{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,9]],"date-time":"2026-07-09T06:57:32Z","timestamp":1783580252390,"version":"3.55.0"},"reference-count":34,"publisher":"Oxford University Press (OUP)","issue":"11","license":[{"start":{"date-parts":[[2020,7,15]],"date-time":"2020-07-15T00:00:00Z","timestamp":1594771200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["5R21AI128216-02)"],"award-info":[{"award-number":["5R21AI128216-02)"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,12,6]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Antibiotic stewardship programs (ASPs) have demonstrated success at reducing costs, yet there is limited quality evidence of their effectiveness in reducing infections of high-profile drug-resistant organisms.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>This retrospective, cohort study included all Kaiser Permanente Southern California (KPSC) members aged \u226518 years hospitalized in 9 KPSC hospitals from 1 January 2008 to 31 December 2016. We measured the impact of staggered ASP implementation on consumption of 18 ASP-targeted antibiotics using generalized linear mixed-effects models. We used multivariable generalized linear mixed-effects models to estimate the adjusted effect of an ASP on rates of infection with drug-resistant organisms. Analyses were adjusted for confounding by time, cluster effects, and patient- and hospital-level characteristics.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>We included 765 111 hospitalizations (288 257 pre-ASP, 476 854 post-ASP). By defined daily dose, we found a 6.1% (\u22127.5% to \u22124.7%) overall decrease antibiotic use post-ASP; by days of therapy, we detected a 4.3% (\u22125.4% to \u22123.1%) decrease in overall use of antibiotics. The number of prescriptions increased post-ASP (1.04 [1.03\u20131.05]). In adjusted analyses, we detected an overall increase in vancomycin-resistant enterococci infections post-ASP (1.37 [1.10\u20131.69]). We did not detect a change in the rates of extended-spectrum beta-lactamase, carbapenem-resistant Enterobacteriaceae, and multidrug-resistant Pseudomonas aeruginosa infections post-ASP.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>ASPs with successful reductions in consumption of targeted antibiotics may not see changes in infection rates with antibiotic-resistant organisms in the 2 to 6 years post-implementation. There are likely differing timescales for reversion to susceptibility across organisms and antibiotics, and unintended consequences from compensatory prescribing may occur.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/cid\/ciaa1004","type":"journal-article","created":{"date-parts":[[2020,7,14]],"date-time":"2020-07-14T03:21:27Z","timestamp":1594696887000},"page":"e4454-e4462","source":"Crossref","is-referenced-by-count":15,"title":["Do Inpatient Antimicrobial Stewardship Programs Help Us in the Battle Against Antimicrobial Resistance?"],"prefix":"10.1093","volume":"73","author":[{"given":"Sara Y","family":"Tartof","sequence":"first","affiliation":[{"name":"Kaiser Permanente Southern California Department of Research & Evaluation, Pasadena, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lie Hong","family":"Chen","sequence":"additional","affiliation":[{"name":"Kaiser Permanente Southern California Department of Research & Evaluation, Pasadena, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yun","family":"Tian","sequence":"additional","affiliation":[{"name":"Kaiser Permanente Southern California Department of Research & Evaluation, Pasadena, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rong","family":"Wei","sequence":"additional","affiliation":[{"name":"Kaiser Permanente Southern California Department of Research & Evaluation, Pasadena, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Theresa","family":"Im","sequence":"additional","affiliation":[{"name":"Kaiser Permanente Southern California Department of Research & Evaluation, Pasadena, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kalvin","family":"Yu","sequence":"additional","affiliation":[{"name":"Inpatient Pharmacy Department, Kaiser Permanent Fontana Medical Center, Fontana, California, USA"},{"name":"Department of Infectious Diseases, Southern California Permanente Medical Group, West Hollywood, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gunter","family":"Rieg","sequence":"additional","affiliation":[{"name":"Inpatient Pharmacy Department, Kaiser Permanent Fontana Medical Center, Fontana, California, USA"},{"name":"Department of Infectious Diseases, Southern California Permanente Medical Group, South Bay, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zoe","family":"Bider-Canfield","sequence":"additional","affiliation":[{"name":"Kaiser Permanente Southern California Department of Research & Evaluation, Pasadena, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frances","family":"Wong","sequence":"additional","affiliation":[{"name":"Inpatient Pharmacy Department, Kaiser Permanent Fontana Medical Center, Fontana, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Harpreet S","family":"Takhar","sequence":"additional","affiliation":[{"name":"Kaiser Permanente Southern California Department of Research & Evaluation, Pasadena, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Qian","sequence":"additional","affiliation":[{"name":"Kaiser Permanente Southern California Department of Research & Evaluation, Pasadena, California, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,7,15]]},"reference":[{"key":"2021121517095957200_CIT0001","author":"Centers for Disease Control and Prevention","year":"2019"},{"key":"2021121517095957200_CIT0002","author":"Infectious Diseases Society of America. Antimicrobial Resistance: A Public Health Crisis"},{"key":"2021121517095957200_CIT0003","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1086\/510393","article-title":"Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship","volume":"44","author":"Dellit","year":"2007","journal-title":"Clin Infect Dis"},{"key":"2021121517095957200_CIT0004","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.4065\/mcp.2011.0358","article-title":"Antimicrobial stewardship","volume":"86","author":"Doron","year":"2011","journal-title":"Mayo Clin Proc"},{"key":"2021121517095957200_CIT0005","first-page":"S397","article-title":"Combating antimicrobial resistance: policy recommendations to save lives","volume":"52 Suppl 5","author":"Spellberg","year":"2011","journal-title":"Clin Infect Dis"},{"key":"2021121517095957200_CIT0006","author":"Centers for Disease Control and Prevention","year":"2014"},{"key":"2021121517095957200_CIT0007","author":"Centers for Disease Control and Prevention","year":"2015"},{"key":"2021121517095957200_CIT0008","author":"Centers for Medicare & Medicaid Services","year":"2019"},{"key":"2021121517095957200_CIT0009","doi-asserted-by":"crossref","first-page":"348","DOI":"10.1086\/380964","article-title":"Long-term antibiotic cost savings from a comprehensive intervention program in a medical department of a university-affiliated teaching hospital","volume":"38","author":"R\u00fcttimann","year":"2004","journal-title":"Clin Infect Dis"},{"key":"2021121517095957200_CIT0010","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1111\/j.1532-5415.2004.52019.x","article-title":"Effect of a comprehensive, multidisciplinary, educational program on the use of antibiotics in a geriatric university hospital","volume":"52","author":"Lutters","year":"2004","journal-title":"J Am Geriatr Soc"},{"key":"2021121517095957200_CIT0011","doi-asserted-by":"crossref","first-page":"1270","DOI":"10.1001\/jama.280.14.1270","article-title":"Antibiotic resistance\u2013squeezing the balloon?","volume":"280","author":"Burke","year":"1998","journal-title":"JAMA"},{"key":"2021121517095957200_CIT0012","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.1097\/01.mlr.0000182534.19832.83","article-title":"Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data","volume":"43","author":"Quan","year":"2005","journal-title":"Med Care"},{"key":"2021121517095957200_CIT0013","doi-asserted-by":"crossref","first-page":"1677","DOI":"10.1093\/cid\/ciy354","article-title":"Benchmarking inpatient antimicrobial use: a comparison of risk-adjusted observed-to-expected ratios","volume":"67","author":"Yu","year":"2018","journal-title":"Clin Infect Dis"},{"key":"2021121517095957200_CIT0014","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1086\/511640","article-title":"Measurement of adult antibacterial drug use in 130 US hospitals: comparison of defined daily dose and days of therapy","volume":"44","author":"Polk","year":"2007","journal-title":"Clin Infect Dis"},{"key":"2021121517095957200_CIT0015","doi-asserted-by":"crossref","first-page":"1309","DOI":"10.1056\/NEJMoa1914433","article-title":"Multidrug-resistant bacterial infections in U.S. hospitalized patients, 2012-2017","volume":"382","author":"Jernigan","year":"2020","journal-title":"N Engl J Med"},{"key":"2021121517095957200_CIT0016","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1086\/666331","article-title":"Association between vancomycin-resistant enterococci bacteremia and ceftriaxone usage","volume":"33","author":"McKinnell","year":"2012","journal-title":"Infect Control Hosp Epidemiol"},{"key":"2021121517095957200_CIT0017","doi-asserted-by":"crossref","first-page":"1925","DOI":"10.1056\/NEJM200012283432604","article-title":"Effect of antibiotic therapy on the density of vancomycin-resistant enterococci in the stool of colonized patients","volume":"343","author":"Donskey","year":"2000","journal-title":"N Engl J Med"},{"key":"2021121517095957200_CIT0018","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1086\/502081","article-title":"Recurrence of vancomycin-resistant Enterococcus stool colonization during antibiotic therapy","volume":"23","author":"Donskey","year":"2002","journal-title":"Infect Control Hosp Epidemiol"},{"key":"2021121517095957200_CIT0019","doi-asserted-by":"crossref","first-page":"3117","DOI":"10.1128\/AAC.00125-06","article-title":"Antibiotic-induced enterococcal expansion in the mouse intestine occurs throughout the small bowel and correlates poorly with suppression of competing flora","volume":"50","author":"Lakticov\u00e1","year":"2006","journal-title":"Antimicrob Agents Chemother"},{"key":"2021121517095957200_CIT0020","doi-asserted-by":"crossref","first-page":"384","DOI":"10.1086\/314874","article-title":"Effect of parenteral antibiotic administration on persistence of vancomycin-resistant Enterococcus faecium in the mouse gastrointestinal tract","volume":"180","author":"Donskey","year":"1999","journal-title":"J Infect Dis"},{"key":"2021121517095957200_CIT0021","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1093\/cid\/ciy1102","article-title":"The association of antibiotic stewardship with fluoroquinolone prescribing in Michigan hospitals: a multi-hospital cohort study","volume":"69","author":"Vaughn","year":"2019","journal-title":"Clin Infect Dis"},{"key":"2021121517095957200_CIT0022","doi-asserted-by":"crossref","first-page":"4840","DOI":"10.1128\/AAC.00825-16","article-title":"Systematic review and meta-analysis of clinical and economic outcomes from the implementation of hospital-based antimicrobial stewardship programs","volume":"60","author":"Karanika","year":"2016","journal-title":"Antimicrob Agents Chemother"},{"key":"2021121517095957200_CIT0023","first-page":"CD003543","article-title":"Interventions to improve antibiotic prescribing practices for hospital inpatients","volume":"2","author":"Davey","year":"2017","journal-title":"Cochrane Database Syst Rev"},{"key":"2021121517095957200_CIT0024","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1093\/jac\/dkh163","article-title":"Reduction in broad-spectrum antimicrobial use associated with no improvement in hospital antibiogram","volume":"53","author":"Cook","year":"2004","journal-title":"J Antimicrob Chemother"},{"key":"2021121517095957200_CIT0025","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1093\/jac\/dkq058","article-title":"Improved susceptibility of gram-negative bacteria in an intensive care unit following implementation of a computerized antibiotic decision support system","volume":"65","author":"Yong","year":"2010","journal-title":"J Antimicrob Chemother"},{"key":"2021121517095957200_CIT0026","first-page":"416426","article-title":"Impact of a multimodal antimicrobial stewardship program on Pseudomonas aeruginosa susceptibility and antimicrobial use in the intensive care unit setting","volume":"2011","author":"Slain","year":"2011","journal-title":"Crit Care Res Pract"},{"key":"2021121517095957200_CIT0027","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.1001\/jama.280.14.1233","article-title":"Class restriction of cephalosporin use to control total cephalosporin resistance in nosocomial Klebsiella","volume":"280","author":"Rahal","year":"1998","journal-title":"JAMA"},{"key":"2021121517095957200_CIT0028","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1093\/jac\/dkn218","article-title":"Electronic antibiotic stewardship\u2013reduced consumption of broad-spectrum antibiotics using a computerized antimicrobial approval system in a hospital setting","volume":"62","author":"Buising","year":"2008","journal-title":"J Antimicrob Chemother"},{"key":"2021121517095957200_CIT0029","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1016\/j.ijantimicag.2011.08.011","article-title":"Implementation and outcomes of a hospital-wide computerised antimicrobial stewardship programme in a large medical centre in Taiwan","volume":"38","author":"Chan","year":"2011","journal-title":"Int J Antimicrob Agents"},{"key":"2021121517095957200_CIT0030","doi-asserted-by":"crossref","first-page":"884","DOI":"10.7326\/0003-4819-124-10-199605150-00004","article-title":"Implementing antibiotic practice guidelines through computer-assisted decision support: clinical and financial outcomes","volume":"124","author":"Pestotnik","year":"1996","journal-title":"Ann Intern Med"},{"key":"2021121517095957200_CIT0031","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.ajic.2013.09.025","article-title":"Effectiveness of infection prevention measures featuring advanced source control and environmental cleaning to limit transmission of extremely-drug resistant Acinetobacter baumannii in a Thai intensive care unit: an analysis before and after extensive flooding","volume":"42","author":"Apisarnthanarak","year":"2014","journal-title":"Am J Infect Control"},{"key":"2021121517095957200_CIT0032","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1007\/s15010-008-7377-8","article-title":"Results of a local antibiotic management program on antibiotic use in a tertiary intensive care unit in Hungary","volume":"36","author":"Peto","year":"2008","journal-title":"Infection"},{"key":"2021121517095957200_CIT0033","volume-title":"Core elements of hospital antibiotic stewardship programs","author":"Centers for Disease Control and Prevention"},{"key":"2021121517095957200_CIT0034","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1128\/CMR.00047-06","article-title":"Setting and revising antibacterial susceptibility breakpoints","volume":"20","author":"Turnidge","year":"2007","journal-title":"Clin Microbiol Rev"}],"container-title":["Clinical Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/cid\/advance-article-pdf\/doi\/10.1093\/cid\/ciaa1004\/33499955\/ciaa1004.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cid\/article-pdf\/73\/11\/e4454\/41607761\/ciaa1004.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/cid\/article-pdf\/73\/11\/e4454\/41607761\/ciaa1004.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,12,15]],"date-time":"2021-12-15T17:10:32Z","timestamp":1639588232000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/cid\/article\/73\/11\/e4454\/5871999"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,15]]},"references-count":34,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,7,15]]},"published-print":{"date-parts":[[2021,12,6]]}},"URL":"https:\/\/doi.org\/10.1093\/cid\/ciaa1004","relation":{},"ISSN":["1058-4838","1537-6591"],"issn-type":[{"value":"1058-4838","type":"print"},{"value":"1537-6591","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2021,12,1]]},"published":{"date-parts":[[2020,7,15]]}}}