Skip to main content
Log in

Thermophilic anaerobic digestion is an effective treatment for reducing cefazolin-resistant bacteria and ESBL-producers in dairy manure

  • ORIGINAL ARTICLE
  • Published:
Journal of Material Cycles and Waste Management Aims and scope Submit manuscript

Abstract

The application of thermophilic anaerobic digestion (TAD) treatments to dairy manure in a biogas plant was evaluated to investigate whether the prominent countermeasure was sufficient for the dissemination of antimicrobial-resistant (AMR) bacteria in the dairy industry. To determine the changes in the number of AMR bacteria in dairy manure after TAD, cefazolin-resistant (CEZ-R) and ampicillin-resistant (AMP-R) bacteria in dairy manure and digestate were quantified by plate spread methods performed with combinations of antimicrobials added to agar plates and selective and differential agar plates. In addition, extended-spectrum β-lactamase (ESBL)-producing bacteria were also quantified to evaluate the effect of TAD on plasmid-borne resistant bacteria. CEZ-R and AMP-R bacteria were widely reduced after TAD compared with the susceptible bacteria against these antimicrobials. The classification into E. coli, other coliforms, and non-coliform bacteria revealed that CEZ-R and AMP-R coliform bacteria were more significantly reduced than non-coliform bacteria by TAD. Moreover, ESBL-producing bacteria were reduced significantly among CEZ-R bacteria. From these results, TAD appears to be a useful treatment to counter the dissemination of AMR bacteria in dairy manure by the preferential elimination of AMR bacteria.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Roca I, Akova M, Baquero F, Carlet J, Cavaleri M, Coenen S, Cohen J, Findlay D, Gyssens I, Heure OE, Kahlmeter G, Kruse H, Laxminarayan R, Liébana E, López-Cerero L, MacGowan A, Martins M, Rodríguez-Baño J, Rolain JM, Segovia C, Sigauque B, Tacconelli E, Wellington E, Vila J (2015) The global threat of antimicrobial resistance: science for intervention. New Microbes New Infect 6:22–29. https://doi.org/10.1016/j.nmni.2015.02.007

    Article  Google Scholar 

  2. Asai T, Kojima A, Harada K, Ishihara K, Takahashi T, Tamura Y (2005) Correlation between the usage volume of veterinary therapeutic antimicrobials and resistance in Escherichia coli isolated from the feces of food-producing animals in Japan. Jpn J Infect Dis 58:369–372

    Google Scholar 

  3. Furuya EY, Franklin DL (2006) Antimicrobial-resistant bacteria in the community setting. Nat Rev Microbiol 4:36–45. https://doi.org/10.1038/nrmicro1325

    Article  Google Scholar 

  4. The National Veterinary Assay Laboratory, Ministry of Agriculture, Forestry, and Fisheries (2013) Report of the Japanese veterinary antimicrobial resistance monitoring system—2008 to 2011. http://www.maff.go.jp/nval/. Accessed 23 Mar 2017

  5. Iwasaki M, Yamashiro T, Beneragama N, Nishida T, Kida K, Ihara I, Takahashi J, Umetsu K (2011) The effect of temperature on survival of pathogenic bacteria in biogas plants. Anim Sci J 82:707–712. https://doi.org/10.1111/j.1740-0929.2011.00887.x

    Article  Google Scholar 

  6. Brinas L, Moreno MA, Zarazaga M, Porrero C, Saenz Y, García M, Dominguez L, Torres C (2003) Detection of CMY-2, CTX-M-14, and SHV-12 β-lactamases in Escherichia coli fecal-sample isolates from healthy chickens. Antimicrob Agents Chemother 47:2056–2058

    Article  Google Scholar 

  7. Jacoby GA (2006) β-Lactamase nomenclature. Antimicrob Agents Chemother 50:1123–1129. https://doi.org/10.1128/AAC.50.4.1123-1129.2006

    Article  Google Scholar 

  8. Batchelor M, Threlfall EJ, Liebana E (2005) Cephalosporin resistance among animal-associated Enterobacteria: a current perspective. Expert Rev Anti Infect Ther 3:403–417. https://doi.org/10.1586/14787210.3.3.403

    Article  Google Scholar 

  9. Carattoli A (2008) Animal reservoirs for extended spectrum β-lactamase producers. Clin Microbiol Infect 14(Suppl 1):117–123. https://doi.org/10.1111/j.1469-0691.2007.01851.x

    Article  Google Scholar 

  10. Asuming-Brempong S, Aferi NK (2014) Isolation of phosphate solubilizing bacteria from tropical soil. Glob Adv Res J Agric Sci 3:8–15

    Google Scholar 

  11. Lowe SE, Jain MK, Zeikus JG (1993) Biology, ecology, and biotechnological applications of anaerobic bacteria adapted to environmental stresses in temperature, pH, salinity, or substrates. Microbiol Rev 57:451–509

    Google Scholar 

  12. Sahlstrom L (2003) A review of survival of pathogenic bacteria in organic waste used in biogas plants. Bioresour Technol 87:161–166. https://doi.org/10.1016/S0960-8524(02)00168-2

    Article  Google Scholar 

  13. Desbois AP, Smith VJ (2010) Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol 85:1629–1642. https://doi.org/10.1007/s00253-009-2355-3

    Article  Google Scholar 

  14. Aldsworth TG, Sharman RL, Dodd CER (1999) Bacterial suicide through stress. Cell Mol Life Sci 56:378–383. https://doi.org/10.1007/s000180050439

    Article  Google Scholar 

  15. Palleroni NJ (2005) Genus I. Pseudomonas. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM (eds) Bergey’s Manual of Systematic Bacteriology, vol 2, 2nd edn. Springer, East Lansing, pp 323–379

    Google Scholar 

  16. Qi G, Pan Z, Sugawa Y, Andriamanohiarisoamanana FJ, Yamashiro T, Iwasaki M, Kawamoto K, Ihara I, Umetsu K (2018) Comparative fertilizer properties of digestates from mesophilic and thermophilic anaerobic digestion of dairy manure: focusing on plant growth promoting bacteria (PGPB) and environmental risk. J Mater Cycles Waste. https://doi.org/10.1007/s10163-018-0708-7

    Google Scholar 

Download references

Acknowledgements

This study was supported in part by a Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan (No. 10670499).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kazutaka Umetsu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Iwasaki, M., Miyake, M., Maseda, H. et al. Thermophilic anaerobic digestion is an effective treatment for reducing cefazolin-resistant bacteria and ESBL-producers in dairy manure. J Mater Cycles Waste Manag 21, 293–299 (2019). https://doi.org/10.1007/s10163-018-0789-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10163-018-0789-3

Keywords

Navigation