Advertisement

First Report on vanA-Enterococcus faecalis Recovered from Soils Subjected to Long-Term Livestock Agricultural Practices in Azores Archipelago

  • Vanessa Silva
  • Fernando Peixoto
  • Gilberto Igrejas
  • Carolina Parelho
  • Patrícia Garcia
  • Isabel Carvalho
  • Margarida Sousa
  • José Eduardo Pereira
  • Armindo Rodrigues
  • Patrícia Alexandra Curado Quintas Dinis PoetaEmail author
Research paper

Abstract

Antibiotic resistance represents a serious threat to human health. Some agricultural practices may lead to the acquisition of antibiotic resistance on soil bacteria. The aim of this study was to characterize the antibiotic-resistant profile of enterococci in soils exposed to livestock agricultural practices in Azores archipelago. Twenty-four soil samples were collected in 3 different pasture lands of São Miguel Island from Azores archipelago, with a different number of grazing animals, and from a control site. Eight Enterococcus spp. isolates were recovered: E. faecium (n = 5), E. hirae (n = 1), E.faecalis (n = 1) and E. gallinarum (n = 1). The isolates were tested for antibiotic resistance and virulence genes. The E. faecalis isolate was resistant to vancomycin (VRE) and harboured the van(A), the aph(3′) and aac(6′)-Ie-aph(2′)-Ia antibiotic resistance genes as well the esp virulence gene. Almost all non-VRE isolates were resistant to erythromycin and ampicillin and harboured the erm(B) gene. The antibiotics used in dairy and beef livestock cattle production are excreted through manure, which may exert a selective pressure on soil bacteria, leading to a higher bacterial resistome in the soil. This represents a public health problem due to the negative consequences and it might represent to human health.

Keywords

Antimicrobial resistance Enterococci Soil Livestock Azores archipelago 

References

  1. Abriouel H, Omar NB, Molinos AC, López RL, Grande MJ, Martínez-Viedma P, Ortega E, Cañamero MM, Galvez A (2008) Comparative analysis of genetic diversity and incidence of virulence factors and antibiotic resistance among enterococcal populations from raw fruit and vegetable foods, water and soil, and clinical samples. Int J Food Microbiol 123(1–2):38–49.  https://doi.org/10.1016/j.ijfoodmicro.2007.11.067 CrossRefGoogle Scholar
  2. Araujo C, Munoz-Atienza E, Hernandez PE, Herranz C, Cintas LM, Igrejas G, Poeta P (2015) Evaluation of Enterococcus spp. from rainbow trout (Oncorhynchus mykiss, Walbaum), feed, and rearing environment against fish pathogens. Foodborne Pathog. Dis 12:311–322.  https://doi.org/10.1089/fpd.2014.1906 CrossRefGoogle Scholar
  3. Ben Said L, Klibi N, Dziri R, Borgo F, Boudabous A, Ben Slama K, Torres C (2015) Prevalence, antimicrobial resistance and genetic lineages of Enterococcus spp. from vegetable food, soil and irrigation water in farm environments in Tunisia. J Sci Food Agric 96:1627–1633.  https://doi.org/10.1002/jsfa.7264 CrossRefGoogle Scholar
  4. Centinkaya Y, Yalk P, Mayhall CG (2000) Vancomycin-resistant Enterococci. Clin Microbiol Rev 2000(13):686–707CrossRefGoogle Scholar
  5. Chee-Sanford JC, Mackie R, Koike S, Krapac I, Lin Y, Yannarell A, Maxwell S, Aminov R (2009) Fate and transport of antibiotic residues and antibiotic resistance genes. J Environ Qual 38:1086–1108.  https://doi.org/10.2134/jeq2008.0128 CrossRefGoogle Scholar
  6. Chow JW (2000) Aminoglycoside resistance in Enterococci. Clin Infect Dis 31:586–589CrossRefGoogle Scholar
  7. Cruz JV, Pereira R, Moreira A (2007) Carta de Ocupação do Solo da Região Autónoma dos Açores (Report), Secretaria Regional do Ambiente e do Mar, Direcção Regional do Ordenamento do Território e dos Recursos Hídricos. http://www.azores.gov.pt/NR/rdonlyres/730FD13F-9AEE-4C6A-A2DA-4226FC77DCE0/388321/COSRAARELATORIO.pdf
  8. Day MJ, Rodriguez I, van Essen-Zandbergen A, Dierikx C, Kadlec K, Schink AK, Wu G, Chattaway MA, DoNascimento V, Wain J, Helmuth R, Guerra B, Schwarz S, Threlfall J, Woodward MJ, Coldham N, Mevius D, Woodford N (2016) Diversity of STs, plasmids and ESBL genes among Escherichia coli from humans, animals and food in Germany, the Netherlands and the UK. J Antimicrob Chemother 71(5):1178–1182.  https://doi.org/10.1093/jac/dkv485 CrossRefGoogle Scholar
  9. De Leener E, Martel A, De Graef EM, Top J, Butaye P, Haesebrouck F, Willems R, Decostere A (2004) Molecular analysis of human, porcine, and poultry Enterococcus faecium isolates and their erm(B) Genes. Appl Environ Microbiol 71(5):2766–2770.  https://doi.org/10.1128/AEM.71.5.2766-2770.2005 CrossRefGoogle Scholar
  10. Freire MP, Oshiro IC, Pierrotti LC, Bonazzi PR, de Oliveira LM, Song AT, Camargo CH, van der Heijden IM, Rossi F, Costa SF, D’Albuquerque LA, Abdala E (2016) Carbapenem-resistant Enterobacteriaceae acquired before liver transplantation: impact on recipient outcomes. Transplantation 101(4):811–820.  https://doi.org/10.1097/TP.0000000000001620 CrossRefGoogle Scholar
  11. Haack SK, Duris JW, Kolpin DW, Focazio MJ, Meyer MT, Johnson HE, Oster RJ, Foreman WT (2016) Contamination with bacterial zoonotic pathogen genes in U.S. streams influenced by varying types of animal agriculture. Sci Total Environ 563–564:340–350.  https://doi.org/10.1016/j.scitotenv.2016.04.087 CrossRefGoogle Scholar
  12. Haenni M, Saras E, Chatre P, Meunier D, Martin S, Lepage G, Menard M, Lebreton P, Rambaud T, Madec J (2009) vanA in Enterococcus faecium, Enterococcus faecalis, and Enterococcus casseliflavus detected in french cattle. Foodborne Pathog Dis 6(9):1107–1111.  https://doi.org/10.1089/fpd.2009.0303 CrossRefGoogle Scholar
  13. He LY, Ying GG, Liu YS, Su HC, Chen J, Liu SS, Zhao JL (2016) Discharge of swine wastes risks water quality and food safety: Antibiotics and antibiotic resistance genes from swine sources to the receiving environments. Environ Int 92–93:210–219.  https://doi.org/10.1016/j.envint.2016.03.023 CrossRefGoogle Scholar
  14. Kang M, Xie Y, He C, Chen ZX, Guo L, Yang Q, Liu JY, Du Y, Ou QS, Wang LL (2014) Molecular characteristics of vancomycin-resistant Enterococcus faecium from a tertiary care hospital in Chengdu, China. Eur J Clin Microbiol Infect Dis 33:933–939.  https://doi.org/10.1007/s10096-013-2029-z CrossRefGoogle Scholar
  15. Marinho C, Silva N, Pombo S, Santos T, Monteiro R, Goncalves A, Micael J, Rodrigues P, Costa AC, Igrejas G, Poeta P (2013) Echinoderms from Azores islands: an unexpected source of antibiotic resistant Enterococcus spp. and Escherichia coli isolates. Mar Pollut Bull 69(1–2):122–127.  https://doi.org/10.1016/j.marpolbul.2013.01.017 CrossRefGoogle Scholar
  16. Martínez JL (2012) Bottlenecks in the Transferability of Antibiotic Resistance from Natural Ecosystems to Human Bacterial Pathogens. Frontiers Microbiol 2:265.  https://doi.org/10.3389/fmicb.2011.00265 CrossRefGoogle Scholar
  17. Poeta P, Costa D, Rodrigues J, Torres C (2005) Study of faecal colonization by vanA-containing Enterococcus strains in healthy humans, pets, poultry and wild animals in Portugal. J Antimicrob Chemother 55:278e80CrossRefGoogle Scholar
  18. Radhouani H, Pinto L, Coelho C, Sargo R, Araujo C, Lopez M, Torres C, Igrejas G, Poeta P (2010) MLST and a genetic study of antibiotic resistance and virulence factors in vanA-containing Enterococcus from buzzards (Buteo buteo). Lett Appl Microbiol 50:537–541.  https://doi.org/10.1111/j.1472-765X.2010.02807 CrossRefGoogle Scholar
  19. Radhouani H, Silva N, Poeta P, Torres C, Correia S, Igrejas G (2014) Potential impact of antimicrobial resistance in wildlife, environment and human health. Frontiers Microbiol 5:23.  https://doi.org/10.3389/fmicb.2014.00023 CrossRefGoogle Scholar
  20. Reyes K, Bardossy AC, Zervos M (2016) Vancomycin-resistant Enterococci epidemiology, infection prevention, and control. Infect Dis Clin N Am 30(2016):953–965.  https://doi.org/10.1016/j.idc.2016.07.009 CrossRefGoogle Scholar
  21. Rummukainen ML, Mäkelä M, Noro A, Finne-Soveri H, Lyytikäinen O (2013) Assessing prevalence of antimicrobial use and infections using the minimal data set in Finnish long-term care facilities. Am J Infect Control 41(4):e35–e37.  https://doi.org/10.1016/j.ajic.2012.09.007 CrossRefGoogle Scholar
  22. Santos T, Silva N, Igrejas G, Rodrigues P, Micael J, Rodrigues T, Cunha R, Poeta P (2013) Anaerobe dissemination of antibiotic resistant Enterococcus spp. and Escherichia coli from wild birds of Azores archipelago. Anaerobe 24:25–31CrossRefGoogle Scholar
  23. Silva V, Igrejas G, Carvalho I, Peixoto F, Cardoso L, Pereira JE, del Campo R, Poeta P (2017) Genetic characterization of vanA-Enterococcus faecium isolates from wild red-legged partridges in Portugal. Microb Drug Resist.  https://doi.org/10.1089/mdr.2017.0040 Google Scholar
  24. Tang Q, Song P, Li J, Kong F, Sun L, Xu L (2016) Control of antibiotic resistance in China must not be delayed: The current state of resistance and policy suggestions for the government, medical facilities, and patients. BioSci Trends 10(1):1–6.  https://doi.org/10.5582/bst.2016.01034 CrossRefGoogle Scholar
  25. Thaller MC, Marquez C, Tapia W, Cedeño V, Rossolini GM (2010) Tracking acquired antibiotic resistance in commensal bacteria of Galápagos land iguanas: no man, no resistance. PLoS One 5(2):e8989.  https://doi.org/10.1371/journal.pone.0008989 CrossRefGoogle Scholar
  26. Torres C, Tenorio C, Portillo A, García M, Martínez C, Del Campo R, Ruiz-Larrea F, Zarazaga M (2003) Intestinal colonization by vanA- or vanB2-containing enterococcal isolates of healthy animals in Spain. Microb Drug Resist 9(Suppl 1):S47–S52CrossRefGoogle Scholar
  27. Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J (2014) Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci USA 111(42):15202–15207.  https://doi.org/10.1073/pnas.1409836111 CrossRefGoogle Scholar
  28. USDA (2016) Antibiotic resistance can occur naturally in soil bacteria. In: ScienceDailyGoogle Scholar
  29. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA 112(18):5649–5654.  https://doi.org/10.1073/pnas.1503141112 CrossRefGoogle Scholar
  30. Werner G, Coque TM, Hammerum AM, Hope R, Hryniewicz W, Johnson A et al (2008) Emergence and spread of vancomycin resistance among enterococci in Europe. Euro Surveill 13:19046Google Scholar
  31. Woolhouse M, Ward M, van Bunnik B, Farrarr J (2015) Antimicrobial resistance in humans, livestock and the wider environment. Philos Trans R Soc Lond B Biol Sci 370(1670):1–7.  https://doi.org/10.1098/rstb.2014.0083 CrossRefGoogle Scholar

Copyright information

© University of Tehran 2018

Authors and Affiliations

  • Vanessa Silva
    • 1
    • 2
    • 3
  • Fernando Peixoto
    • 1
  • Gilberto Igrejas
    • 2
    • 3
    • 4
  • Carolina Parelho
    • 5
    • 6
  • Patrícia Garcia
    • 5
    • 6
  • Isabel Carvalho
    • 1
    • 2
    • 3
  • Margarida Sousa
    • 1
    • 2
    • 3
  • José Eduardo Pereira
    • 1
    • 7
  • Armindo Rodrigues
    • 5
    • 8
  • Patrícia Alexandra Curado Quintas Dinis Poeta
    • 1
    • 4
    Email author
  1. 1.Department of Veterinary SciencesUniversity of Trás-os-Montes and Alto Douro (UTAD)Vila RealPortugal
  2. 2.Department of Genetics and BiotechnologyUniversity of Trás-os-Montes and Alto DouroVila RealPortugal
  3. 3.Functional Genomics and Proteomics UnitUniversity of Trás-os-Montes and Alto Douro (UTAD)Vila RealPortugal
  4. 4.Associated Laboratory for Green Chemistry (LAQV-REQUIMTE)University NOVA of LisboaLisbonPortugal
  5. 5.Faculty of Sciences and TechnologyUniversity of the AzoresPonta DelgadaPortugal
  6. 6.cE3c, Centre for Ecology, Evolution and Environmental Changes, Azorean Biodiversity GroupUniversity of the AzoresPonta DelgadaPortugal
  7. 7.CECAV, University of Trás-os-Montes and Alto DouroVila RealPortugal
  8. 8.IVAR, Institute of Volcanology and Risks AssessmentUniversity of the AzoresPonta DelgadaPortugal

Personalised recommendations