{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,9]],"date-time":"2025-12-09T08:25:10Z","timestamp":1765268710204,"version":"3.41.2"},"reference-count":45,"publisher":"Oxford University Press (OUP)","issue":"3","license":[{"start":{"date-parts":[[2021,7,7]],"date-time":"2021-07-07T00:00:00Z","timestamp":1625616000000},"content-version":"vor","delay-in-days":67,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,5,7]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Background<\/jats:title>\n                  <jats:p>Axillary staging via sentinel lymph node biopsy (SLNB) is performed for clinically node-negative (N0) breast cancer patients. The Sk\u00e5ne University Hospital (SUS) nomogram was developed to assess the possibility of omitting SLNB for patients with a low risk of nodal metastasis. Area under the receiver operating characteristic curve (AUC) was 0.74. The aim was to validate the SUS nomogram using only routinely collected data from the Swedish National Quality Registry for Breast Cancer at two breast cancer centres during different time periods.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Method<\/jats:title>\n                  <jats:p>This retrospective study included patients with primary breast cancer who were treated at centres in Lund and Malm\u00f6 during 2008\u20132013. Clinicopathological predictors in the SUS nomogram were age, mode of detection, tumour size, multifocality, lymphovascular invasion and surrogate molecular subtype. Multiple imputation was used for missing data. Validation performance was assessed using AUC and calibration.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>The study included 2939 patients (1318 patients treated in Lund and 1621 treated in Malm\u00f6). Node-positive disease was detected in 1008 patients. The overall validation AUC was 0.74 (Lund cohort AUC: 0.75, Malm\u00f6 cohort AUC: 0.73), and the calibration was satisfactory. Accepting a false-negative rate of 5 per cent for predicting N0, a possible SLNB reduction rate of 15 per cent was obtained in the overall cohort.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Conclusion<\/jats:title>\n                  <jats:p>The SUS nomogram provided acceptable power for predicting a disease-free axilla in the validation cohort. This tool may assist surgeons in identifying and counselling patients with a low risk of nodal metastasis on the omission of SLNB staging.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/bjsopen\/zrab027","type":"journal-article","created":{"date-parts":[[2021,2,24]],"date-time":"2021-02-24T20:10:18Z","timestamp":1614197418000},"source":"Crossref","is-referenced-by-count":7,"title":["Validation of the Sk\u00e5ne University Hospital nomogram for the preoperative prediction of a disease-free axilla in patients with breast cancer"],"prefix":"10.1093","volume":"5","author":[{"given":"S","family":"Majid","sequence":"first","affiliation":[{"name":"Department of Clinical Sciences Malm\u00f6, Lund University , Malm\u00f6, Sweden"},{"name":"Department of Surgery, Sk\u00e5ne University Hospital , Lund-Malm\u00f6, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"P-O","family":"Bendahl","sequence":"additional","affiliation":[{"name":"Department of Oncology and Pathology, Clinical Sciences, Lund University , Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"L","family":"Huss","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences Malm\u00f6, Lund University , Malm\u00f6, Sweden"},{"name":"Department of Surgery, Helsingborg Hospital , Helsingborg, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J","family":"Manjer","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences Malm\u00f6, Lund University , Malm\u00f6, Sweden"},{"name":"Department of Surgery, Sk\u00e5ne University Hospital , Lund-Malm\u00f6, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"L","family":"Ryd\u00e9n","sequence":"additional","affiliation":[{"name":"Department of Surgery, Sk\u00e5ne University Hospital , Lund-Malm\u00f6, Sweden"},{"name":"Department of Clinical Sciences Lund, Lund University , Lund, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7932-3982","authenticated-orcid":false,"given":"L","family":"Dihge","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences Lund, Lund University , Lund, Sweden"},{"name":"Department of Plastic and Reconstructive Surgery, Sk\u00e5ne University Hospital , Malm\u00f6, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2021,6,22]]},"reference":[{"key":"2022070815273642100_zrab027-B1","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.1002\/bjs.5052","article-title":"Multicentre validation study of sentinel node biopsy for staging in breast cancer","volume":"92","author":"Bergkvist","year":"2005","journal-title":"Br J Surg"},{"key":"2022070815273642100_zrab027-B2","doi-asserted-by":"crossref","first-page":"7703","DOI":"10.1200\/JCO.2005.08.001","article-title":"American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer","volume":"23","author":"Lyman","year":"2005","journal-title":"J Clin Oncol"},{"key":"2022070815273642100_zrab027-B3","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1016\/S1470-2045(07)70278-4","article-title":"Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial","volume":"8","author":"Krag","year":"2007","journal-title":"Lancet Oncol"},{"key":"2022070815273642100_zrab027-B4","doi-asserted-by":"crossref","first-page":"R134","DOI":"10.1186\/bcr3080","article-title":"Long-term prognosis of breast cancer detected by mammography screening or other methods","volume":"13","author":"Lehtimaki","year":"2011","journal-title":"Breast Cancer Res"},{"key":"2022070815273642100_zrab027-B5","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.1001\/jama.2013.277804","article-title":"Axillary node interventions in breast cancer: a systematic review","volume":"310","author":"Rao","year":"2013","journal-title":"JAMA"},{"key":"2022070815273642100_zrab027-B6","doi-asserted-by":"crossref","first-page":"1674","DOI":"10.1093\/annonc\/mdz189","article-title":"Early breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up","volume":"30","author":"Cardoso","year":"2019","journal-title":"Ann Oncol"},{"key":"2022070815273642100_zrab027-B7","doi-asserted-by":"crossref","first-page":"2838","DOI":"10.1200\/JCO.2017.74.0472","article-title":"Use of biomarkers to guide decisions on adjuvant systemic therapy for women with early-stage invasive breast cancer: American Society of Clinical Oncology Clinical Practice Guideline Focused Update","volume":"35","author":"Krop","year":"2017","journal-title":"J Clin Oncol"},{"key":"2022070815273642100_zrab027-B8","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1016\/j.breast.2012.06.013","article-title":"Abandoning sentinel lymph node biopsy in early breast cancer? A new trial in progress at the European Institute of Oncology of Milan (SOUND: Sentinel node vs Observation after axillary UltraSouND)","volume":"21","author":"Gentilini","year":"2012","journal-title":"Breast"},{"key":"2022070815273642100_zrab027-B9","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1055\/s-0042-122853","article-title":"Restricted axillary staging in clinically and sonographically node-negative early invasive breast cancer (c\/iT1-2) in the context of breast conserving therapy: first results following commencement of the Intergroup-Sentinel-Mamma (INSEMA) Trial","volume":"77","author":"Reimer","year":"2017","journal-title":"Geburtshilfe Frauenheilkd"},{"key":"2022070815273642100_zrab027-B10","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1007\/s00268-012-1788-5","article-title":"Clinical assessment of axillary lymph nodes and tumor size in breast cancer compared with histopathological examination: a population-based analysis of 2,537 women","volume":"37","author":"Majid","year":"2013","journal-title":"World J Surg"},{"key":"2022070815273642100_zrab027-B11","doi-asserted-by":"crossref","first-page":"761","DOI":"10.1007\/s10549-015-3280-z","article-title":"Efficacy of physical examination, ultrasound, and ultrasound combined with fine-needle aspiration for axilla staging of primary breast cancer","volume":"149","author":"Feng","year":"2015","journal-title":"Breast Cancer Res Treat"},{"key":"2022070815273642100_zrab027-B12","doi-asserted-by":"crossref","first-page":"976","DOI":"10.3109\/0284186X.2016.1146826","article-title":"The accuracy of preoperative axillary nodal staging in primary breast cancer by ultrasound is modified by nodal metastatic load and tumor biology","volume":"55","author":"Dihge","year":"2016","journal-title":"Acta Oncol"},{"key":"2022070815273642100_zrab027-B13","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1002\/bjs.9663","article-title":"Meta-analysis of ultrasound-guided biopsy of suspicious axillary lymph nodes in the selection of patients with extensive axillary tumour burden in breast cancer","volume":"102","author":"van Wely","year":"2015","journal-title":"Br J Surg"},{"key":"2022070815273642100_zrab027-B14","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1245\/s10434-013-3229-6","article-title":"Value of preoperative ultrasound-guided axillary lymph node biopsy for preventing completion axillary lymph node dissection in breast cancer: a systematic review and meta-analysis","volume":"21","author":"Diepstraten","year":"2014","journal-title":"Ann Surg Oncol"},{"key":"2022070815273642100_zrab027-B15","doi-asserted-by":"crossref","first-page":"396","DOI":"10.1016\/j.crad.2018.01.003","article-title":"Evolving imaging techniques for staging axillary lymph nodes in breast cancer","volume":"73","author":"Lowes","year":"2018","journal-title":"Clin Radiol"},{"key":"2022070815273642100_zrab027-B16","doi-asserted-by":"crossref","first-page":"3670","DOI":"10.1200\/JCO.2006.08.8013","article-title":"Doctor, what are my chances of having a positive sentinel node? A validated nomogram for risk estimation","volume":"25","author":"Bevilacqua","year":"2007","journal-title":"J Clin Oncol"},{"key":"2022070815273642100_zrab027-B17","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1016\/j.ejca.2012.04.025","article-title":"Assessment of the Memorial Sloan-Kettering Cancer Center nomogram to predict sentinel lymph node metastases in a Dutch breast cancer population","volume":"49","author":"van la Parra","year":"2013","journal-title":"Eur J Cancer"},{"key":"2022070815273642100_zrab027-B18","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1007\/s10549-012-2219-x","article-title":"Predicting sentinel lymph node metastasis in a Chinese breast cancer population: assessment of an existing nomogram and a new predictive nomogram","volume":"135","author":"Chen","year":"2012","journal-title":"Breast Cancer Res Treat"},{"key":"2022070815273642100_zrab027-B19","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1007\/s10549-014-3225-y","article-title":"Reduced risk of axillary lymphatic spread in triple-negative breast cancer","volume":"149","author":"Holm-Rasmussen","year":"2015","journal-title":"Breast Cancer Res Treat"},{"key":"2022070815273642100_zrab027-B20","doi-asserted-by":"crossref","first-page":"55534","DOI":"10.18632\/oncotarget.15022","article-title":"Lymph node status in different molecular subtype of breast cancer: triple negative tumours are more likely lymph node negative","volume":"8","author":"Liu","year":"2017","journal-title":"Oncotarget"},{"key":"2022070815273642100_zrab027-B21","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1002\/bjs.10583","article-title":"Nomograms for preoperative prediction of axillary nodal status in breast cancer","volume":"104","author":"Dihge","year":"2017","journal-title":"Br J Surg"},{"year":"2008","author":"Regionala cancercentrum i samverkan. National","key":"2022070815273642100_zrab027-B22"},{"key":"2022070815273642100_zrab027-B23","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1002\/bjs.9736","article-title":"Transparent Reporting of a multivariable prediction model for Individual Prognosis Or Diagnosis (TRIPOD): the TRIPOD Statement","volume":"102","author":"Collins","year":"2015","journal-title":"Br J Surg"},{"key":"2022070815273642100_zrab027-B24","doi-asserted-by":"crossref","first-page":"h5527","DOI":"10.1136\/bmj.h5527","article-title":"STARD 2015: an updated list of essential items for reporting diagnostic accuracy studies","volume":"351","author":"Bossuyt","year":"2015","journal-title":"Bmj"},{"year":"2008","author":"Regionala cancercentrum i samverkan. Swedish National Guidelines for Breast Cancer","key":"2022070815273642100_zrab027-B25"},{"key":"2022070815273642100_zrab027-B26","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1186\/s12889-019-6846-6","article-title":"Validation of data quality in the Swedish National Register for Breast Cancer","volume":"19","author":"Lofgren","year":"2019","journal-title":"BMC Public Health"},{"year":"2020","author":"The Swedish Society of Pathology (KVAST)","key":"2022070815273642100_zrab027-B27"},{"key":"2022070815273642100_zrab027-B28","doi-asserted-by":"crossref","first-page":"2206","DOI":"10.1093\/annonc\/mdt303","article-title":"Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013","volume":"24","author":"Goldhirsch","year":"2013","journal-title":"Ann Oncol"},{"key":"2022070815273642100_zrab027-B29","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1001\/jama.284.1.79","article-title":"Users' guides to the medical literature \u2013 XXII: how to use articles about clinical decision rules","volume":"284","author":"McGinn","year":"2000","journal-title":"JAMA"},{"key":"2022070815273642100_zrab027-B30","doi-asserted-by":"crossref","DOI":"10.1002\/9781118548387","volume-title":"Applied Logistic Regression","author":"Hosmer","year":"2013","edition":"3rd edn)."},{"key":"2022070815273642100_zrab027-B31","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1186\/1471-2288-14-40","article-title":"External validation of multivariable prediction models: a systematic review of methodological conduct and reporting","volume":"14","author":"Collins","year":"2014","journal-title":"BMC Med Res Methodol"},{"key":"2022070815273642100_zrab027-B32","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1016\/S1470-2045(13)70035-4","article-title":"Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): a phase 3 randomised controlled trial","volume":"14","author":"Galimberti","year":"2013","journal-title":"Lancet Oncol"},{"key":"2022070815273642100_zrab027-B33","doi-asserted-by":"crossref","first-page":"918","DOI":"10.1001\/jama.2017.11470","article-title":"Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: The ACOSOG Z0011 (Alliance) randomized clinical trial","volume":"318","author":"Giuliano","year":"2017","journal-title":"JAMA"},{"key":"2022070815273642100_zrab027-B34","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.1056\/NEJMoa022152","article-title":"Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer","volume":"347","author":"Fisher","year":"2002","journal-title":"N Engl J Med"},{"key":"2022070815273642100_zrab027-B35","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1200\/JCO.2005.01.5784","article-title":"Randomized trial comparing axillary clearance versus no axillary clearance in older patients with breast cancer: first results of International Breast Cancer Study Group Trial 10-93","volume":"24","author":"International Breast Cancer Study Group","year":"2006","journal-title":"J Clin Oncol"},{"key":"2022070815273642100_zrab027-B36","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1016\/j.ejso.2014.03.029","article-title":"Axillary dissection versus no axillary dissection in older T1N0 breast cancer patients: 15-year results of trial and out-trial patients","volume":"40","author":"Martelli","year":"2014","journal-title":"Eur J Surg Oncol"},{"key":"2022070815273642100_zrab027-B37","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1002\/cncr.28499","article-title":"Axillary lymph node dissection versus no dissection in patients with T1N0 breast cancer","volume":"120","author":"Agresti","year":"2014","journal-title":"Cancer"},{"key":"2022070815273642100_zrab027-B38","doi-asserted-by":"crossref","first-page":"1277","DOI":"10.1016\/j.ejso.2008.01.034","article-title":"Axillary recurrence after a tumour-negative sentinel node biopsy in breast cancer patients: a systematic review and meta-analysis of the literature","volume":"34","author":"van der Ploeg","year":"2008","journal-title":"Eur J Surg Oncol"},{"key":"2022070815273642100_zrab027-B39","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1016\/S1470-2045(10)70207-2","article-title":"Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial","volume":"11","author":"Krag","year":"2010","journal-title":"Lancet Oncol"},{"key":"2022070815273642100_zrab027-B40","doi-asserted-by":"crossref","first-page":"35311","DOI":"10.18632\/oncotarget.13330","article-title":"A nomogram to predict the probability of axillary lymph node metastasis in female patients with breast cancer in China: a nationwide, multicenter, 10-year epidemiological study","volume":"8","author":"Zhang","year":"2017","journal-title":"Oncotarget"},{"key":"2022070815273642100_zrab027-B41","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1038\/nrclinonc.2011.178","article-title":"Practical implications of gene-expression-based assays for breast oncologists","volume":"9","author":"Prat","year":"2011","journal-title":"Nat Rev Clin Oncol"},{"key":"2022070815273642100_zrab027-B42","doi-asserted-by":"crossref","first-page":"R83","DOI":"10.1186\/bcr3198","article-title":"Local-regional control according to surrogate markers of breast cancer subtypes and response to neoadjuvant chemotherapy in breast cancer patients undergoing breast conserving therapy","volume":"14","author":"Caudle","year":"2012","journal-title":"Breast Cancer Res"},{"key":"2022070815273642100_zrab027-B43","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.jclinepi.2019.02.016","article-title":"The proportion of missing data should not be used to guide decisions on multiple imputation","volume":"110","author":"Madley-Dowd","year":"2019","journal-title":"J Clin Epidemiol"},{"key":"2022070815273642100_zrab027-B44","doi-asserted-by":"crossref","first-page":"610","DOI":"10.1186\/s12885-019-5827-6","article-title":"Artificial neural network models to predict nodal status in clinically node-negative breast cancer","volume":"19","author":"Dihge","year":"2019","journal-title":"BMC Cancer"},{"key":"2022070815273642100_zrab027-B45","doi-asserted-by":"crossref","first-page":"6368","DOI":"10.1158\/1078-0432.CCR-19-0075","article-title":"Prediction of lymph node metastasis in breast cancer by gene expression and clinicopathological models: development and validation within a population-based cohort","volume":"25","author":"Dihge","year":"2019","journal-title":"Clin Cancer Res"}],"container-title":["BJS Open"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bjsopen\/article-pdf\/5\/3\/zrab027\/44658094\/zrab027.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bjsopen\/article-pdf\/5\/3\/zrab027\/44658094\/zrab027.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,8]],"date-time":"2022-07-08T15:30:50Z","timestamp":1657294250000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bjsopen\/article\/doi\/10.1093\/bjsopen\/zrab027\/6308066"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5]]},"references-count":45,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2021,5,7]]}},"URL":"https:\/\/doi.org\/10.1093\/bjsopen\/zrab027","relation":{},"ISSN":["2474-9842"],"issn-type":[{"type":"electronic","value":"2474-9842"}],"subject":[],"published-other":{"date-parts":[[2021,5]]},"published":{"date-parts":[[2021,5]]},"article-number":"zrab027"}}