{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T07:46:15Z","timestamp":1791359175611,"version":"4.3.1"},"reference-count":36,"publisher":"American Medical Association (AMA)","issue":"10","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JAMA Netw Open"],"abstract":"Importance<\/jats:title>Colony-stimulating factors are prescribed to patients undergoing chemotherapy to reduce the risk of febrile neutropenia. Research suggests that 55% to 95% of colony-stimulating factor prescribing is inconsistent with national guidelines.<\/jats:p><\/jats:sec>Objective<\/jats:title>To examine whether a guideline-based standing order for primary prophylactic colony-stimulating factors improves use and reduces the incidence of febrile neutropenia.<\/jats:p><\/jats:sec>Design, Setting, and Participants<\/jats:title>This cluster randomized clinical trial, the Trial Assessing CSF Prescribing Effectiveness and Risk (TrACER), involved 32 community oncology clinics in the US. Participants were adult patients with breast, colorectal, or non\u2013small cell lung cancer initiating cancer therapy and enrolled between January 2016 and April 2020. Data analysis was performed from July to October 2021.<\/jats:p><\/jats:sec>Interventions<\/jats:title>Sites were randomized 3:1 to implementation of a guideline-based primary prophylactic colony-stimulating factor standing order system or usual care. Automated orders were added for high-risk regimens, and an alert not to prescribe was included for low-risk regimens. Risk was based on National Comprehensive Cancer Network guidelines.<\/jats:p><\/jats:sec>Main Outcomes and Measures<\/jats:title>The primary outcome was to find an increase in colony-stimulating factor use among high-risk patients from 40% to 75%, a reduction in use among low-risk patients from 17% to 7%, and a 50% reduction in febrile neutropenia rates in the intervention group. Mixed model logistic regression adjusted for correlation of outcomes within a clinic.<\/jats:p><\/jats:sec>Results<\/jats:title>A total of 2946 patients (median [IQR] age, 59.0 [50.0-67.0] years; 2233 women [77.0%]; 2292 White [79.1%]) were enrolled; 2287 were randomized to the intervention, and 659 were randomized to usual care. Colony-stimulating factor use for patients receiving high-risk regimens was high and not significantly different between groups (847 of 950 patients [89.2%] in the intervention group vs 296 of 309 patients [95.8%] in the usual care group). Among high-risk patients, febrile neutropenia rates for the intervention (58 of 947 patients [6.1%]) and usual care (13 of 308 patients [4.2%]) groups were not significantly different. The febrile neutropenia rate for patients receiving high-risk regimens not receiving colony-stimulating factors was 14.9% (17 of 114 patients). Among the 585 patients receiving low-risk regimens, colony-stimulating factor use was low and did not differ between groups (29 of 457 patients [6.3%] in the intervention group vs 7 of 128 patients [5.5%] in the usual care group). Febrile neutropenia rates did not differ between usual care (1 of 127 patients [0.8%]) and the intervention (7 of 452 patients [1.5%]) groups.<\/jats:p><\/jats:sec>Conclusions and Relevance<\/jats:title>In this cluster randomized clinical trial, implementation of a guideline-informed standing order did not affect colony-stimulating factor use or febrile neutropenia rates in high-risk and low-risk patients. Overall, use was generally appropriate for the level of risk. Standing order interventions do not appear to be necessary or effective in the setting of prophylactic colony-stimulating factor prescribing.<\/jats:p><\/jats:sec>Trial Registration<\/jats:title>ClinicalTrials.gov Identifier: NCT02728596<\/jats:ext-link><\/jats:p><\/jats:sec>","DOI":"10.1001\/jamanetworkopen.2022.38191","type":"journal-article","created":{"date-parts":[[2022,10,24]],"date-time":"2022-10-24T15:31:59Z","timestamp":1666625519000},"page":"e2238191","source":"Crossref","is-referenced-by-count":7,"title":["Effects of a Guideline-Informed Clinical Decision Support System Intervention to Improve Colony-Stimulating Factor Prescribing"],"prefix":"10.1001","volume":"5","author":[{"given":"Scott D.","family":"Ramsey","sequence":"first","affiliation":[{"name":"Hutchinson Institute for Cancer Outcomes Research, Fred Hutchinson Cancer Research Center, Seattle, Washington"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aasthaa","family":"Bansal","sequence":"additional","affiliation":[{"name":"Hutchinson Institute for Cancer Outcomes Research, Fred Hutchinson Cancer Research Center, Seattle, Washington"},{"name":"The Comparative Health Outcomes, Policy, and Economics Institute, School of Pharmacy, University of Washington, Seattle"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sean D.","family":"Sullivan","sequence":"additional","affiliation":[{"name":"Hutchinson Institute for Cancer Outcomes Research, Fred Hutchinson Cancer Research Center, Seattle, Washington"},{"name":"The Comparative Health Outcomes, Policy, and Economics Institute, School of Pharmacy, University of Washington, Seattle"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gary H.","family":"Lyman","sequence":"additional","affiliation":[{"name":"Hutchinson Institute for Cancer Outcomes Research, Fred Hutchinson Cancer Research Center, Seattle, Washington"},{"name":"School of Medicine, University of Washington, Seattle"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William E.","family":"Barlow","sequence":"additional","affiliation":[{"name":"Hutchinson Institute for Cancer Outcomes Research, Fred Hutchinson Cancer Research Center, Seattle, Washington"},{"name":"SWOG Statistics and Data Management Center, Seattle, Washington"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathryn B.","family":"Arnold","sequence":"additional","affiliation":[{"name":"Hutchinson Institute for Cancer Outcomes Research, Fred Hutchinson Cancer Research Center, Seattle, Washington"},{"name":"SWOG Statistics and Data Management Center, Seattle, Washington"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kate","family":"Watabayashi","sequence":"additional","affiliation":[{"name":"Hutchinson Institute for Cancer Outcomes Research, Fred Hutchinson Cancer Research Center, Seattle, Washington"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ari","family":"Bell-Brown","sequence":"additional","affiliation":[{"name":"Hutchinson Institute for Cancer Outcomes Research, Fred Hutchinson Cancer Research Center, Seattle, Washington"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karma","family":"Kreizenbeck","sequence":"additional","affiliation":[{"name":"Hutchinson Institute for Cancer Outcomes Research, Fred Hutchinson Cancer Research Center, Seattle, Washington"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nguyet A.","family":"Le-Lindqwister","sequence":"additional","affiliation":[{"name":"Illinois CancerCare\u2013Peoria (Heartland Cancer Research National Cancer Institute Community Oncology Research Program), Peoria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carrie L.","family":"Dul","sequence":"additional","affiliation":[{"name":"Ascension St John Hospital (Michigan Cancer Research Consortium National Cancer Institute Community Oncology Research Program), Detroit"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ursa A.","family":"Brown-Glaberman","sequence":"additional","affiliation":[{"name":"University of New Mexico Cancer Center (New Mexico Minority Underserved National Cancer Institute Community Oncology Research Program, Albuquerque"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert J.","family":"Behrens","sequence":"additional","affiliation":[{"name":"Medical Oncology and Hematology Associates\u2013Des Moines (Iowa-Wide Oncology Research Coalition National Cancer Institute Community Oncology Research Program), Des Moines"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victor","family":"Vogel","sequence":"additional","affiliation":[{"name":"Geisinger Medical Center (Geisinger Cancer Institute National Cancer Institute Community Oncology Research Program), Danville, Pennsylvania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nitya","family":"Alluri","sequence":"additional","affiliation":[{"name":"St Luke\u2019s Cancer Institute\u2013Boise (Pacific Cancer Research Consortium National Cancer Institute Community Oncology Research Program), Boise, Idaho"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dawn L.","family":"Hershman","sequence":"additional","affiliation":[{"name":"Department of Medicine and Epidemiology, Columbia University, New York, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"10","published-online":{"date-parts":[[2022,10,24]]},"reference":[{"issue":"1","key":"zoi221080r1","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.ejca.2010.10.013","article-title":"2010 Update of EORTC guidelines for the use of granulocyte-colony stimulating factor to reduce the incidence of chemotherapy-induced febrile neutropenia in adult patients with lymphoproliferative disorders and solid tumours.","volume":"47","author":"Aapro","year":"2011","journal-title":"Eur J Cancer"},{"issue":"12","key":"zoi221080r2","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1093\/jnci\/djr152","article-title":"Use of colony-stimulating factors with chemotherapy: opportunities for cost savings and improved outcomes.","volume":"103","author":"Potosky","year":"2011","journal-title":"J Natl Cancer Inst"},{"issue":"9","key":"zoi221080r3","first-page":"678","article-title":"Colony-stimulating factor prescribing patterns in patients receiving chemotherapy for cancer.","volume":"16","author":"Ramsey","year":"2010","journal-title":"Am J Manag Care"},{"issue":"2","key":"zoi221080r4","doi-asserted-by":"publisher","first-page":"109","DOI":"10.6004\/jnccn.2008.0012","article-title":"Risk and timing of neutropenic events in adult cancer patients receiving chemotherapy: the results of a prospective nationwide study of oncology practice.","volume":"6","author":"Crawford","year":"2008","journal-title":"J Natl Compr Canc Netw"},{"issue":"19","key":"zoi221080r5","doi-asserted-by":"publisher","first-page":"3187","DOI":"10.1200\/JCO.2006.06.4451","article-title":"2006 Update of recommendations for the use of white blood cell growth factors: an evidence-based clinical practice guideline.","volume":"24","author":"Smith","year":"2006","journal-title":"J Clin Oncol"},{"issue":"14","key":"zoi221080r6","doi-asserted-by":"publisher","first-page":"1715","DOI":"10.1200\/JCO.2012.42.8375","article-title":"American Society of Clinical Oncology identifies five key opportunities to improve care and reduce costs: the top five list for oncology.","volume":"30","author":"Schnipper","year":"2012","journal-title":"J Clin Oncol"},{"issue":"3","key":"zoi221080r10","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1007\/s00520-013-2021-2","article-title":"Neutropenia management and granulocyte colony-stimulating factor use in patients with solid tumours receiving myelotoxic chemotherapy: findings from clinical practice.","volume":"22","author":"Krzemieniecki","year":"2014","journal-title":"Support Care Cancer"},{"issue":"2","key":"zoi221080r11","doi-asserted-by":"publisher","first-page":"360","DOI":"10.1007\/s10120-014-0375-x","article-title":"Chemotherapy treatment patterns and neutropenia management in gastric cancer.","volume":"18","author":"Kalinka-Warzocha","year":"2015","journal-title":"Gastric Cancer"},{"issue":"8","key":"zoi221080r12","doi-asserted-by":"publisher","first-page":"2167","DOI":"10.1007\/s00520-014-2184-5","article-title":"Use of pegfilgrastim primary prophylaxis and risk of infection, by chemotherapy cycle and regimen, among patients with breast cancer or non-Hodgkin\u2019s lymphoma.","volume":"22","author":"Langeberg","year":"2014","journal-title":"Support Care Cancer"},{"issue":"6","key":"zoi221080r13","doi-asserted-by":"publisher","first-page":"1619","DOI":"10.1007\/s00520-014-2121-7","article-title":"Granulocyte colony-stimulating factor (G-CSF) patterns of use in cancer patients receiving myelosuppressive chemotherapy.","volume":"22","author":"Choi","year":"2014","journal-title":"Support Care Cancer"},{"issue":"11","key":"zoi221080r14","doi-asserted-by":"publisher","DOI":"10.1001\/jamanetworkopen.2021.33474","article-title":"Trends in use of granulocyte colony-stimulating factor following introduction of biosimilars among adults with cancer and commercial or Medicare insurance from 2014 to 2019.","volume":"4","author":"Wang","year":"2021","journal-title":"JAMA Netw Open"},{"issue":"5","key":"zoi221080r15","doi-asserted-by":"publisher","first-page":"454","DOI":"10.1056\/NEJMra1510059","article-title":"Pragmatic trials.","volume":"375","author":"Ford","year":"2016","journal-title":"N Engl J Med"},{"issue":"5","key":"zoi221080r16","doi-asserted-by":"publisher","first-page":"461","DOI":"10.2217\/cer-2017-0005","article-title":"A stakeholder-informed randomized, controlled comparative effectiveness study of an order prescribing intervention to improve colony stimulating factor use for cancer patients receiving myelosuppressive chemotherapy: the TrACER study.","volume":"6","author":"Bansal","year":"2017","journal-title":"J Comp Eff Res"},{"issue":"1","key":"zoi221080r17","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1186\/s12874-019-0764-2","article-title":"Effective stakeholder engagement: design and implementation of a clinical trial (SWOG S1415CD) to improve cancer care.","volume":"19","author":"Barger","year":"2019","journal-title":"BMC Med Res Methodol"},{"issue":"21","key":"zoi221080r19","doi-asserted-by":"publisher","first-page":"3158","DOI":"10.1200\/JCO.2006.08.8823","article-title":"Impact of primary prophylaxis with granulocyte colony-stimulating factor on febrile neutropenia and mortality in adult cancer patients receiving chemotherapy: a systematic review.","volume":"25","author":"Kuderer","year":"2007","journal-title":"J Clin Oncol"},{"issue":"7","key":"zoi221080r20","doi-asserted-by":"publisher","first-page":"1576","DOI":"10.1177\/1078155218799859","article-title":"Appropriateness of granulocyte colony-stimulating factor use in patients receiving chemotherapy by febrile neutropenia risk level.","volume":"25","author":"Baig","year":"2019","journal-title":"J Oncol Pharm Pract"},{"issue":"6","key":"zoi221080r21","doi-asserted-by":"publisher","first-page":"1477","DOI":"10.1002\/cam4.2014.3.issue-6","article-title":"G-CSF utilization rate and prescribing patterns in United States: associations between physician and patient factors and GCSF use.","volume":"3","author":"Barnes","year":"2014","journal-title":"Cancer Med"},{"issue":"1","key":"zoi221080r25","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1188\/17.CJON.121-122","article-title":"On-body injector: an administration device for pegfilgrastim.","volume":"21","author":"Mahler","year":"2017","journal-title":"Clin J Oncol Nurs"},{"issue":"1","key":"zoi221080r26","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1007\/s00520-017-3841-2","article-title":"Administration options for pegfilgrastim prophylaxis: patient and physician preferences from a cross-sectional survey.","volume":"26","author":"Brett Hauber","year":"2018","journal-title":"Support Care Cancer"},{"issue":"8","key":"zoi221080r27","doi-asserted-by":"publisher","first-page":"524","DOI":"10.1016\/j.cmi.2017.02.028","article-title":"A systematic review of clinical decision support systems for antimicrobial management: are we failing to investigate these interventions appropriately?","volume":"23","author":"Rawson","year":"2017","journal-title":"Clin Microbiol Infect"},{"key":"zoi221080r28","doi-asserted-by":"publisher","first-page":"788","DOI":"10.1007\/s11606-020-06096-3","article-title":"Impact of clinical decision support on antibiotic prescribing for acute respiratory infections: a cluster randomized implementation trial.","volume":"35","author":"Mann","year":"2020","journal-title":"J Gen Intern Med"},{"issue":"5","key":"zoi221080r29","doi-asserted-by":"publisher","first-page":"1015","DOI":"10.2214\/AJR.19.21511","article-title":"Randomized clinical trial of a clinical decision support tool for improving the appropriateness scores for ordering imaging studies in primary and specialty care ambulatory clinics.","volume":"213","author":"Palen","year":"2019","journal-title":"AJR Am J Roentgenol"},{"issue":"1","key":"zoi221080r30","doi-asserted-by":"publisher","first-page":"5","DOI":"10.1186\/s13012-019-0955-6","article-title":"Computerized clinical decision support system for diabetes in primary care does not improve quality of care: a cluster-randomized controlled trial.","volume":"15","author":"Heselmans","year":"2020","journal-title":"Implement Sci"},{"issue":"4","key":"zoi221080r31","doi-asserted-by":"publisher","first-page":"331","DOI":"10.6004\/jnccn.2018.7104","article-title":"A systematic review of clinical decision support systems for clinical oncology practice.","volume":"17","author":"Pawloski","year":"2019","journal-title":"J Natl Compr Canc Netw"},{"key":"zoi221080r32","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.ijmedinf.2016.12.001","article-title":"Factors influencing implementation success of guideline-based clinical decision support systems: a systematic review and gaps analysis.","volume":"98","author":"Kilsdonk","year":"2017","journal-title":"Int J Med Inform"},{"issue":"5","key":"zoi221080r33","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1055\/s-0038-1634216","article-title":"Development and implementation of computerized clinical guidelines: barriers and solutions.","volume":"41","author":"Trivedi","year":"2002","journal-title":"Methods Inf Med"},{"issue":"1","key":"zoi221080r34","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1016\/j.ijmedinf.2006.01.008","article-title":"Context, automated decision support, and clinical practice guidelines: does the literature apply to the United States practice environment?","volume":"76","author":"Edmonson","year":"2007","journal-title":"Int J Med Inform"},{"issue":"1","key":"zoi221080r35","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1186\/s13012-017-0644-2","article-title":"What hinders the uptake of computerized decision support systems in hospitals? a qualitative study and framework for implementation.","volume":"12","author":"Liberati","year":"2017","journal-title":"Implement Sci"},{"issue":"16","key":"zoi221080r36","doi-asserted-by":"publisher","first-page":"1763","DOI":"10.1200\/JCO.21.02342","article-title":"Impact of the oncology care model on use of supportive care medications during cancer treatment.","volume":"40","author":"Brooks","year":"2022","journal-title":"J Clin Oncol"},{"key":"zoi221080r7","unstructured":"National Comprehensive Cancer Network. Clinical practice guidelines in oncology: breast cancer, v.1.2010. 2011. Accessed March 25, 2022. https:\/\/www.nccn.org\/guidelines\/guidelines-detail?category=1&id=1419"},{"key":"zoi221080r8","unstructured":"National Comprehensive Cancer Network. Clinical practice guidelines in oncology: myeloid growth factors, v.1.2010. 2011. Accessed March 25, 2022. https:\/\/www.nccn.org\/professionals\/physician_gls\/f_guidelines.asp"},{"key":"zoi221080r9","unstructured":"National Comprehensive Cancer Network. Clinical practice guidelines in oncology: non-small cell lung cancer, v.2.2009. 2011. Accessed March 25, 2022. https:\/\/www.nccn.org\/guidelines\/guidelines-detail?category=1&id=1450"},{"key":"zoi221080r18","unstructured":"National Cancer Institute. Common Terminology Criteria for Adverse Events (CTCAE) version 4.0. 2021. Accessed October 26, 2021. https:\/\/ctep.cancer.gov\/protocoldevelopment\/electronic_applications\/ctc.htm#ctc_40"},{"key":"zoi221080r22","unstructured":"American Society of Clinical Oncology. 10 Things physicians and patients should question. 2014. Accessed August 6, 2014. https:\/\/www.choosingwisely.org\/doctor-patient-lists\/american-society-of-clinical-oncology\/"},{"key":"zoi221080r23","unstructured":"ABIM Foundation. Choosing Wisely: a special report on the first five years. 2017. Accessed September 20, 2022. https:\/\/www.choosingwisely.org\/wp-content\/uploads\/2017\/10\/Choosing-Wisely-at-Five.pdf"},{"key":"zoi221080r24","unstructured":"Amgen Inc. Neulasta OnPro Kit website. Published 2021. Updated 2021. Accessed January 31, 2022. https:\/\/www.neulasta.com\/stay-at-home-with-neulasta-onpro"}],"container-title":["JAMA Network Open"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/jamanetwork.com\/journals\/jamanetworkopen\/articlepdf\/2797592\/ramsey_2022_oi_221080_1665755000.68208.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,10,24]],"date-time":"2022-10-24T15:32:05Z","timestamp":1666625525000},"score":1,"resource":{"primary":{"URL":"https:\/\/jamanetwork.com\/journals\/jamanetworkopen\/fullarticle\/2797592"}},"subtitle":["A Cluster Randomized Clinical Trial"],"short-title":[],"issued":{"date-parts":[[2022,10,24]]},"references-count":36,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2022,10,3]]}},"URL":"https:\/\/doi.org\/10.1001\/jamanetworkopen.2022.38191","relation":{},"ISSN":["2574-3805"],"issn-type":[{"value":"2574-3805","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,24]]}}}