Increasing incidence and antimicrobial resistance in Escherichia coli bloodstream infections: a multinational population-based cohort study

doi:10.1186/s13756-021-00999-4

Multicenter Study

. 2021 Sep 6;10(1):131.

doi: 10.1186/s13756-021-00999-4.

Increasing incidence and antimicrobial resistance in Escherichia coli bloodstream infections: a multinational population-based cohort study

Melissa C MacKinnon¹, Scott A McEwen², David L Pearl², Outi Lyytikäinen³, Gunnar Jacobsson^{4

5}, Peter Collignon^{6

7}, Daniel B Gregson^{8

9}, Louis Valiquette¹⁰, Kevin B Laupland^{11

12

13}

Affiliations

¹ Department of Population Medicine, University of Guelph, 50 Stone Rd E, Guelph, ON, N1G 2W1, Canada. mmacki05@uoguelph.ca.
² Department of Population Medicine, University of Guelph, 50 Stone Rd E, Guelph, ON, N1G 2W1, Canada.
³ Department of Health Security, National Institute for Health and Welfare, Helsinki, Finland.
⁴ Department of Infectious Diseases, Skaraborg Hospital, Skövde, Sweden.
⁵ CARe - Center for Antibiotic Resistance Research, Institute of Biomedicine, University of Gothenburg, Gothenburg, Sweden.
⁶ Department of Infectious Disease and Microbiology, The Canberra Hospital, Garran, ACT, Australia.
⁷ Medical School, Australian National University, Acton, ACT, Australia.
⁸ Departments of Medicine, and Pathology and Laboratory Medicine, University of Calgary, Calgary, AB, Canada.
⁹ Alberta Health Services, Calgary Zone, Calgary, AB, Canada.
¹⁰ Department of Microbiology-Infectious Diseases, Université de Sherbrooke, Sherbrooke, QC, Canada.
¹¹ Department of Medicine, Royal Inland Hospital, Kamloops, BC, Canada.
¹² Department of Intensive Care Medicine, Royal Brisbane and Women's Hospital, Brisbane, QLD, Australia.
¹³ Faculty of Health, Queensland University of Technology (QUT), Brisbane, QLD, Australia.

PMID: 34488891
PMCID: PMC8422618
DOI: 10.1186/s13756-021-00999-4

Multicenter Study

Increasing incidence and antimicrobial resistance in Escherichia coli bloodstream infections: a multinational population-based cohort study

Melissa C MacKinnon et al. Antimicrob Resist Infect Control. 2021.

. 2021 Sep 6;10(1):131.

doi: 10.1186/s13756-021-00999-4.

Authors

Affiliations

¹ Department of Population Medicine, University of Guelph, 50 Stone Rd E, Guelph, ON, N1G 2W1, Canada. mmacki05@uoguelph.ca.
² Department of Population Medicine, University of Guelph, 50 Stone Rd E, Guelph, ON, N1G 2W1, Canada.
³ Department of Health Security, National Institute for Health and Welfare, Helsinki, Finland.
⁴ Department of Infectious Diseases, Skaraborg Hospital, Skövde, Sweden.
⁵ CARe - Center for Antibiotic Resistance Research, Institute of Biomedicine, University of Gothenburg, Gothenburg, Sweden.
⁶ Department of Infectious Disease and Microbiology, The Canberra Hospital, Garran, ACT, Australia.
⁷ Medical School, Australian National University, Acton, ACT, Australia.
⁸ Departments of Medicine, and Pathology and Laboratory Medicine, University of Calgary, Calgary, AB, Canada.
⁹ Alberta Health Services, Calgary Zone, Calgary, AB, Canada.
¹⁰ Department of Microbiology-Infectious Diseases, Université de Sherbrooke, Sherbrooke, QC, Canada.
¹¹ Department of Medicine, Royal Inland Hospital, Kamloops, BC, Canada.
¹² Department of Intensive Care Medicine, Royal Brisbane and Women's Hospital, Brisbane, QLD, Australia.
¹³ Faculty of Health, Queensland University of Technology (QUT), Brisbane, QLD, Australia.

PMID: 34488891
PMCID: PMC8422618
DOI: 10.1186/s13756-021-00999-4

Abstract

Background: Escherichia coli is an important pathogen in humans and is the most common cause of bacterial bloodstream infections (BSIs). The objectives of our study were to determine factors associated with E. coli BSI incidence rate and third-generation cephalosporin resistance in a multinational population-based cohort.

Methods: We included all incident E. coli BSIs (2014-2018) from national (Finland) and regional (Australia [Canberra], Sweden [Skaraborg], and Canada [Calgary, Sherbrooke, and western interior]) surveillance. Incidence rates were directly age and sex standardized to the European Union 28-country 2018 population. Multivariable negative binomial and logistic regression models estimated factors significantly associated with E. coli BSI incidence rate and third-generation cephalosporin resistance, respectively. The explanatory variables considered for inclusion in both models were year (2014-2018), region (six areas), age (< 70-years-old and ≥ 70-years-old), and sex (female and male).

Results: We identified 31,889 E. coli BSIs from 40.7 million person-years of surveillance. Overall and third-generation cephalosporin-resistant standardized rates were 87.1 and 6.6 cases/100,000 person-years, respectively, and increased 14.0% and 40.1% over the five-year study. Overall, 7.8% (2483/31889) of E. coli BSIs were third-generation cephalosporin-resistant. Calgary, Canberra, Sherbrooke, and western interior had significantly lower E. coli BSI rates compared to Finland. The significant association between age and E. coli BSI rate varied with sex. Calgary, Canberra, and western interior had significantly greater odds of third-generation cephalosporin-resistant E. coli BSIs compared to Finland. Compared to 2014, the odds of third-generation cephalosporin-resistant E. coli BSIs were significantly increased in 2016, 2017, and 2018. The significant association between age and the odds of having a third-generation cephalosporin-resistant E. coli BSI varied with sex.

Conclusions: Increases in overall and third-generation cephalosporin-resistant standardized E. coli BSI rates were clinically important. Overall, E. coli BSI incidence rates were 40-104% greater than previous investigations from the same study areas. Region, sex, and age are important variables when analyzing E. coli BSI rates and third-generation cephalosporin resistance in E. coli BSIs. Considering E. coli is the most common cause of BSIs, this increasing burden and evolving third-generation cephalosporin resistance will have an important impact on human health, especially in aging populations.

Keywords: Antimicrobial resistance; Bacteremia; Bloodstream infection; Escherichia coli; Incidence rate; Population-based; Third-generation cephalosporins.

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Conflict of interest statement

MCM reports a scholarship from the Canadian Institutes of Health Research and funding for a Federal Student Work Experience Program placement from the Government of Canada—Genome Research Development Initiative, both related to her PhD program and outside the submitted work. LV reports being a stock holder of Lumed Inc., outside the submitted work. All other authors declare that they have no competing interests.

Figures

**Fig. 1**
Number of *E. coli* bloodstream infections by age category and sex

**Fig. 2**
Directly age and sex standardized *E. coli* bloodstream infection incidence rates by area^a,b. a Overall, and third-generation cephalosporin-resistant and -susceptible standardized incidence rates by area^a,b. b Third-generation cephalosporin-resistant standardized incidence rates by area^a,b. *3GC-R* Third-generation cephalosporin-resistant; *3GC-S* Third-generation cephalosporin-susceptible. ^aStandard population—European Union 28-country 2018 population. ^bStandardized *E. coli* bloodstream infection rates by area are available in Additional file 4

**Fig. 3**
Directly age and sex standardized *E. coli* bloodstream infection incidence rates by year^a,b. a Overall, and third-generation cephalosporin-resistant and -susceptible standardized incidence rates by year^a,b. b Third-generation cephalosporin-resistant standardized incidence rates by year^a,b. *3GC-R* Third-generation cephalosporin-resistant; *3GC-S* Third-generation cephalosporin-susceptible. ^aStandard population—European Union 28-country 2018 population. ^bStandardized *E. coli* bloodstream infection rates by year are available in Additional file 4

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References

1. Skogberg K, Lyytikainen O, Ollgren J, Nuorti JP, Ruutu P. Population-based burden of bloodstream infections in Finland. Clin Microbiol Infect. 2012;18(6):E170–E176. doi: 10.1111/j.1469-0691.2012.03845.x. - DOI - PubMed
1. Nielsen SL, Pedersen C, Jensen TG, Gradel KO, Kolmos HJ, Lassen AT. Decreasing incidence rates of bacteremia: a 9-year population-based study. J Infect. 2014;69(1):51–59. doi: 10.1016/j.jinf.2014.01.014. - DOI - PubMed
1. Bonten M, Johnson JR, van den Biggelaar AHJ, Georgalis L, Geurtsen J, de Palacios PI, et al. Epidemiology of Escherichia coli bacteremia: a systematic literature review. Clin Infect Dis. 2020;72(7):1211–1219. doi: 10.1093/cid/ciaa210. - DOI - PubMed
1. Kennedy KJ, Roberts JL, Collignon PJ. Escherichia coli bacteraemia in Canberra: incidence and clinical features. Med J Aust. 2008;188(4):209–213. doi: 10.5694/j.1326-5377.2008.tb01586.x. - DOI - PubMed
1. Laupland KB, Gregson DB, Church DL, Ross T, Pitout JDD. Incidence, risk factors and outcomes of Escherichia coli bloodstream infections in a large Canadian region. Clin Microbiol Infect. 2008;14(11):1041–1047. doi: 10.1111/j.1469-0691.2008.02089.x. - DOI - PubMed

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[1] Skogberg K, Lyytikainen O, Ollgren J, Nuorti JP, Ruutu P. Population-based burden of bloodstream infections in Finland. Clin Microbiol Infect. 2012;18(6):E170–E176. doi: 10.1111/j.1469-0691.2012.03845.x. - DOI - PubMed

[2] Skogberg K, Lyytikainen O, Ollgren J, Nuorti JP, Ruutu P. Population-based burden of bloodstream infections in Finland. Clin Microbiol Infect. 2012;18(6):E170–E176. doi: 10.1111/j.1469-0691.2012.03845.x. - DOI - PubMed

[3] Nielsen SL, Pedersen C, Jensen TG, Gradel KO, Kolmos HJ, Lassen AT. Decreasing incidence rates of bacteremia: a 9-year population-based study. J Infect. 2014;69(1):51–59. doi: 10.1016/j.jinf.2014.01.014. - DOI - PubMed

[4] Nielsen SL, Pedersen C, Jensen TG, Gradel KO, Kolmos HJ, Lassen AT. Decreasing incidence rates of bacteremia: a 9-year population-based study. J Infect. 2014;69(1):51–59. doi: 10.1016/j.jinf.2014.01.014. - DOI - PubMed

[5] Bonten M, Johnson JR, van den Biggelaar AHJ, Georgalis L, Geurtsen J, de Palacios PI, et al. Epidemiology of Escherichia coli bacteremia: a systematic literature review. Clin Infect Dis. 2020;72(7):1211–1219. doi: 10.1093/cid/ciaa210. - DOI - PubMed

[6] Bonten M, Johnson JR, van den Biggelaar AHJ, Georgalis L, Geurtsen J, de Palacios PI, et al. Epidemiology of Escherichia coli bacteremia: a systematic literature review. Clin Infect Dis. 2020;72(7):1211–1219. doi: 10.1093/cid/ciaa210. - DOI - PubMed

[7] Kennedy KJ, Roberts JL, Collignon PJ. Escherichia coli bacteraemia in Canberra: incidence and clinical features. Med J Aust. 2008;188(4):209–213. doi: 10.5694/j.1326-5377.2008.tb01586.x. - DOI - PubMed

[8] Kennedy KJ, Roberts JL, Collignon PJ. Escherichia coli bacteraemia in Canberra: incidence and clinical features. Med J Aust. 2008;188(4):209–213. doi: 10.5694/j.1326-5377.2008.tb01586.x. - DOI - PubMed

[9] Laupland KB, Gregson DB, Church DL, Ross T, Pitout JDD. Incidence, risk factors and outcomes of Escherichia coli bloodstream infections in a large Canadian region. Clin Microbiol Infect. 2008;14(11):1041–1047. doi: 10.1111/j.1469-0691.2008.02089.x. - DOI - PubMed

[10] Laupland KB, Gregson DB, Church DL, Ross T, Pitout JDD. Incidence, risk factors and outcomes of Escherichia coli bloodstream infections in a large Canadian region. Clin Microbiol Infect. 2008;14(11):1041–1047. doi: 10.1111/j.1469-0691.2008.02089.x. - DOI - PubMed

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Increasing incidence and antimicrobial resistance in Escherichia coli bloodstream infections: a multinational population-based cohort study

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Increasing incidence and antimicrobial resistance in Escherichia coli bloodstream infections: a multinational population-based cohort study

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Conflict of interest statement

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