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Abstract

Background

The rapid increase of bacterial antibiotic resistance could soon render our most effective method to address infections obsolete. Factors influencing pathogen resistance prevalence in human populations remain poorly described, though temperature is known to contribute to mechanisms of spread.

Aim

To quantify the role of temperature, spatially and temporally, as a mechanistic modulator of transmission of antibiotic resistant microbes.

Methods

An ecologic analysis was performed on country-level antibiotic resistance prevalence in three common bacterial pathogens across 28 European countries, collectively representing over 4 million tested isolates. Associations of minimum temperature and other predictors with change in antibiotic resistance rates over 17 years (2000–2016) were evaluated with multivariable models. The effects of predictors on the antibiotic resistance rate change across geographies were quantified.

Results

During 2000–2016, for and , European countries with 10°C warmer ambient minimum temperatures compared to others, experienced more rapid resistance increases across all antibiotic classes. Increases ranged between 0.33%/year (95% CI: 0.2 to 0.5) and 1.2%/year (95% CI: 0.4 to 1.9), even after accounting for recognised resistance drivers including antibiotic consumption and population density. For a decreasing relationship of −0.4%/year (95% CI:  −0.7 to 0.0) was found for meticillin resistance, reflecting widespread declines in meticillin-resistant across Europe over the study period.

Conclusion

We found evidence of a long-term effect of ambient minimum temperature on antibiotic resistance rate increases in Europe. Ambient temperature might considerably influence antibiotic resistance growth rates, and explain geographic differences observed in cross-sectional studies. Rising temperatures globally may hasten resistance spread, complicating mitigation efforts.

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2020-11-12
2024-12-18
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References

  1. Lipsitch M, Samore MH. Antimicrobial use and antimicrobial resistance: a population perspective. Emerg Infect Dis. 2002;8(4):347-54.  https://doi.org/10.3201/eid0804.010312  PMID: 11971765 
  2. Barbosa TM, Levy SB. The impact of antibiotic use on resistance development and persistence. Drug Resist Updat. 2000;3(5):303-11.  https://doi.org/10.1054/drup.2000.0167  PMID: 11498398 
  3. McCarthy M. Science academies of G7 nations call for action on antibiotic resistance and neglected tropical diseases. BMJ. 2015;350(apr30 11):h2346-2346.  https://doi.org/10.1136/bmj.h2346  PMID: 25929670 
  4. Nathan C, Cars O. Antibiotic resistance--problems, progress, and prospects. N Engl J Med. 2014;371(19):1761-3.  https://doi.org/10.1056/NEJMp1408040  PMID: 25271470 
  5. Tornimbene B, Eremin S, Escher M, Griskeviciene J, Manglani S, Pessoa-Silva CL. WHO Global Antimicrobial Resistance Surveillance System early implementation 2016-17. Lancet Infect Dis. 2018;18(3):241-2.  https://doi.org/10.1016/S1473-3099(18)30060-4  PMID: 29396007 
  6. Berendonk TU, Manaia CM, Merlin C, Fatta-Kassinos D, Cytryn E, Walsh F, et al. Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol. 2015;13(5):310-7.  https://doi.org/10.1038/nrmicro3439  PMID: 25817583 
  7. Martínez JL. Antibiotics and antibiotic resistance genes in natural environments. Science. 2008;321(5887):365-7.  https://doi.org/10.1126/science.1159483  PMID: 18635792 
  8. Morris AM, Calderwood MS, Fridkin SK, Livorsi DJ, McGregor JC, Mody L, et al. Research needs in antibiotic stewardship. Infect Control Hosp Epidemiol. 2019;40(12):1334-43.  https://doi.org/10.1017/ice.2019.276  PMID: 31662139 
  9. Ratkowsky DA, Olley J, McMeekin TA, Ball A. Relationship between temperature and growth rate of bacterial cultures. J Bacteriol. 1982;149(1):1-5.  https://doi.org/10.1128/JB.149.1.1-5.1982  PMID: 7054139 
  10. Walsh TR, Weeks J, Livermore DM, Toleman MA. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis. 2011;11(5):355-62.  https://doi.org/10.1016/S1473-3099(11)70059-7  PMID: 21478057 
  11. Kaier K, Frank U, Conrad A, Meyer E. Seasonal and ascending trends in the incidence of carriage of extended-spectrum ß-lactamase-producing Escherichia coli and Klebsiella species in 2 German hospitals. Infect Control Hosp Epidemiol. 2010;31(11):1154-9.  https://doi.org/10.1086/656748  PMID: 20849274 
  12. Babinszky L, Halas V, Verstegen MWA. Impacts of Climate Change on Animal Production and Quality of Animal Food Products. in Climate Change – Socioeconomic Effects. 2011.  https://doi.org/10.5772/23840 
  13. The Lancet Infectious Diseases. The Lancet Infectious Diseases. Climate change: the role of the infectious disease community. Lancet Infect Dis. 2017;17(12):1219.  https://doi.org/10.1016/S1473-3099(17)30645-X 
  14. MacFadden DR, McGough SF, Fisman D, Santillana M, Brownstein JS. Antibiotic Resistance Increases with Local Temperature. Nat Clim Chang. 2018;8(6):510-4.  https://doi.org/10.1038/s41558-018-0161-6  PMID: 30369964 
  15. Weist K, Högberg LD. ECDC publishes 2015 surveillance data on antimicrobial resistance and antimicrobial consumption in Europe. Euro Surveill. 2016;21(46):30399.  https://doi.org/10.2807/1560-7917.ES.2016.21.46.30399  PMID: 27918266 
  16. European Centre for Disease Prevention and Control (ECDC). Surveillance Atlas of Infectious Diseases. Stockholm: ECDC; 2016. Available from: http://atlas.ecdc.europa.eu/public/
  17. European Centre for Disease Prevention and Control (ECDC). European Surveillance of Antimicrobial Consumption Network (ESAC-Net). Stockholm: ECDC; 2018. Available from: https://ecdc.europa.eu/en/about-us/partnerships-and-networks/disease-and-laboratory-networks/esac-net
  18. Clarke A, Morris GJ, Fonseca F, Murray BJ, Acton E, Price HC. A Low Temperature Limit for Life on Earth. PLoS One. 2013;8(6):e66207.  https://doi.org/10.1371/journal.pone.0066207  PMID: 23840425 
  19. Sutherst RW. Global change and human vulnerability to vector-borne diseases. Clin Microbiol Rev. 2004;17(1):136-73.  https://doi.org/10.1128/CMR.17.1.136-173.2004  PMID: 14726459 
  20. Gelaro R, McCarty W, Suárez MJ, Todling R, Molod A, Takacs L, et al. The Modern-Era Retrospective Analysis for Research and Applications, Version 2 (MERRA-2). J Clim. 2017;30(13):5419-54.  https://doi.org/10.1175/JCLI-D-16-0758.1  PMID: 32020988 
  21. R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013. Available from: http://www.R-project.org/
  22. Goossens H, Ferech M, Vander Stichele R, Elseviers M, ESAC Project Group. Outpatient antibiotic use in Europe and association with resistance: a cross-national database study. Lancet. 2005;365(9459):579-87.  https://doi.org/10.1016/S0140-6736(05)70799-6  PMID: 15708101 
  23. Köck R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J, et al. Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Euro Surveill. 2010;15(41):19688.  https://doi.org/10.2807/ese.15.41.19688-en  PMID: 20961515 
  24. Kaba HEJ, Kuhlmann E, Scheithauer S. Thinking outside the box: Association of antimicrobial resistance with climate warming in Europe - A 30 country observational study. Int J Hyg Environ Health. 2020;223(1):151-8.  https://doi.org/10.1016/j.ijheh.2019.09.008  PMID: 31648934 
  25. Alvarez-Uria G, Midde M. Trends and factors associated with antimicrobial resistance of Acinetobacter spp. invasive isolates in Europe: A country-level analysis. J Glob Antimicrob Resist. 2018;14:29-32.  https://doi.org/10.1016/j.jgar.2018.05.024  PMID: 29879490 
  26. Collignon P, Beggs JJ, Walsh TR, Gandra S, Laxminarayan R. Anthropological and socioeconomic factors contributing to global antimicrobial resistance: a univariate and multivariable analysis. Lancet Planet Health. 2018;2(9):e398-405.  https://doi.org/10.1016/S2542-5196(18)30186-4  PMID: 30177008 
  27. Compare. Global Sewage Surveillance Project. Compare Europe. [Accessed: 23 May 2018]. Available from: http://www.compare-europe.eu/Library/Global-Sewage-Surveillance-Project
  28. Robinson TP, Bu DP, Carrique-Mas J, Fèvre EM, Gilbert M, Grace D, et al. Antibiotic resistance is the quintessential One Health issue. Trans R Soc Trop Med Hyg. 2016;110(7):377-80.  https://doi.org/10.1093/trstmh/trw048  PMID: 27475987 
  29. Holmes AH, Moore LSP, Sundsfjord A, Steinbakk M, Regmi S, Karkey A, et al. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet. 2016;387(10014):176-87.  https://doi.org/10.1016/S0140-6736(15)00473-0  PMID: 26603922 
  30. Relman DA, Guttmacher AE, Relman DA. Microbial genomics and infectious diseases. N Engl J Med. 2011;365(4):347-57.  https://doi.org/10.1056/NEJMra1003071  PMID: 21793746 
  31. Surette MD, Wright GD. Lessons from the Environmental Antibiotic Resistome. Annu Rev Microbiol. 2017;71(1):309-29.  https://doi.org/10.1146/annurev-micro-090816-093420  PMID: 28657887 
  32. MacFadden DR, Fisman DN, Hanage WP, Lipsitch M. The Relative Impact of Community and Hospital Antibiotic Use on the Selection of Extended-Spectrum Beta-lactamase-Producing Escherichia coli. Clin Infect Dis. 2018.  https://doi.org/10.1093/cid/ciy978  PMID: 30462185 
  33. Wang A, Daneman N, Tan C, Brownstein JS, MacFadden DR. Evaluating the Relationship Between Hospital Antibiotic Use and Antibiotic Resistance in Common Nosocomial Pathogens. Infect Control Hosp Epidemiol. 2017;38(12):1457-63.  https://doi.org/10.1017/ice.2017.222  PMID: 29072150 
  34. Change IC. The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. USA: Cambridge University Press; 2013.
  35. O’Neill J. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations. Welcome Trust. May 2016. Available from: https://wellcomecollection.org/works/thvwsuba/items?sierraId=b28644797&langCode=eng&canvas=1
  36. Woolhouse M, Waugh C, Perry MR, Nair H. Global disease burden due to antibiotic resistance - state of the evidence. J Glob Health. 2016;6(1):010306.  https://doi.org/10.7189/jogh.06.010306  PMID: 27350872 
  37. Abat C, Rolain J-M, Dubourg G, Fournier P-E, Chaudet H, Raoult D. Evaluating the Clinical Burden and Mortality Attributable to Antibiotic Resistance: The Disparity of Empirical Data and Simple Model Estimations. Clin Infect Dis. 2017;65(suppl_1):S58-63.  https://doi.org/10.1093/cid/cix346  PMID: 28859341 
  38. Tillotson GS, Zinner SH. Burden of antimicrobial resistance in an era of decreasing susceptibility. Expert Rev Anti Infect Ther. 2017;15(7):663-76.  https://doi.org/10.1080/14787210.2017.1337508  PMID: 28580804 
Rates of increase of antibiotic resistance and ambient temperature in Europe: a cross-national analysis of 28 countries between 2000 and 2016
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Sarah+F+McGough&option1=author&noRedirect=true" class="nonDisambigAuthorLink">McGough Sarah F</a>, <a href="/search?value1=Derek+R+MacFadden&option1=author&noRedirect=true" class="nonDisambigAuthorLink">MacFadden Derek R</a>, <a href="/search?value1=Mohammad+W+Hattab&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Hattab Mohammad W</a>, <a href="/search?value1=K%C3%A5re+M%C3%B8lbak&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Mølbak Kåre</a>, <a href="/search?value1=Mauricio+Santillana&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Santillana Mauricio</a></span>. Rates of increase of antibiotic resistance and ambient temperature in Europe: a cross-national analysis of 28 countries between 2000 and 2016. <a href="/content/ecdc">Euro Surveill.</a> 2020;25(45):pii=1900414. <a href="https://doi.org/10.2807/1560-7917.ES.2020.25.45.1900414" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2020.25.45.1900414</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 24 Jun 2019;&nbsp;&nbsp; <span class="generated">Accepted</span>: 02 Feb 2020 </span> </p>
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