoonosis y enfermedades transmisibles comunes al hombre y a los animales: Volumen 1: bacteriosis and micosis. 3rd ed. Washington: Organização Panamericana de la Salud; 2001. 398 p. (Publicación Científica y Técnica, 580). https://doi.org/10.1590/S0102-311X2005000300038
Guo W, Bi SS, Wang WW, Zhou M, Neves ALA, Degen AA, Guan LL, Long RJ. Maternal rumen and milk microbiota shape the establishment of early-life rumen microbiota in grazing yak calves. J Dairy Sci. 2023;106(3):2054–2070. https://doi.org/10.3168/jds.2022-22655
Messman RD, Lemley CO. Bovine neonatal microbiome origins: A review of proposed microbial community presence from conception to colostrum. Transl Anim Sci. 2023;7:txad057. https://doi.org/10.1093/tas/txad057
Perez-Muñoz ME, Arrieta MC, Ramer-Tait AE, Walter J. A critical assessment of the "sterile womb" and "in utero colonization" hypotheses: implications for research. Microbiome. 2017;5:48. https://doi.org/10.1186/s40168-017-0268-4
Rackaityte E, Halkias J, Fukui EM, Mendoza VF, Hayzelden C, Crawford ED, et al. Viable bacterial colonization is highly limited in the human intestine in utero. Nat Med. 2020;26(4):599–607. https://doi.org/10.1038/s41591-020-0761-3
AOAC, Association of Official Analytical Chemists – International. Official Methods of Analysis. 23st ed. Gaithersburg, MD, USA; 2023. https://www.aoac.org/official-methods-of-analysis/
Mertens DR. Measuring fiber and its effectiveness in ruminant diets. US Dairy Forage Research Center, USDA-ARS, Madison, WI; 2002. www.nutritionmodels.com/papers/MertensPNC2002.pdf
EUCTSA, The European Committee on Antimicrobial Susceptibility Testing, 2018. Available from: https://www.eucTSA.org. Accessed on: 01 july 2024
CLSI, Clinical and Laboratory Standards Institute, Inc. [Internet]. 2018 [cited 2024 Jul 01]. Available from: https://clsi.org/
Sampaio, IBM. Estatística aplicada à experimentação animal. Fundação de Ensino e Pesquisa em Medicina Veterinária e Zootecnia. 3.ed. Belo Horizonte – MG, 2002, 265p.
Stinson LF, Boyce MC, Payne MS, Keelan JA. The not so sterile womb: evidence that the human fetus is exposed to bacteria before birth. Front Microbiol. 2019;10:1124. https://doi.org/10.3389/fmicb.2019.01124
Salter SJ, Cox MJ, Turek EM, et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 2014;12:87. https://doi.org/10.1186/s12915-014-0087-x.
Winters AD, Romero R, Greenberg JM, et al. Does the amniotic fluid of mice contain a viable microbiota? Front Immunol. 2022;13:820366. https://doi.org/10.3389/fimmu.2022.820366.
Al-Balawi M, Morsy FM. Prenatal versus postnatal initial colonization of healthy neonates' colon ecosystem by the Enterobacterium Escherichia coli. Microbiol Spectr. 2021;9(2):e0050621. https://doi.org/10.1128/Spectrum.00379-21
Martínez I, Maldonado-Gomez MX, et al. Experimental assessment of the importance of colonization history in shaping the gut microbiota in early life. eLife. 2018;7:e36521. https://doi.org/10.7554/eLife.36521
Mancuso G, Midiri A, Gerace E, Biondo C. Bacterial Antibiotic Resistance: The Most Critical Pathogens. Pathogens. 2021 Oct 12;10(10):1310. https://doi.org/10.3390/pathogens10101310
Kristich CJ, Rice LB, Arias CA. Enterococcal Infection—Treatment and Antibiotic Resistance. 2014 Feb 6. In: Gilmore MS, Clewell DB, Ike Y, et al., editors. Enterococci: From Commensals to Leading Causes of Drug Resistant Infection [Internet]. Boston: Massachusetts Eye and Ear Infirmary; 2014-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK190420/
Macpherson AJ, de Agüero MG, Ganal-Vonarburg SC. How nutrition and the maternal microbiota shape the neonatal immune system. Nat Rev Immunol. 2017;17(8):508-517. https://doi.org/10.1038/nri.2017.58
Maqsood R, Rodgers R, Rodriguez C. Discordant transmission of bacteria and viruses from mothers to babies at birth. Microbiome. 2019;7:156. https://doi.org/0.1186/s40168-019-0766-7
Haulisah NA, Hassan L, Bejo SK, et al. High levels of antibiotic resistance in isolates from diseased livestock. Front Vet Sci. 2021;8:652351. https://doi.org/10.3389/fvets.2021.652351.
De Jong A, Bywater R, Butty P, et al. A pan-European survey of antimicrobial susceptibility towards human-use antimicrobial drugs among zoonotic and commensal enteric bacteria isolated from healthy food-producing animals. J Antimicrob Chemother. 2009;63(4):733-744. https://doi.org/10.1093/jac/dkp012
O’Neill L, García Manzanilla E, Ekhlas D, et al. Antimicrobial resistance in commensal Escherichia coli of the porcine gTSArointestinal tract. Antibiotics (Basel). 2023;12:1616. https://doi.org/10.3390/antibiotics12111616
Burow E, Rostalski A, et al. Antibiotic resistance in Coliforms from pigs from birth to slaughter and its association with antibiotic treatment. Prev Vet Med. 2019;165:52-62. https://doi.org/10.1016/j.prevetmed.2019.02.008
Chen F, Qingqing W, Wei-Dong W, Yan-Dong. Microbiota intestinal: um moderador integral em saúde e doença. Front Microbiol. 2018;9:151. https://doi.org/10.3389/fmicb.2018.00151
Seale, J., Millar, M., 2014. Perinatal vertical transmission of antibiotic-resistant bacteria: a systematic review and proposed research strategy. BJOG: An International Journal of Obstetrics and Gynaecology, 121, 923-928. https://doi.org/10.1111/1471-0528.12746
Holmes AH, Moore LS, Sundsfjord A, et al. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet. 2016;387:176–187. https://doi.org/10.1016/S0140-6736(15)00473-0
Murray LM, Hayes A, Snape J, et al. Co-selection for antibiotic resistance by environmental contaminants. npj Antimicrob Resist. 2024;2:9. https://doi.org/10.1038/s44259-024-00026-7
Goh YX, Anupoju SMB, Nguyen A, Zhang H, Ponder M, Krometis LA, Pruden A, Liao J. Evidence of horizontal gene transfer and environmental selection impacting antibiotic resistance evolution in soil-dwelling Listeria. Nat Commun. 2024;15:54459. https://doi.org/10.1038/s41467-024-54459-9
Hollenbeck BL, Rice LB. Intrinsic and acquired resistance mechanisms in Enterococcus. Virulence. 2012;3(5):421–433. https://doi.org/10.4161/viru.21282
Verraes C, Van Boxstael S, Van Meervenne E, et al. Antimicrobial resistance in the food chain: A review. Int J Environ Res Public Health. 2013;10(7):2643–2669. https://doi.org/10.3390/ijerph10072643
Seiler C, Berendonk TU. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol. 2012;3:399. https://doi.org/10.3389/fmicb.2012.00399
Gordo I. Evolutionary change in the human gut microbiome: from a static to a dynamic view. PLoS Biol. 2019;17:2. https://doi.org/10.1371/journal.pbio.3000126
Centers for Disease Control and Prevention (CDC). Antibiotic Resistance Threats in the United States, 2019 [Internet]. Atlanta (GA): Centers for Disease Control and Prevention (US); 2019 [cited 2024 Jul 29]. Available from: https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf
Published
How to Cite
Issue
Section
License
Copyright (c) 2025 Brazilian Animal Science/ Ciência Animal Brasileira

This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g. in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
Data statement
-
The research data is contained in the manuscript























