Risk factors for bloodstream infections due to carbapenem-resistant Enterobacterales: a nested case-control-control study
Abstract Background Carbapenem-resistant Enterobacterales (CRE) bloodstream infections (BSIs) are a major threat to patients. To date, data on risk factors have been limited, with low internal and external validity. In this multicentre study, risk factors for CRE BSI were determined by comparison wi...
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creator | Zhou, Hongyu Buetti, Niccolò Pérez-Galera, Salvador Bravo-Ferrer, Jose Gutiérrez-Gutiérrez, Belén Paniagua-García, María Feifel, Jan Sauser, Julien Kostyanev, Tomi Canton, Rafael Tan, Lionel K Basoulis, Dimitris Pintado, Vicente Roilides, Emmanuel Dragovac, Gorana Torre-Cisneros, Julian Mediç, Deana Akova, Murat Goossens, Herman Bonten, Marc Harbarth, Stephan Rodriguez-Baño, Jesus De Kraker, Marlieke E A |
description | Abstract
Background
Carbapenem-resistant Enterobacterales (CRE) bloodstream infections (BSIs) are a major threat to patients. To date, data on risk factors have been limited, with low internal and external validity. In this multicentre study, risk factors for CRE BSI were determined by comparison with two control groups: patients with carbapenem-susceptible Enterobacterales (CSE) BSI, and patients without Enterobacterales infection (uninfected patients).
Methods
A multicentre, case-control-control study was nested in a European prospective cohort study on CRE (EURECA). CRE BSI:CSE BSI matching was 1:1, CRE BSI:Uninfected patients matching was 1:3, based on hospital, ward and length of stay. Conditional logistic regression was applied.
Results
From March 2016 to November 2018, 73 CRE BSIs, 73 CSE BSIs and 219 uninfected patients were included from 18 European hospitals. For CRE versus CSE BSI, previous CRE colonization/infection [incidence rate ratio (IRR) 7.32; 95% CI 1.65–32.38) increased the risk. For CRE versus uninfected controls, independent risk factors included: older age (IRR 1.03; 95% CI 1.01–1.06), patient referral (long-term care facility: IRR 7.19; 95% CI 1.51–34.24; acute care hospital: IRR 5.26; 95% CI 1.61–17.11), previous colonization/infection with other MDR organisms (MDROs) (IRR 9.71; 95% CI 2.33–40.56), haemodialysis (IRR 8.59; 95% CI 1.82–40.53), invasive procedures (IRR 5.66; 95% CI 2.11–15.16), and β-lactam/β-lactamase inhibitor combinations (IRR 3.92; 95% CI 1.68–9.13) or third/fourth generation cephalosporin (IRR 2.75; 95% CI 1.06–7.11) exposure within 3 months before enrolment.
Conclusions
Evidence of previous CRE colonization/infection was a major risk factor for carbapenem resistance among Enterobacterales BSI. Compared with uninfected patients, evidence of previous MDRO colonization/infection and healthcare exposure were important risk factors for CRE BSI. Targeted screening, infection prevention and antimicrobial stewardship should focus on these high-risk patients. |
doi_str_mv | 10.1093/jac/dkae157 |
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Background
Carbapenem-resistant Enterobacterales (CRE) bloodstream infections (BSIs) are a major threat to patients. To date, data on risk factors have been limited, with low internal and external validity. In this multicentre study, risk factors for CRE BSI were determined by comparison with two control groups: patients with carbapenem-susceptible Enterobacterales (CSE) BSI, and patients without Enterobacterales infection (uninfected patients).
Methods
A multicentre, case-control-control study was nested in a European prospective cohort study on CRE (EURECA). CRE BSI:CSE BSI matching was 1:1, CRE BSI:Uninfected patients matching was 1:3, based on hospital, ward and length of stay. Conditional logistic regression was applied.
Results
From March 2016 to November 2018, 73 CRE BSIs, 73 CSE BSIs and 219 uninfected patients were included from 18 European hospitals. For CRE versus CSE BSI, previous CRE colonization/infection [incidence rate ratio (IRR) 7.32; 95% CI 1.65–32.38) increased the risk. For CRE versus uninfected controls, independent risk factors included: older age (IRR 1.03; 95% CI 1.01–1.06), patient referral (long-term care facility: IRR 7.19; 95% CI 1.51–34.24; acute care hospital: IRR 5.26; 95% CI 1.61–17.11), previous colonization/infection with other MDR organisms (MDROs) (IRR 9.71; 95% CI 2.33–40.56), haemodialysis (IRR 8.59; 95% CI 1.82–40.53), invasive procedures (IRR 5.66; 95% CI 2.11–15.16), and β-lactam/β-lactamase inhibitor combinations (IRR 3.92; 95% CI 1.68–9.13) or third/fourth generation cephalosporin (IRR 2.75; 95% CI 1.06–7.11) exposure within 3 months before enrolment.
Conclusions
Evidence of previous CRE colonization/infection was a major risk factor for carbapenem resistance among Enterobacterales BSI. Compared with uninfected patients, evidence of previous MDRO colonization/infection and healthcare exposure were important risk factors for CRE BSI. Targeted screening, infection prevention and antimicrobial stewardship should focus on these high-risk patients.</description><identifier>ISSN: 0305-7453</identifier><identifier>ISSN: 1460-2091</identifier><identifier>EISSN: 1460-2091</identifier><identifier>DOI: 10.1093/jac/dkae157</identifier><identifier>PMID: 38988305</identifier><language>eng</language><publisher>UK: Oxford University Press</publisher><subject>Aged ; Aged, 80 and over ; Anti-Bacterial Agents - pharmacology ; Anti-Bacterial Agents - therapeutic use ; Bacteremia - epidemiology ; Bacteremia - microbiology ; Carbapenem-Resistant Enterobacteriaceae - drug effects ; Carbapenem-Resistant Enterobacteriaceae - isolation & purification ; Carbapenems - pharmacology ; Case-Control Studies ; Enterobacteriaceae Infections - epidemiology ; Enterobacteriaceae Infections - microbiology ; Europe - epidemiology ; Female ; Humans ; Male ; Middle Aged ; Original Research ; Prospective Studies ; Risk Factors</subject><ispartof>Journal of antimicrobial chemotherapy, 2024-09, Vol.79 (9), p.2132-2141</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy. 2024</rights><rights>The Author(s) 2024. Published by Oxford University Press on behalf of British Society for Antimicrobial Chemotherapy.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c301t-d33cf2e56bd912f859ce37b731441e2606c01706551395ac74058f82d002e85a3</cites><orcidid>0000-0002-9668-0770 ; 0000-0001-6732-9001 ; 0000-0002-6904-9473 ; 0000-0002-8096-1834 ; 0000-0003-0903-8614 ; 0000-0003-1675-3173</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,777,781,882,1579,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38988305$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhou, Hongyu</creatorcontrib><creatorcontrib>Buetti, Niccolò</creatorcontrib><creatorcontrib>Pérez-Galera, Salvador</creatorcontrib><creatorcontrib>Bravo-Ferrer, Jose</creatorcontrib><creatorcontrib>Gutiérrez-Gutiérrez, Belén</creatorcontrib><creatorcontrib>Paniagua-García, María</creatorcontrib><creatorcontrib>Feifel, Jan</creatorcontrib><creatorcontrib>Sauser, Julien</creatorcontrib><creatorcontrib>Kostyanev, Tomi</creatorcontrib><creatorcontrib>Canton, Rafael</creatorcontrib><creatorcontrib>Tan, Lionel K</creatorcontrib><creatorcontrib>Basoulis, Dimitris</creatorcontrib><creatorcontrib>Pintado, Vicente</creatorcontrib><creatorcontrib>Roilides, Emmanuel</creatorcontrib><creatorcontrib>Dragovac, Gorana</creatorcontrib><creatorcontrib>Torre-Cisneros, Julian</creatorcontrib><creatorcontrib>Mediç, Deana</creatorcontrib><creatorcontrib>Akova, Murat</creatorcontrib><creatorcontrib>Goossens, Herman</creatorcontrib><creatorcontrib>Bonten, Marc</creatorcontrib><creatorcontrib>Harbarth, Stephan</creatorcontrib><creatorcontrib>Rodriguez-Baño, Jesus</creatorcontrib><creatorcontrib>De Kraker, Marlieke E A</creatorcontrib><creatorcontrib>COMBACTE- EURECA project team</creatorcontrib><title>Risk factors for bloodstream infections due to carbapenem-resistant Enterobacterales: a nested case-control-control study</title><title>Journal of antimicrobial chemotherapy</title><addtitle>J Antimicrob Chemother</addtitle><description>Abstract
Background
Carbapenem-resistant Enterobacterales (CRE) bloodstream infections (BSIs) are a major threat to patients. To date, data on risk factors have been limited, with low internal and external validity. In this multicentre study, risk factors for CRE BSI were determined by comparison with two control groups: patients with carbapenem-susceptible Enterobacterales (CSE) BSI, and patients without Enterobacterales infection (uninfected patients).
Methods
A multicentre, case-control-control study was nested in a European prospective cohort study on CRE (EURECA). CRE BSI:CSE BSI matching was 1:1, CRE BSI:Uninfected patients matching was 1:3, based on hospital, ward and length of stay. Conditional logistic regression was applied.
Results
From March 2016 to November 2018, 73 CRE BSIs, 73 CSE BSIs and 219 uninfected patients were included from 18 European hospitals. For CRE versus CSE BSI, previous CRE colonization/infection [incidence rate ratio (IRR) 7.32; 95% CI 1.65–32.38) increased the risk. For CRE versus uninfected controls, independent risk factors included: older age (IRR 1.03; 95% CI 1.01–1.06), patient referral (long-term care facility: IRR 7.19; 95% CI 1.51–34.24; acute care hospital: IRR 5.26; 95% CI 1.61–17.11), previous colonization/infection with other MDR organisms (MDROs) (IRR 9.71; 95% CI 2.33–40.56), haemodialysis (IRR 8.59; 95% CI 1.82–40.53), invasive procedures (IRR 5.66; 95% CI 2.11–15.16), and β-lactam/β-lactamase inhibitor combinations (IRR 3.92; 95% CI 1.68–9.13) or third/fourth generation cephalosporin (IRR 2.75; 95% CI 1.06–7.11) exposure within 3 months before enrolment.
Conclusions
Evidence of previous CRE colonization/infection was a major risk factor for carbapenem resistance among Enterobacterales BSI. Compared with uninfected patients, evidence of previous MDRO colonization/infection and healthcare exposure were important risk factors for CRE BSI. Targeted screening, infection prevention and antimicrobial stewardship should focus on these high-risk patients.</description><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Anti-Bacterial Agents - therapeutic use</subject><subject>Bacteremia - epidemiology</subject><subject>Bacteremia - microbiology</subject><subject>Carbapenem-Resistant Enterobacteriaceae - drug effects</subject><subject>Carbapenem-Resistant Enterobacteriaceae - isolation & purification</subject><subject>Carbapenems - pharmacology</subject><subject>Case-Control Studies</subject><subject>Enterobacteriaceae Infections - epidemiology</subject><subject>Enterobacteriaceae Infections - microbiology</subject><subject>Europe - epidemiology</subject><subject>Female</subject><subject>Humans</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Original Research</subject><subject>Prospective Studies</subject><subject>Risk Factors</subject><issn>0305-7453</issn><issn>1460-2091</issn><issn>1460-2091</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNp9kU1r3DAQhkVpaTZpT7kXnUohuBlZliXnEkrIFwQCoT0LWRqnTmxpK8mB_fdV2U1oLmEOc5iHZ2Z4CTlk8J1Bx48fjD12jwaZkO_IijUtVDV07D1ZAQdRyUbwPbKf0gMAtKJVH8keV51SZbgim7sxPdLB2BxiokOItJ9CcClHNDMd_YA2j8En6hakOVBrYm_W6HGuIqYxZeMzPfcZY-iLBKOZMJ1QQz2mjK7wCSsbfI5heu405cVtPpEPg5kSft71A_Lr4vzn2VV1c3t5ffbjprIcWK4c53aoUbS961g9KNFZ5LKXnDUNw7qF1gKT5THBeCeMlQ0INajaAdSohOEH5HTrXS_9jM5iucFMeh3H2cSNDmbUryd-_K3vw5NmjLeqqWUxfNsZYvizlL_0PCaL02Q8hiVpDlJJVgoKerRFbQwpRRxe9jDQ_9LSJS29S6vQX_4_7YV9jqcAX7dAWNZvmv4CYHKhMw</recordid><startdate>20240903</startdate><enddate>20240903</enddate><creator>Zhou, Hongyu</creator><creator>Buetti, Niccolò</creator><creator>Pérez-Galera, Salvador</creator><creator>Bravo-Ferrer, Jose</creator><creator>Gutiérrez-Gutiérrez, Belén</creator><creator>Paniagua-García, María</creator><creator>Feifel, Jan</creator><creator>Sauser, Julien</creator><creator>Kostyanev, Tomi</creator><creator>Canton, Rafael</creator><creator>Tan, Lionel K</creator><creator>Basoulis, Dimitris</creator><creator>Pintado, Vicente</creator><creator>Roilides, Emmanuel</creator><creator>Dragovac, Gorana</creator><creator>Torre-Cisneros, Julian</creator><creator>Mediç, Deana</creator><creator>Akova, Murat</creator><creator>Goossens, Herman</creator><creator>Bonten, Marc</creator><creator>Harbarth, Stephan</creator><creator>Rodriguez-Baño, Jesus</creator><creator>De Kraker, Marlieke E A</creator><general>Oxford University Press</general><scope>TOX</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9668-0770</orcidid><orcidid>https://orcid.org/0000-0001-6732-9001</orcidid><orcidid>https://orcid.org/0000-0002-6904-9473</orcidid><orcidid>https://orcid.org/0000-0002-8096-1834</orcidid><orcidid>https://orcid.org/0000-0003-0903-8614</orcidid><orcidid>https://orcid.org/0000-0003-1675-3173</orcidid></search><sort><creationdate>20240903</creationdate><title>Risk factors for bloodstream infections due to carbapenem-resistant Enterobacterales: a nested case-control-control study</title><author>Zhou, Hongyu ; Buetti, Niccolò ; Pérez-Galera, Salvador ; Bravo-Ferrer, Jose ; Gutiérrez-Gutiérrez, Belén ; Paniagua-García, María ; Feifel, Jan ; Sauser, Julien ; Kostyanev, Tomi ; Canton, Rafael ; Tan, Lionel K ; Basoulis, Dimitris ; Pintado, Vicente ; Roilides, Emmanuel ; Dragovac, Gorana ; Torre-Cisneros, Julian ; Mediç, Deana ; Akova, Murat ; Goossens, Herman ; Bonten, Marc ; Harbarth, Stephan ; Rodriguez-Baño, Jesus ; De Kraker, Marlieke E A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c301t-d33cf2e56bd912f859ce37b731441e2606c01706551395ac74058f82d002e85a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Anti-Bacterial Agents - therapeutic use</topic><topic>Bacteremia - epidemiology</topic><topic>Bacteremia - microbiology</topic><topic>Carbapenem-Resistant Enterobacteriaceae - drug effects</topic><topic>Carbapenem-Resistant Enterobacteriaceae - isolation & purification</topic><topic>Carbapenems - pharmacology</topic><topic>Case-Control Studies</topic><topic>Enterobacteriaceae Infections - epidemiology</topic><topic>Enterobacteriaceae Infections - microbiology</topic><topic>Europe - epidemiology</topic><topic>Female</topic><topic>Humans</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Original Research</topic><topic>Prospective Studies</topic><topic>Risk Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhou, Hongyu</creatorcontrib><creatorcontrib>Buetti, Niccolò</creatorcontrib><creatorcontrib>Pérez-Galera, Salvador</creatorcontrib><creatorcontrib>Bravo-Ferrer, Jose</creatorcontrib><creatorcontrib>Gutiérrez-Gutiérrez, Belén</creatorcontrib><creatorcontrib>Paniagua-García, María</creatorcontrib><creatorcontrib>Feifel, Jan</creatorcontrib><creatorcontrib>Sauser, Julien</creatorcontrib><creatorcontrib>Kostyanev, Tomi</creatorcontrib><creatorcontrib>Canton, Rafael</creatorcontrib><creatorcontrib>Tan, Lionel K</creatorcontrib><creatorcontrib>Basoulis, Dimitris</creatorcontrib><creatorcontrib>Pintado, Vicente</creatorcontrib><creatorcontrib>Roilides, Emmanuel</creatorcontrib><creatorcontrib>Dragovac, Gorana</creatorcontrib><creatorcontrib>Torre-Cisneros, Julian</creatorcontrib><creatorcontrib>Mediç, Deana</creatorcontrib><creatorcontrib>Akova, Murat</creatorcontrib><creatorcontrib>Goossens, Herman</creatorcontrib><creatorcontrib>Bonten, Marc</creatorcontrib><creatorcontrib>Harbarth, Stephan</creatorcontrib><creatorcontrib>Rodriguez-Baño, Jesus</creatorcontrib><creatorcontrib>De Kraker, Marlieke E A</creatorcontrib><creatorcontrib>COMBACTE- EURECA project team</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of antimicrobial chemotherapy</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhou, Hongyu</au><au>Buetti, Niccolò</au><au>Pérez-Galera, Salvador</au><au>Bravo-Ferrer, Jose</au><au>Gutiérrez-Gutiérrez, Belén</au><au>Paniagua-García, María</au><au>Feifel, Jan</au><au>Sauser, Julien</au><au>Kostyanev, Tomi</au><au>Canton, Rafael</au><au>Tan, Lionel K</au><au>Basoulis, Dimitris</au><au>Pintado, Vicente</au><au>Roilides, Emmanuel</au><au>Dragovac, Gorana</au><au>Torre-Cisneros, Julian</au><au>Mediç, Deana</au><au>Akova, Murat</au><au>Goossens, Herman</au><au>Bonten, Marc</au><au>Harbarth, Stephan</au><au>Rodriguez-Baño, Jesus</au><au>De Kraker, Marlieke E A</au><aucorp>COMBACTE- EURECA project team</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Risk factors for bloodstream infections due to carbapenem-resistant Enterobacterales: a nested case-control-control study</atitle><jtitle>Journal of antimicrobial chemotherapy</jtitle><addtitle>J Antimicrob Chemother</addtitle><date>2024-09-03</date><risdate>2024</risdate><volume>79</volume><issue>9</issue><spage>2132</spage><epage>2141</epage><pages>2132-2141</pages><issn>0305-7453</issn><issn>1460-2091</issn><eissn>1460-2091</eissn><abstract>Abstract
Background
Carbapenem-resistant Enterobacterales (CRE) bloodstream infections (BSIs) are a major threat to patients. To date, data on risk factors have been limited, with low internal and external validity. In this multicentre study, risk factors for CRE BSI were determined by comparison with two control groups: patients with carbapenem-susceptible Enterobacterales (CSE) BSI, and patients without Enterobacterales infection (uninfected patients).
Methods
A multicentre, case-control-control study was nested in a European prospective cohort study on CRE (EURECA). CRE BSI:CSE BSI matching was 1:1, CRE BSI:Uninfected patients matching was 1:3, based on hospital, ward and length of stay. Conditional logistic regression was applied.
Results
From March 2016 to November 2018, 73 CRE BSIs, 73 CSE BSIs and 219 uninfected patients were included from 18 European hospitals. For CRE versus CSE BSI, previous CRE colonization/infection [incidence rate ratio (IRR) 7.32; 95% CI 1.65–32.38) increased the risk. For CRE versus uninfected controls, independent risk factors included: older age (IRR 1.03; 95% CI 1.01–1.06), patient referral (long-term care facility: IRR 7.19; 95% CI 1.51–34.24; acute care hospital: IRR 5.26; 95% CI 1.61–17.11), previous colonization/infection with other MDR organisms (MDROs) (IRR 9.71; 95% CI 2.33–40.56), haemodialysis (IRR 8.59; 95% CI 1.82–40.53), invasive procedures (IRR 5.66; 95% CI 2.11–15.16), and β-lactam/β-lactamase inhibitor combinations (IRR 3.92; 95% CI 1.68–9.13) or third/fourth generation cephalosporin (IRR 2.75; 95% CI 1.06–7.11) exposure within 3 months before enrolment.
Conclusions
Evidence of previous CRE colonization/infection was a major risk factor for carbapenem resistance among Enterobacterales BSI. Compared with uninfected patients, evidence of previous MDRO colonization/infection and healthcare exposure were important risk factors for CRE BSI. Targeted screening, infection prevention and antimicrobial stewardship should focus on these high-risk patients.</abstract><cop>UK</cop><pub>Oxford University Press</pub><pmid>38988305</pmid><doi>10.1093/jac/dkae157</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-9668-0770</orcidid><orcidid>https://orcid.org/0000-0001-6732-9001</orcidid><orcidid>https://orcid.org/0000-0002-6904-9473</orcidid><orcidid>https://orcid.org/0000-0002-8096-1834</orcidid><orcidid>https://orcid.org/0000-0003-0903-8614</orcidid><orcidid>https://orcid.org/0000-0003-1675-3173</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aged Aged, 80 and over Anti-Bacterial Agents - pharmacology Anti-Bacterial Agents - therapeutic use Bacteremia - epidemiology Bacteremia - microbiology Carbapenem-Resistant Enterobacteriaceae - drug effects Carbapenem-Resistant Enterobacteriaceae - isolation & purification Carbapenems - pharmacology Case-Control Studies Enterobacteriaceae Infections - epidemiology Enterobacteriaceae Infections - microbiology Europe - epidemiology Female Humans Male Middle Aged Original Research Prospective Studies Risk Factors |
title | Risk factors for bloodstream infections due to carbapenem-resistant Enterobacterales: a nested case-control-control study |
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