Skip to main content

Investigating the relationship between extended spectrum β-lactamase producing Escherichia coli in the environment and food chains with the presence of this infection in people suspected of septicemia: Using the fuzzy set qualitative comparative analysis

Journal of Environmental Health Science and Engineering volume 18, pages 1509–1520 (2020)Cite this article

Abstract

Propose

Among antibiotic resistance cases, resistance to β-lactam antibiotics is a major concern for the treatment of microbial infections. Furthermore, the prevalence of extended-spectrum β-lactamases (ESBL) Escherichia coli (E. coli) in environment, food, and human resources of Iran has increased over the past few years. This study aimed to predict the relationship between the prevalence of ESBL E. coli in the environment and the food chains with the presence of this infection in people suspected of septicemia using fuzzy set qualitative comparative analysis model.

Methods

In this analytical cross sectional study samples were collected from the environment (hospital sewage, downstream and upstream urban sewage, and slaughterhouse sewage), food (chicken), and human chains (people suspected of septicemia) in Tehran province, Iran. This study was conducted from September to February 2019 and the prevalence of ESBL E. coli was calculated in each resource. Then, the relationship between the prevalence of ESBL E. coli in the environment and food chains and its prevalence in the human chain was predicted using the fuzzy set qualitative comparative analysis.

Results

The results showed the prevalence of ESBL E. coli in those suspected of septicemia in September, October, November, December, January and February was 58.1%, 60%, 33.3%, 100%, 43%, and 57.8%, respectively. Also, the results of the fuzzy set qualitative comparative analysis indicated hospital wastewater and chicken contamination with ESBL E. coli were the main causes of contamination with ESBL E. coli in people suspected of septicemia.

Conclusions

According to the results of this study, if there is a contamination of hospital wastewater and chickens in an area, it can be claimed that people suspected of septicemia are infected with ESBL E. coli, and the percentage of this contamination can be high. On the other hand, controlling ESBL E. coli in hospital wastewater (environmental chain) and chickens (food chain) can prevent contamination in people with suspected septicemia.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Wall S. Prevention of antibiotic resistance–an epidemiological scoping review to identify research categories and knowledge gaps. Glob Health Action. 2019;12(sup1):1756191.

    Article  Google Scholar 

  2. Smith RA, M’ikanatha NM, Read AF. Antibiotic resistance: a primer and call to action. Health Commun. 2015;30(3):309–14.

    Article  Google Scholar 

  3. Chen J-S, Ni C-F, Liang C-P, Chiang C-C. Analytical power series solution for contaminant transport with hyperbolic asymptotic distance-dependent dispersivity. J Hydrol. 2008;362(1–2):142–9.

    Article  Google Scholar 

  4. Chen J-S, Chen J-T, Liu C-W, Liang C-P, Lin C-W. Analytical solutions to two-dimensional advection–dispersion equation in cylindrical coordinates in finite domain subject to first-and third-type inlet boundary conditions. J Hydrol. 2011;405(3–4):522–31.

    Article  Google Scholar 

  5. Escudero E, Vinue L, Teshager T, Torres C, Moreno M. Resistance mechanisms and farm-level distribution of fecal Escherichia coli isolates resistant to extended-spectrum cephalosporins in pigs in Spain. Res Vet Sci. 2010;88(1):83–7.

    CAS  Article  Google Scholar 

  6. Blanc V, Mesa R, Saco M, Lavilla S, Prats G, Miró E, et al. ESBL-and plasmidic class C β-lactamase-producing E. coli strains isolated from poultry, pig and rabbit farms. Vet Microbiol. 2006;118(3–4):299–304.

  7. Bortolaia V, Guardabassi L, Trevisani M, Bisgaard M, Venturi L, Bojesen AM. High diversity of extended-spectrum β-lactamases in Escherichia coli isolates from Italian broiler flocks. Antimicrob Agents Chemother. 2010;54(4):1623–6.

    CAS  Article  Google Scholar 

  8. Randall L, Clouting C, Horton R, Coldham N, Wu G, Clifton-Hadley F, et al. Prevalence of Escherichia coli carrying extended-spectrum β-lactamases (CTX-M and TEM-52) from broiler chickens and turkeys in Great Britain between 2006 and 2009. J Antimicrob Chemother. 2011;66(1):86–95.

    CAS  Article  Google Scholar 

  9. Girlich D, Poirel L, Carattoli A, Kempf I, Lartigue M-F, Bertini A, et al. Extended-spectrum β-lactamase CTX-M-1 in Escherichia coli isolates from healthy poultry in France. Appl Environ Microbiol. 2007;73(14):4681–5.

    CAS  Article  Google Scholar 

  10. Gonçalves A, Torres C, Silva N, Carneiro C, Radhouani H, Coelho C, et al. Genetic characterization of extended-spectrum beta-lactamases in Escherichia coli isolates of pigs from a Portuguese intensive swine farm. Foodborne Pathog Dis. 2010;7(12):1569–73.

    Article  Google Scholar 

  11. Aminzadeh Z, Kashi MS, Shaabani M. Bacteriuria by extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolates in a governmental hospital in south of Tehran, Iran. 2008.

  12. Maxwell JA. Using qualitative methods for causal explanation. Field Methods. 2004;16(3):243–64.

    Article  Google Scholar 

  13. Miethe TD, Drass KA. Exploring the social context of instrumental and expressive homicides: An application of qualitative comparative analysis. J Quant Criminol. 1999;15(1):1–21.

    Article  Google Scholar 

  14. Schweizer T. Actor and event orderings across time: Lattice representation and Boolean analysis of the political disputes in Chen Village, China. Soc Netw. 1996;18(3):247–66.

    Article  Google Scholar 

  15. Aspinall LJ, Kilsby DC. A microbiological quality control procedure based on tube counts. J Appl Bacteriol. 1979;46(2):325–9.

  16. Zhi S, Banting G, Stothard P, Ashbolt NJ, Checkley S, Meyer K, et al. Evidence for the evolution, clonal expansion and global dissemination of water treatment-resistant naturalized strains of Escherichia coli in wastewater. Water Res. 2019;156:208–22.

    CAS  Article  Google Scholar 

  17. Uzoechi SC, Abu-Lail NI. Changes in cellular elasticities and conformational properties of bacterial surface biopolymers of multidrug-resistant Escherichia coli (MDR-E. coli) strains in response to ampicillin. Cell Surf. 2019;5:100019.

  18. Sahu C, Jain V, Mishra P, Prasad KN. Clinical and laboratory standards institute versus European committee for antimicrobial susceptibility testing guidelines for interpretation of carbapenem antimicrobial susceptibility results for Escherichia coli in urinary tract infection (UTI). J Lab Phys. 2018;10(3):289.

    CAS  Google Scholar 

  19. Perez VP, Carvalho JK, de Oliveira MS, Rossato AM, Dani C, Corção G, d’Azevedo PA. Coagulase-negative staphylococci in outpatient routines: the implications of switching from CLSI to BrCAST/EUCAST guidelines. Braz J Microbiol. 2020;23:1–8.

  20. Ragin CC, Berg-Schlosser D, De Meur G. Political methodology: Qualitative methods. A new handbook of political science. 1996;10:749–68.

  21. Douglas EJ, Shepherd DA, Prentice C. Using fuzzy-set qualitative comparative analysis for a finer-grained understanding of entrepreneurship. J Bus Ventur. 2020;35(1):105970.

    Article  Google Scholar 

  22. de Guinea AO, Raymond L. Enabling innovation in the face of uncertainty through IT ambidexterity: A fuzzy set qualitative comparative analysis of industrial service SMEs. Int J Inf Manag. 2020;50:244–60.

    Article  Google Scholar 

  23. Ragin CC. Qualitative comparative analysis using fuzzy sets (fsQCA). Configurational comparative methods: Qualitative comparative analysis (QCA) and related techniques. 2009;51:87–121.

  24. Berg-Schlosser D, De Meur G, Rihoux B, Ragin CC. Qualitative comparative analysis (QCA) as an approach. Configurational comparative methods: Qualitative comparative analysis (QCA) and related techniques. 2009;1:18.

  25. Ragin CC. The comparative method: Moving beyond qualitative and quantitative strategies. Berkeley: Univ of California Press; 2014.

  26. Mudryk ZJ. Occurrence and distribution antibiotic resistance of heterotrophic bacteria isolated from a marine beach. Mar Pollut Bull. 2005;50(1):80–6.

    CAS  Article  Google Scholar 

  27. Iversen A, Kühn I, Franklin A, Möllby R. High prevalence of vancomycin-resistant enterococci in Swedish sewage. Appl Environ Microbiol. 2002;68(6):2838–42.

    CAS  Article  Google Scholar 

  28. Homem V, Santos L. Degradation and removal methods of antibiotics from aqueous matrices–a review. J Environ Manag. 2011;92(10):2304–47.

    CAS  Article  Google Scholar 

  29. Thomas KV, Bijlsma L, Castiglioni S, Covaci A, Emke E, Grabic R, et al. Comparing illicit drug use in 19 European cities through sewage analysis. Sci Total Environ. 2012;432:432–9.

    CAS  Article  Google Scholar 

  30. Varela AR, Ferro G, Vredenburg J, Yanık M, Vieira L, Rizzo L, et al. Vancomycin resistant enterococci: from the hospital effluent to the urban wastewater treatment plant. Sci Total Environ. 2013;450:155–61.

    Article  Google Scholar 

  31. Al-Ahmad A, Daschner F, Kümmerer K. Biodegradability of cefotiam, ciprofloxacin, meropenem, penicillin G, and sulfamethoxazole and inhibition of waste water bacteria. Arch Environ Contam Toxicol. 1999;37(2):158–63.

    CAS  Article  Google Scholar 

  32. Kümmerer K. Significance of antibiotics in the environment. J Antimicrob Chemother. 2003;52(1):5–7.

    Article  Google Scholar 

  33. Kümmerer K. Resistance in the environment. J Antimicrob Chemother. 2004;54(2):311–20.

    Article  Google Scholar 

  34. Kümmerer K, Alexy R, Hüttig J, Schöll A. Standardized tests fail to assess the effects of antibiotics on environmental bacteria. Water Res. 2004;38(8):2111–6.

    Article  Google Scholar 

  35. Guerrero JP, Skaggs T. Analytical solution for one-dimensional advection–dispersion transport equation with distance-dependent coefficients. J Hydrol. 2010;390(1–2):57–65.

    Article  Google Scholar 

  36. Alexy R, Sommer A, Lange FT, Kümmerer K. Local use of antibiotics and their input and fate in a small sewage treatment plant–significance of balancing and analysis on a local scale vs. nationwide scale. Acta Hydrochim Hydrobiol. 2006;34(6):587–92.

  37. Dehghanzadeh RR, Roshani M. Determination of antibiotic farshchianm. resistance spectrum in enterobacteriaceae andstaphylococcus bacteria isolated from hospital wastewaters in Tabriz, 2015. 2018.

  38. Reihani RD, Roshani M, Farshchian MR. Determination of Antibiotic Resistance Spectrum in Enterobacteriaceae and Staphylococcus Bacteria Isolated from Hospital Wastewaters in Tabriz, 2015. Majallah-i pizishki-i Danishgah-i Ulum-i Pizishki va Khadamat-i Bihdashti-i Darmani-i Tabriz. 2018;40(4):24–30.

  39. Hadi M, Shokoohi R, Ebrahimzadeh Namvar A, Karimi M, Solaimany Aminabad M. Antibiotic resistance of isolated bacteria from urban and hospital wastewaters in Hamadan City. Iran J Health Environ. 2011;4(1):105–14.

    Google Scholar 

Download references

Acknowledgements

This paper was derived from a PhD thesis in the Department of Epidemiology, School of Public Health, Iran Medical Sciences University.

Author information

Affiliations

  1. Preventive Medicine and Public Health Research Center, Iran University of Medical Sciences, Tehran, Iran

    Babak Eshrati

  2. Department of Epidemiology, School of Public Health, University of Medical Sciences, Tehran, Iran

    Hamid Reza Baradaran, Seyed Abbas Motevalian & Yousef Moradi

  3. Antimicrobial Resistance Research Center, Institute of Immunology and Infectious Diseases, Iran University of Medical Sciences, Tehran, Iran

    Ali Majidpour, Mina Boustanshenas & Somayeh Soleymanzadeh Moghadam

Authors
  1. Babak Eshrati
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hamid Reza Baradaran
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seyed Abbas Motevalian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ali Majidpour
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mina Boustanshenas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Somayeh Soleymanzadeh Moghadam
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yousef Moradi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YM, BE, and HB contributed to the conception and design of the study, interpretation of data, literature review, modeling, and writing and revising the manuscript. SAM and AM contributed to the acquisition of data. MB and SSM performed all the microbial assays.

Corresponding authors

Correspondence to Hamid Reza Baradaran or Yousef Moradi.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest. This study was supported by the Deputy of Research and Technology of Iran University of Medical Sciences, Tehran, Iran (Grant no. 15,396 and ethical code: IR.IUMS.REC.1398.679).

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Eshrati, B., Baradaran, H.R., Motevalian, S.A. et al. Investigating the relationship between extended spectrum β-lactamase producing Escherichia coli in the environment and food chains with the presence of this infection in people suspected of septicemia: Using the fuzzy set qualitative comparative analysis. J Environ Health Sci Engineer 18, 1509–1520 (2020). https://doi.org/10.1007/s40201-020-00567-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40201-020-00567-9

Keywords

  • Extended spectrum β-lactamase producing
  • Escherichia coli
  • Food chain
  • Human chain
  • Environment chain
  • Fuzzy set qualitative comparative analysis