Skip to main content
SpringerLink
Log in

Detection of β-lactamase encoding genes in feces, soil and water from a Brazilian pig farm

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

β-lactam antibiotics are widely used for the treatment of different types of infections worldwide and the resistance to these antibiotics has grown sharply, which is of great concern. Resistance to β-lactams in gram-negative bacteria is mainly due to the production of β-lactamases, which are classified according to their functional activities. The aim of this study was to verify the presence of β-lactamases encoding genes in feces, soil, and water from a Brazilian pig farm. Different β-lactamases encoding genes were found, including blaCTX-M-Gp1, blaCTX-M-Gp9, blaSHV, blaOXA-1-like, blaGES, and blaVEB. The blaSHV and blaCTX-M-Gp1 genes have been detected in all types of samples, indicating the spread of β-lactam resistant bacteria among farm pigs and the environment around them. These results indicate that β-lactamase encoding genes belonging to the cloxacillinase, ESBL, and carbapenemase and they have high potential to spread in different sources, due to the fact that genes are closely related to mobile genetic elements, especially plasmids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Ben Said, L., Jouini, A., Alonso, C. A., Klibi, N., Dziri, R., Boudabous, A., Ben Slama, K., & Torres, C. (2016). Characteristics of extended-spectrum β-lactamase (ESBL)- and pAmpC beta-lactamase-producing Enterobacteriaceae of water samples in Tunisia. The Science of the Total Environment, 550, 1103–1109. https://doi.org/10.1016/j.scitotenv.2016.01.042.

    Article  CAS  Google Scholar 

  • Blaak, H., Hamidjaja, R. A., van Hoek, A. H., de Heer, L., Husman, A. M. R., & Schets, F. M. (2014). Detection of extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli on flies at poultry farms. Applied and Environmental Microbiology, 80(1), 239–246. https://doi.org/10.1128/AEM.02616-13.

    Article  CAS  Google Scholar 

  • Bush, K. (2010). Bench-to-bedside review: the role of β-lactamases in antibiotic-resistant gram-negative infections. Critical Care, 14(3), 224. https://doi.org/10.1186/cc8892.

    Article  Google Scholar 

  • Bush, K., & Jacoby, G. A. (2010). Updated functional classification of β-lactamases. Antimicrobial Agents and Chemotherapy, 54(3), 969–976. https://doi.org/10.1128/AAC.01009-09.

    Article  CAS  Google Scholar 

  • Carattoli, A. (2008). Animal reservoirs for extended spectrum β-lactamase producers. Clinical Microbiology and Infection, 14(Suppl 1), 117–123. https://doi.org/10.1111/j.1469-0691.2007.01851.x.

    Article  Google Scholar 

  • Clímaco, E. C., Oliveira, M. L., Pitondo-Silva, A., Oliveira, M. G., Medeiros, M., Lincopan, N., & da Costa Darini, A. L. (2013). Clonal complexes 104, 109 and 113 playing a major role in the dissemination of OXA-carbapenemase-producing Acinetobacter baumannii in Southeast Brazil. Infection, Genetics and Evolution, 19, 127–133. https://doi.org/10.1016/j.meegid.2013.06.024.

    Article  Google Scholar 

  • Dahms, C., Hübner, N. O., Kossow, A., Mellmann, A., Dittmann, K., & Kramer, A. (2015). Occurrence of ESBL-producing Escherichia coli in livestock and farm workers in Mecklenburg-Western Pomerania, Germany. PLoS One, 10(11), e0143326. https://doi.org/10.1371/journal.pone.0143326.

    Article  Google Scholar 

  • Dallenne, C., Costa, A., Decré, D., Favier, C., & Arlet, G. (2010). Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae. The Journal of Antimicrobial Chemotherapy, 65(3), 490–495. https://doi.org/10.1093/jac/dkp498.

    Article  CAS  Google Scholar 

  • De Boeck, H., Miwanda, B., Lunguya-Metila, O., Muyembe-Tamfum, J. J., Stobberingh, E., Glupczynski, Y., & Jacobs, J. (2012). ESBL-positive Enterobacteria isolates in drinking water. Emerging Infectious Diseases, 18(6), 1019–1020. https://doi.org/10.3201/eid1806.111214.

    Article  Google Scholar 

  • Dohmen, W., Bonten, M. J., Bos, M. E., van Marm, S., Scharringa, J., Wagenaar, J. A., et al. (2015). Carriage of extended-spectrum β-lactamases in pig farmers is associated with occurrence in pigs. Clinical Microbiology and Infection, 21(10), 917–923. https://doi.org/10.1016/j.cmi.2015.05.032.

    Article  CAS  Google Scholar 

  • Ellington, M. J., Kistler, J., Livemore, D. M., & Woodford, N. (2007). Multiplex PCR for rapid detection of genes encoding acquired metallo-β-lactamases. The Journal of Antimicrobial Chemotherapy, 59(2), 321–322. https://doi.org/10.1093/jac/dkl481.

    Article  CAS  Google Scholar 

  • Escudero, E., Vinué, L., Teshager, T., Torres, C., & Moreno, M. A. (2010). Resistance mechanisms and farm-level distribution of fecal Escherichia coli isolates resistant to extended-spectrum cephalosporins in pigs in Spain. Research in Veterinary Science, 88(1), 83–87. https://doi.org/10.1016/j.rvsc.2009.05.021.

    Article  CAS  Google Scholar 

  • Ewers, C., Bethe, A., Semmler, T., Guenther, S., & Wieler, L. H. (2012). Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clinical Microbiology and Infection, 18(7), 646–655. https://doi.org/10.1111/j.1469-0691.2012.03850.x.

    Article  CAS  Google Scholar 

  • Furlan, J. P. R., & Stehling, E. G. (2017a). Presence of β-lactamases encoding genes in soil samples from different origins. Water, Air, and Soil Pollution, 228(4), 125. https://doi.org/10.1007/s11270-017-3318-4.

    Article  Google Scholar 

  • Furlan, J. P. R., & Stehling, E. G. (2017b). High-level of resistance to β-lactam and presence of β-lactamases encoding genes in Ochrobactrum sp. and Achromobacter sp. isolated from soil. Journal of Global Antimicrobial Resistance, 11, 133–137. https://doi.org/10.1016/j.jgar.2017.10.014.

    Article  Google Scholar 

  • Furlan, J. P. R., Stehling, E. G., & Pitondo-Silva, A. (2017). Importance of sequencing to determine functional blaTEM variants. Antimicrob Agents Chemother, 61(5), e00237–e00217. https://doi.org/10.1128/AAC.00237-17.

    Article  CAS  Google Scholar 

  • Gatica, J., Yang, K., Pagaling, E., Jurkevitch, E., Yan, T., & Cytryn, E. (2015). Resistance of undisturbed soil microbiomes to ceftriaxone indicates extended Spectrum β-lactamase activity. Frontiers in Microbiology, 6, 1233. https://doi.org/10.3389/fmicb.2015.01233.

    Article  Google Scholar 

  • Graham, D. W., Knapp, C. W., Christensen, B. T., McCluskey, S., & Dolfing, J. (2016). Appearance of β-lactam resistance genes in agricultural soils and clinical isolates over the 20th century. Scientific Reports, 6(1). https://doi.org/10.1038/srep21550.

  • Haque, A., Yoshizumi, A., Saga, T., Ishii, Y., & Tateda, K. (2014). ESBL-producing Enterobacteriaceae in environmental water in Dhaka, Bangladesh. Journal of Infection and Chemotherapy, 20(11), 735–737. https://doi.org/10.1016/j.jiac.2014.07.003.

    Article  Google Scholar 

  • Heritier, C., Dubouix, A., Poirel, L., Marty, N., & Nordmann, P. (2005). A nosocomial outbreak of Acinetobacter baumannii isolates expressing the carbapenem-hydrolysing oxacillinase OXA-58. The Journal of Antimicrobial Chemotherapy, 55(1), 115–118. https://doi.org/10.1093/jac/dkh500.

    Article  CAS  Google Scholar 

  • Hille, K., Fischer, J., Falgenhauer, L., Sharp, H., Brenner, G. M., Kadlec, K., Friese, A., Schwarz, S., Imirzalioglu, C., Kietzmann, M., von Münchhausen, C., & Kreienbrock, L. (2014). On the occurence of extended-spectrum- and AmpC-beta-lactamase-producing Escherichia coli in livestock: results of selected European studies. Berliner und Münchener Tierärztliche Wochenschrift, 127(9–10), 403–411.

    Google Scholar 

  • Jacoby, G., & Bush, K. (2016). The curious case of TEM-116. Antimicrobial Agents and Chemotherapy, 60(11), 7000. https://doi.org/10.1128/AAC.01777-16.

    Article  CAS  Google Scholar 

  • Jeong, S. H., Bae, I. K., Kim, D., Hong, S. G., Song, J. S., Lee, J. H., & Lee, S. H. (2005). First outbreak of Klebsiella pneumoniae clinical isolates producing GES-5 and SHV-12 extended-spectrum β-lactamases in Korea. Antimicrobial Agents and Chemotherapy, 49(11), 4809–4810. https://doi.org/10.1128/AAC.49.11.4809-4810.2005.

    Article  CAS  Google Scholar 

  • Kola, A., Kohler, C., Pfeifer, Y., Schwab, F., Kuhn, K., Schulz, K., Balau, V., Breitbach, K., Bast, A., Witte, W., Gastmeier, P., & Steinmetz, I. (2012). High prevalence of extended-spectrum betalactamase-producing Enterobacteriaceae in organic and conventional retail chicken meat, Germany. The Journal of Antimicrobial Chemotherapy, 67(11), 2631–2634. https://doi.org/10.1093/jac/dks295.

    Article  CAS  Google Scholar 

  • Leverstein-van Hall, M. A., Dierikx, C. M., Cohen Stuart, J., Voets, G. M., van den Munckhof, M. P., van Essen-Zandbergen, A., Platteel, T., Fluit, A. C., van de Sande-Bruinsma, N., Scharinga, J., Bonten, M. J., Mevius, D. J., & National ESBL surveillance group. (2011). Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clinical Microbiology and Infection, 17(6), 873–880. https://doi.org/10.1111/j.1469-0691.2011.03497.

    Article  CAS  Google Scholar 

  • Nicoletti, A. G., Marcondes, M. F., Martins, W. M., Almeida, L. G., Nicolás, M. F., Vasconcelos, A. T., et al. (2015). Characterization of BKC-1 class A carbapenemase from Klebsiella pneumoniae clinical isolates in Brazil. Antimicrobial Agents and Chemotherapy, 59(9), 5159–5164. https://doi.org/10.1128/AAC.00158-15.

    Article  CAS  Google Scholar 

  • Overdevest, I., Willemsen, I., Rijnsburger, M., Eustace, A., Xu, L., Hawkey, P., Heck, M., Savelkoul, P., Vandenbroucke-Grauls, C., van der Zwaluw, K., Huijsdens, X., & Kluytmans, J. (2011). Extended-Spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerging Infectious Diseases, 17(7), 1216–1222. https://doi.org/10.3201/eid1707.110209.

    Article  Google Scholar 

  • Peirano, G., Ahamed-Bentley, J., Woodford, N., & Pitout, J. D. (2011). New Delhi metallo-β-lactamase from traveler returning to Canada. Emering Infectious Diseases, 17, 240–242. https://doi.org/10.3201/eid1702.101313.

    Google Scholar 

  • Pitondo-Silva, A., Devechio, B. B., Moretto, J. A., & Stehling, E. G. (2016). High prevalence of blaVIM-1 gene in bacteria from Brazilian soil. Canadian Journal of Microbiology, 62(10), 820–826. https://doi.org/10.1139/cjm-2015-0787.

    Article  CAS  Google Scholar 

  • Pitondo-Silva, A., Martins, V. V., & Stehling, E. G. (2015). First report of the blaVIM gene in environmental isolates of Buttiauxella sp. APMSI, 62(10), 820–826. https://doi.org/10.1111/apm.12358.

    Google Scholar 

  • Pitout, J. D., Gregson, D. B., Poirel, L., McClure, J. A., Le, P., & Church, D. L. (2005). Detection of Pseudomonas aeruginosa producing metallo-Beta-lactamases in a large centralized laboratory. Journal of Clinical Microbiology, 43(7), 3129–3135. https://doi.org/10.1128/JCM.43.7.3129-3135.2005.

    Article  CAS  Google Scholar 

  • Poirel, L., Docquier, J. D., De Luca, F., Verlinde, A. d. L., Rossolini, G. M., & Nordmann, P. (2010). Bel-2, an extended-spectrum beta-lactamase with increased activity toward expanded-spectrum cephalosporins in Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy, 54(1), 533–535. https://doi.org/10.1128/AAC.00859-09.

    Article  CAS  Google Scholar 

  • Poirel, L., Weldhagen, G. F., De Champs, C., & Nordmann, P. (2002). A nosocomial outbreak of Pseudomonas aeruginosa isolates expressing the extended-spectrum beta-lactamase GES-2 in South Africa. The Journal of Antimicrobial Chemotherapy, 49(3), 561–565. https://doi.org/10.1093/jac/49.3.561.

    Article  CAS  Google Scholar 

  • Queenan, A. M., & Bush, K. (2007). Carbapenemases: the versatile β-lactamases. Clinical Microbiology Reviews, 20(3), 440–458. https://doi.org/10.1128/C7MR.00001-07.

    Article  CAS  Google Scholar 

  • Queenan, A. M., Torres-Viera, C., Gold, H. S., Carmeli, Y., Eliopoulos, G. M., Moellering Jr., R. C., Moellering, R. C., Quinn, J. P., Hindler, J., Medeiros, A. A., & Bush, K. (2000). SME-type carbapenem-hydrolyzing class A beta-lactamases from geographically diverse Serratia marcescens strains. Antimicrobial Agents and Chemotherapy, 44(11), 3035–3039. https://doi.org/10.1128/AAC.44.11.3035-3039.2000.

    Article  CAS  Google Scholar 

  • Randall, L. P., Lemma, F., Rogers, J. P., Cheney, T. E., Powell, L. F., & Teale, C. J. (2014). Prevalence of extended-spectrum-β-lactamase-producing Escherichia coli from pigs at slaughter in the UK in 2013. The Journal of Antimicrobial Chemotherapy, 69(11), 2947–2950. https://doi.org/10.1093/jac/dku258.

    Article  CAS  Google Scholar 

  • Samanta, I., Joardar, S. N., Mahanti, A., Bandyopadhyay, S., Sar, T. K., & Dutta, T. K. (2015). Approaches to characterize extended spectrum beta-lactamase/beta-lactamase producing Escherichia coli in healthy organized vis-a-vis backyard farmed pigs in India. Infection, Genetics and Evolution, 36, 224–230. https://doi.org/10.1016/j.meegid.2015.09.021.

    Article  CAS  Google Scholar 

  • Schmithausen, R. M., Schulze-Geisthoevel, S. V., Stemmer, F., El-Jade, M., Reif, M., Hack, S., Meilaender, A., Montabauer, G., Fimmers, R., Parcina, M., Hoerauf, A., Exner, M., Petersen, B., Bierbaum, G., & Bekeredjian-Ding, I. (2015). Analysis of transmission of MRSA and ESBL-E among pigs and farm personnel. PLoS One, 10(9), e0138173. https://doi.org/10.1371/journal.pone.0138173.

    Article  Google Scholar 

  • Sharp, H., Valentin, L., Fischer, J., Guerra, B., Appel, B., & Käsbohrer, A. (2014). Estimation of the transfer of ESBL-producing Escherichia coli to humans in Germany. Berliner und Münchener Tierärztliche Wochenschrift, 127(11–12), 464–477.

    Google Scholar 

  • Tissera, S., & Lee, S. M. (2013). Isolation of extended spectrum β-lactamase (ESBL) producing bacteria from urban surface waters in Malaysia. Malays J Med Sci, 20(3), 14–22.

    Google Scholar 

  • Valentin, L., Sharp, H., Hille, K., Seibt, U., Fischer, J., Pfeifer, Y., Michael, G. B., Nickel, S., Schmiedel, J., Falgenhauer, L., Friese, A., Bauerfeind, R., Roesler, U., Imirzalioglu, C., Chakraborty, T., Helmuth, R., Valenza, G., Werner, G., Schwarz, S., Guerra, B., Appel, B., Kreienbrock, L., & Käsbohrer, A. (2014). Subgrouping of ESBL-producing Escherichia coli from animal and human sources: an approach to quantify the distribution of ESBL types between different reservoirs. International Journal of Medical Microbiology, 304(7), 805–816. https://doi.org/10.1016/j.ijmm.2014.07.015.

    Article  Google Scholar 

  • Wang, Y., He, T., Han, J., Wang, J., Foley, S. L., Yang, G., et al. (2012). Prevalence of ESBLs and PMQR genes in fecal Escherichia coli isolated from the non-human primates in six zoos in China. Veterinary Microbiology, 159(1–2), 53–59. https://doi.org/10.1016/j.vetmic.2012.03.009.

    Article  CAS  Google Scholar 

  • Xi, M., Wu, Q., Wang, X., Yang, B., Xia, X., & Li, D. (2015). Characterization of extended-spectrum beta-lactamase-producing Escherichia coli strains isolated from retail foods in Shaanxi Province, China. Journal of Food Protection, 78(5), 1018–1023. https://doi.org/10.4315/0362-028X.JFP-14-490.

    Article  CAS  Google Scholar 

  • Yousef, S. A. A., Farrag, E. S., Ali, A. M., & Mahmoud, S. Y. (2016). Detection of extended spectrum beta-lactamase producing Escherichia coli on water at Hafr Al Batin, Saudi Arabia. Journal of Pollution Effects & Control, 4, 1. https://doi.org/10.4172/2375-4397.1000155.

    Google Scholar 

Download references

Acknowledgments

The authors thank J.D.D. Pitout (University of Calgary, Calgary, AB, Canada) for kindly providing the β-lactamase control strains used in this study.

Funding

This work was supported by the São Paulo Research Foundation—FAPESP [grant number 2015/18990-2].

Author information

Authors and Affiliations

  1. Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Av. do Café S/N. Monte Alegre, Ribeirão Preto, SP, 14040-903, Brazil

    João Pedro Rueda Furlan & Eliana Guedes Stehling

Authors
  1. João Pedro Rueda Furlan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eliana Guedes Stehling
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eliana Guedes Stehling.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical approval

Not required.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Furlan, J.P.R., Stehling, E.G. Detection of β-lactamase encoding genes in feces, soil and water from a Brazilian pig farm. Environ Monit Assess 190, 76 (2018). https://doi.org/10.1007/s10661-017-6453-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-017-6453-x

Keywords

Search

Navigation