{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,5]],"date-time":"2026-09-05T03:52:51Z","timestamp":1788580371199,"version":"build-2803163510"},"reference-count":34,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2022,1,25]],"date-time":"2022-01-25T00:00:00Z","timestamp":1643068800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100014588","name":"Sanofi Pasteur","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100014588","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100017412","name":"Becton, Dickinson and Company","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100017412","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,3,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Viral infections are often treated with empiric antibiotics due to suspected bacterial coinfections, leading to antibiotic overuse. We aimed to describe antibiotic resistance (ABR) trends and their association with the influenza season in ambulatory and inpatient settings in the United States.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Methods<\/jats:title>\n                  <jats:p>We used the BD Insights Research Database to evaluate antibiotic susceptibility profiles in 30-day nonduplicate bacterial isolates collected from patients &amp;gt;17 years old at 257 US healthcare institutions from 2011 to 2019. We investigated ABR in Gram-positive (Staphylococcus aureus and Streptococcus pneumoniae) and Gram-negative (Enterobacterales [ENT], Pseudomonas aeruginosa [PSA], and Acinetobacter baumannii spp [ACB]) bacteria expressed as the proportion of isolates not susceptible ([NS], intermediate or resistant) and resistance per 100 admissions (inpatients only). Antibiotics included carbapenems (Carb), fluoroquinolones (FQ), macrolides, penicillin, extended-spectrum cephalosporins (ESC), and methicillin. Generalized estimating equations models were used to evaluate monthly trends in ABR outcomes and associations with community influenza rates.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>We identified 8\u00a0250\u00a0860 nonduplicate pathogens, including 154\u00a0841 Gram-negative Carb-NS, 1\u00a0502\u00a0796 Gram-negative FQ-NS, 498\u00a0012 methicillin-resistant S aureus (MRSA), and 44\u00a0131 NS S pneumoniae. All S pneumoniae rates per 100 admissions (macrolide-, penicillin-, and ESC-NS) were associated with influenza rates. Respiratory, but not nonrespiratory, MRSA was also associated with influenza. For Gram-negative pathogens, influenza rates were associated with the percentage of FQ-NS ENT, FQ-NS PSA, and Carb-NS ACB.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusions<\/jats:title>\n                  <jats:p>Our study showed expected increases in rates of ABR Gram-positive and identified small but surprising increases in ABR Gram-negative pathogens associated with influenza activity. These insights may help inform antimicrobial stewardship initiatives.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/ofid\/ofac039","type":"journal-article","created":{"date-parts":[[2022,1,26]],"date-time":"2022-01-26T03:20:23Z","timestamp":1643167223000},"source":"Crossref","is-referenced-by-count":12,"title":["Antibiotic Resistance Patterns and Association With the Influenza Season in the United States: A Multicenter Evaluation Reveals Surprising Associations Between Influenza Season and Resistance in Gram-Negative Pathogens"],"prefix":"10.1093","volume":"9","author":[{"given":"Vikas","family":"Gupta","sequence":"first","affiliation":[{"name":"Becton, Dickinson and Company, Franklin Lakes, New Jersey 07417, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kalvin C","family":"Yu","sequence":"additional","affiliation":[{"name":"Becton, Dickinson and Company, Franklin Lakes, New Jersey 07417, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heidi","family":"Kabler","sequence":"additional","affiliation":[{"name":"Sanofi Pasteur, Swiftwater, Pennsylvania, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janet A","family":"Watts","sequence":"additional","affiliation":[{"name":"Becton, Dickinson and Company, Franklin Lakes, New Jersey 07417, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Amine","family":"Amiche","sequence":"additional","affiliation":[{"name":"Sanofi Pasteur, Dubai, United Arab Emirates"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,1,25]]},"reference":[{"key":"2022022812191115700_CIT0001","doi-asserted-by":"crossref","first-page":"166","DOI":"10.2353\/ajpath.2010.100115","article-title":"2009 pandemic influenza (H1N1): pathology and pathogenesis of 100 fatal cases in the United States.","volume":"177","author":"Shieh","year":"2010","journal-title":"Am J Pathol"},{"key":"2022022812191115700_CIT0002","doi-asserted-by":"crossref","first-page":"e321","DOI":"10.1016\/j.ijid.2012.01.003","article-title":"Epidemiology, microbiology, and treatment considerations for bacterial pneumonia complicating influenza.","volume":"16","author":"Metersky","year":"2012","journal-title":"Int J Infect Dis"},{"key":"2022022812191115700_CIT0003","doi-asserted-by":"crossref","first-page":"2047","DOI":"10.4049\/jimmunol.1301152","article-title":"Immune","volume":"191","author":"Metzger","year":"2013","journal-title":"J Immunol"},{"key":"2022022812191115700_CIT0004","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.3389\/fmicb.2017.01041","article-title":"Secondary bacterial infections associated with influenza pandemics.","volume":"8","author":"Morris","year":"2017","journal-title":"Front Microbiol"},{"key":"2022022812191115700_CIT0005","doi-asserted-by":"crossref","first-page":"1328","DOI":"10.1038\/s41564-019-0447-0","article-title":"Direct interactions with influenza promote bacterial adherence during respiratory infections.","volume":"4","author":"Rowe","year":"2019","journal-title":"Nat Microbiol"},{"key":"2022022812191115700_CIT0006","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1111\/irv.12398","article-title":"The frequency of influenza and bacterial coinfection: a systematic review and meta-analysis.","volume":"10","author":"Klein","year":"2016","journal-title":"Influenza Other Respir Viruses"},{"key":"2022022812191115700_CIT0007","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.diagmicrobio.2018.11.014","article-title":"Impact of bacterial and viral coinfection in community-acquired pneumonia in adults.","volume":"94","author":"Lim","year":"2019","journal-title":"Diagn Microbiol Infect Dis"},{"key":"2022022812191115700_CIT0008","doi-asserted-by":"crossref","first-page":"e180243","DOI":"10.1001\/jamanetworkopen.2018.0243","article-title":"Outpatient antibiotic prescribing for acute respiratory infections during influenza seasons.","volume":"1","author":"Havers","year":"2018","journal-title":"JAMA Netw Open"},{"key":"2022022812191115700_CIT0009","doi-asserted-by":"crossref","first-page":"e0221133","DOI":"10.1371\/journal.pone.0221133","article-title":"Seasonality of antimicrobial resistance rates in respiratory bacteria: a systematic review and meta-analysis.","volume":"14","author":"Martinez","year":"2019","journal-title":"PLoS One"},{"key":"2022022812191115700_CIT0010","doi-asserted-by":"crossref","first-page":"742","DOI":"10.1186\/s12879-019-4387-3","article-title":"Trends in resistant Enterobacteriaceae and Acinetobacter species in hospitalized patients in the United States: 2013\u20132017.","volume":"19","author":"Gupta","year":"2019","journal-title":"BMC Infect Dis"},{"key":"2022022812191115700_CIT0011","author":"Centers for Disease Control and Prevention."},{"key":"2022022812191115700_CIT0012","doi-asserted-by":"crossref","first-page":"ofab063","DOI":"10.1093\/ofid\/ofab063","article-title":"A multicenter evaluation of the US prevalence and regional variation in macrolide-resistant S. pneumoniae in ambulatory and hospitalized adult patients in the US.","volume":"8","author":"Gupta","year":"2021","journal-title":"Open Forum Infect Dis"},{"key":"2022022812191115700_CIT0013","doi-asserted-by":"crossref","first-page":"ofy241","DOI":"10.1093\/ofid\/ofy241","article-title":"Carbapenem-nonsusceptible Gram-negative pathogens in ICU and non-ICU settings in US hospitals in 2017: a multicenter study.","volume":"5","author":"McCann","year":"2018","journal-title":"Open Forum Infect Dis"},{"key":"2022022812191115700_CIT0014","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1309\/502AUPR8VE67MBDE","article-title":"A laboratory-based, hospital-wide, electronic marker for nosocomial infection: the future of infection control surveillance?","volume":"125","author":"Brosette","year":"2006","journal-title":"Am J Clin Pathol"},{"key":"2022022812191115700_CIT0015","doi-asserted-by":"crossref","first-page":"e207041","DOI":"10.1001\/jamanetworkopen.2020.7041","article-title":"Comparison of common respiratory virus peak incidence among varying age groups in Rhode Island, 2012-2016.","volume":"3","author":"Choe","year":"2020","journal-title":"JAMA Netw Open"},{"key":"2022022812191115700_CIT0016","author":"Centers for Disease Control and Prevention."},{"key":"2022022812191115700_CIT0017","author":"World Health Organization."},{"key":"2022022812191115700_CIT0018","doi-asserted-by":"crossref","first-page":"100955","DOI":"10.1016\/j.eclinm.2021.100955","article-title":"Outcomes of respiratory viral-bacterial co-infection in adult hospitalized patients.","volume":"37","author":"Liu","year":"2021","journal-title":"EClinicalMedicine"},{"key":"2022022812191115700_CIT0019","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1093\/cid\/cis509","article-title":"Seasonality and temporal correlation between community antibiotic use and resistance in the United States.","volume":"55","author":"Sun","year":"2012","journal-title":"Clin Infect Dis"},{"key":"2022022812191115700_CIT0020","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.ijantimicag.2019.03.010","article-title":"Seasonal variation in antimicrobial resistance rates of community-acquired Escherichia coli bloodstream isolates.","volume":"54","author":"Ramsey","year":"2019","journal-title":"Int J Antimicrob Agents"},{"key":"2022022812191115700_CIT0021","author":"Yu"},{"key":"2022022812191115700_CIT0022","author":"American Society for Microbiology."},{"key":"2022022812191115700_CIT0023","doi-asserted-by":"crossref","first-page":"848","DOI":"10.1017\/ice.2017.83","article-title":"Attributable mortality of healthcare-associated infections due to multidrug-resistant Gram-negative bacteria and methicillin-resistant Staphylococcus.","volume":"38","author":"Nelson","year":"2017","journal-title":"Infect Control Hosp Epidemiol"},{"key":"2022022812191115700_CIT0024","doi-asserted-by":"crossref","first-page":"48.e9","DOI":"10.1016\/j.cmi.2016.09.003","article-title":"Potential economic burden of carbapenem-resistant Enterobacteriaceae (CRE) in the United States.","volume":"23","author":"Bartsch","year":"2017","journal-title":"Clin Microbiol Infect"},{"key":"2022022812191115700_CIT0025","doi-asserted-by":"crossref","first-page":"12896","DOI":"10.1073\/pnas.1721095115","article-title":"Impact of existing vaccines in reducing antibiotic resistance: primary and secondary effects.","volume":"115","author":"Klugman","year":"2018","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2022022812191115700_CIT0026","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1089\/vim.2017.0138","article-title":"The unexpected impact of vaccines on secondary bacterial infections following influenza.","volume":"31","author":"Smith","year":"2018","journal-title":"Viral Immunol"},{"key":"2022022812191115700_CIT0027","doi-asserted-by":"crossref","first-page":"12868","DOI":"10.1073\/pnas.1717157115","article-title":"Antimicrobial resistance and the role of vaccines.","volume":"115","author":"Bloom","year":"2018","journal-title":"Proc Natl Acad Sci"},{"key":"2022022812191115700_CIT0028","doi-asserted-by":"crossref","first-page":"ofaa223","DOI":"10.1093\/ofid\/ofaa223","article-title":"The impact of influenza vaccination on antibiotic use in the United States, 2010\u20132017.","volume":"7","author":"Klein","year":"2020","journal-title":"Open Forum Infect Dis"},{"key":"2022022812191115700_CIT0029","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1186\/s13756-019-0574-7","article-title":"Seasonality of respiratory viruses and bacterial pathogens.","volume":"8","author":"Choe","year":"2019","journal-title":"Antimicrob Resist Infect Control"},{"key":"2022022812191115700_CIT0030","first-page":"20170679","article-title":"An evolutionary model to predict the frequency of antibiotic resistance under seasonal antibiotic use, and an application to Streptococcus pneumoniae.","volume":"284","author":"Blanquart","year":"2017","journal-title":"Proc Biol Sci"},{"key":"2022022812191115700_CIT0031","doi-asserted-by":"crossref","first-page":"ofab232","DOI":"10.1093\/ofid\/ofab232","article-title":"Effect of inadequate empiric antibacterial therapy on hospital outcomes in SARS-CoV-2-positive and -negative US patients with a positive bacterial culture: a multicenter evaluation from March to November 2020.","volume":"8","author":"Puzniak","year":"2021","journal-title":"Open Forum Infect Dis"},{"key":"2022022812191115700_CIT0032","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1186\/s12879-021-05877-3","article-title":"A multicenter analysis of the clinical microbiology and antimicrobial usage in hospitalized patients in the US with or without COVID-19.","volume":"21","author":"Puzniak","year":"2021","journal-title":"BMC Infect Dis"},{"key":"2022022812191115700_CIT0033","doi-asserted-by":"crossref","first-page":"e00902021","DOI":"10.1590\/0037-8682-0090-2021","article-title":"Pre- and post-COVID-19 evaluation of antimicrobial susceptibility for healthcare-associated infections in the intensive care unit of a tertiary hospital.","volume":"54","author":"Gaspar","year":"2021","journal-title":"Rev Soc Bras Med Trop"},{"key":"2022022812191115700_CIT0034","doi-asserted-by":"crossref","first-page":"1657","DOI":"10.1093\/cid\/ciaa773","article-title":"Coronavirus disease 2019 and antimicrobial resistance: parallel and interacting health emergencies.","volume":"72","author":"Nieuwlaat","year":"2021","journal-title":"Clin Infect Dis"}],"container-title":["Open Forum Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/ofid\/advance-article-pdf\/doi\/10.1093\/ofid\/ofac039\/42274240\/ofac039.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ofid\/article-pdf\/9\/3\/ofac039\/42635088\/ofac039.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/ofid\/article-pdf\/9\/3\/ofac039\/42635088\/ofac039.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,2,28]],"date-time":"2022-02-28T12:19:46Z","timestamp":1646050786000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ofid\/article\/doi\/10.1093\/ofid\/ofac039\/6515381"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,25]]},"references-count":34,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2022,3,1]]}},"URL":"https:\/\/doi.org\/10.1093\/ofid\/ofac039","relation":{},"ISSN":["2328-8957"],"issn-type":[{"value":"2328-8957","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022,3,1]]},"published":{"date-parts":[[2022,1,25]]},"article-number":"ofac039"}}