Antimicrobial resistance in ovine production: maternal-descendant similarities in Coliforms and Enterococcus spp.

Carolina Rodriguez Jimenez; Gabriela Assalim; Jessica Ferreira Gomes; Murilo Fernandes; Livia Maria Presuto; Patricia Spoto Correa; Helder Louvandini

doi:10.1590/1809-6891v26e-80984E

Autores

Carolina Rodriguez Jimenez Centro de Energia Nuclear na Agricultura, Universidade de São Paulo (USP), Piracicaba, São Paulo, Brasil https://orcid.org/0000-0001-7731-4858
Gabriela Assalim Faculdade de Americana (FAM), Americana, São Paulo, Brasil https://orcid.org/0009-0003-0796-3184
Jessica Ferreira Gomes Faculdade de Americana (FAM), Americana, São Paulo, Brasil https://orcid.org/0009-0003-1943-9523
Murilo Fernandes Centro de Energia Nuclear na Agricultura, Universidade de São Paulo (USP), Piracicaba, São Paulo, Brasil https://orcid.org/0000-0003-2629-3473
Livia Maria Presuto Centro de Energia Nuclear na Agricultura, Universidade de São Paulo (USP), Piracicaba, São Paulo, Brasil https://orcid.org/0000-0003-4801-6768
Patricia Spoto Correa Centro de Energia Nuclear na Agricultura, Universidade de São Paulo (USP), Piracicaba, São Paulo, Brasil https://orcid.org/0000-0002-8540-6629
Helder Louvandini Centro de Energia Nuclear na Agricultura, Universidade de São Paulo (USP), Piracicaba, São Paulo, Brasil https://orcid.org/0000-0001-7129-8463

DOI:

https://doi.org/10.1590/1809-6891v26e-80984E

Resumo

Resumo: Há uma escassez de relatos sobre o aumento da resistência antimicrobiana e a transferência dessa resistência de progenitores para descendentes em animais de produção. Diante desse cenário, é essencial compreender como os mecanismos de resistência bacteriana se disseminam na criação de ovinos. O objetivo deste estudo é identificar a ocorrência de resistência antimicrobiana em Coliformes e Enterococcus spp. presuntivos presentes em progenitores e seus descendentes durante os períodos de nascimento e desmame. Foram utilizadas vinte e seis ovelhas prenhes (Ovis aries), com peso corporal médio de 40 ± 2,0 kg e escore de condição corporal de 3,5 ± 0,3. Amostras de sangue e fezes foram coletadas tanto das matrizes quanto dos filhotes para análises de hemograma completo e testes de sensibilidade antimicrobiana (TSA). O TSA foi realizado contra os antibióticos penicilina, tetraciclina, enrofloxacina, ampicilina, estreptomicina, eritromicina e ceftiofur, tendo como alvo os gêneros bacterianos Coliformes e presuntivo de (P.) Enterococcus spp. Os resultados mostraram que, nos períodos de nascimento e desmame, os progenitores e seus descendentes apresentaram semelhança nos testes de susceptibilidade. Antibióticos como eritromicina e penicilina apresentaram altos níveis de resistência. Além disso, o ceftiofur, um antibiótico não utilizado na ovinocultura, demonstrou casos isolados de resistência, embora tenham sido baixos e não generalizados, esses achados destacam o potencial impacto de mecanismos bacterianos de resistência pré-existentes sobre a eficácia de antimicrobianos mais recentes. Conclui-se que há uma similaridade materno-descendente entre as bactérias analisadas. Os antibióticos ceftiofur, tetraciclina, estreptomicina, ampicilina e enrofloxacina apresentaram menor resistência, enquanto eritromicina e penicilina mostraram níveis mais elevados. Recomenda-se a realização de estudos específicos em cada sistema de produção ovina para o controle da presença de resistência à eritromicina e penicilina.
Palavras-chave: Antibiótico; cordeiro; ovelha; sensibilidade; susceptibilidade.

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Referências

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