{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T03:38:18Z","timestamp":1788406698777,"version":"build-2803163510"},"reference-count":52,"publisher":"SAGE Publications","issue":"4","license":[{"start":{"date-parts":[[2023,8,1]],"date-time":"2023-08-01T00:00:00Z","timestamp":1690848000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.sagepub.com\/page\/policies\/text-and-data-mining-license"}],"content-domain":{"domain":["journals.sagepub.com"],"crossmark-restriction":true},"short-container-title":["Lymphatic Research and Biology"],"published-print":{"date-parts":[[2023,8,1]]},"abstract":"<jats:sec>\n                    <jats:title>Introduction:<\/jats:title>\n                    <jats:p>The reported incidences of breast cancer-related lymphedema (LE) affecting the arms vary greatly. Reason for this variability includes different diagnostic techniques used across studies. In the current study, we compared the accuracy of indocyanine green lymphography (ICG_L) and bioimpedance spectroscopy (BIS) in detecting LE before presentation of clinical signs.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods and Results:<\/jats:title>\n                    <jats:p>\n                      Patients with no initial detectable signs of clinical LE of their arms after axillary lymph node dissection or removal of &gt;5 lymph nodes on sentinel lymph node biopsy were included. Subclinical LE was defined as BIS values outside the normal range [(\u22657 units (or &gt;10 units)] or a 7-unit (or 10 unit) change between two measurements. We tracked ICG_L and BIS measurements for 133 potentially affected arms (\n                      <jats:italic toggle=\"yes\">n<\/jats:italic>\n                      \u2009=\u2009123). ICG_L detected signs of lymphatic flow disruption in 63 arms (47%). Based on the BIS value of 7 units, 60 arms (45%) had values outside the normal range. When using ICG_L-identified LE cases as true positives, BIS had a 54% accuracy (area under the curve [AUC]\u2009=\u20090.54) in detecting LE. Accuracy was 61% for subclinical LE symptoms when compared with ICG_L (AUC\u2009=\u20090.62). Both BIS and subclinical LE symptoms had &lt;0.70 AUC-receiver characteristic operator curve, suggesting that BIS and development of subclinical LE symptoms are not adequate for identifying patients with subclinical LE.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion:<\/jats:title>\n                    <jats:p>ICG_L is a reliable diagnostic tool for detecting early signs of lymphatic flow disruption in subclinical LE. Utilizing ICG_L to diagnose subclinical LE followed by a personalized treatment plan may provide patients the best chance of preventing disease progression.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1089\/lrb.2022.0066","type":"journal-article","created":{"date-parts":[[2023,3,22]],"date-time":"2023-03-22T10:50:38Z","timestamp":1679482238000},"page":"359-365","update-policy":"https:\/\/doi.org\/10.1177\/sage-journals-update-policy","source":"Crossref","is-referenced-by-count":12,"title":["Early Detection of Breast Cancer-Related Lymphedema: Accuracy of Indocyanine Green Lymphography Compared with Bioimpedance Spectroscopy and Subclinical Lymphedema Symptoms"],"prefix":"10.1177","volume":"21","author":[{"given":"Atilla","family":"Soran","sequence":"first","affiliation":[{"name":"Comprehensive Lymphedema Program, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA."},{"name":"Department of Surgery and University of Pittsburgh, Pittsburgh, Pennsylvania, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6036-3458","authenticated-orcid":false,"given":"Fuat Baris","family":"Bengur","sequence":"additional","affiliation":[{"name":"Department of Plastic and Reconstructive Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wendy","family":"Rodriguez","sequence":"additional","affiliation":[{"name":"Comprehensive Lymphedema Program, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Z.","family":"Chroneos","sequence":"additional","affiliation":[{"name":"Department of Surgery and University of Pittsburgh, Pittsburgh, Pennsylvania, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Efe","family":"Sezgin","sequence":"additional","affiliation":[{"name":"Department of Food Engineering, Izmir Institute of Technology, Izmir, Turkey."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"179","published-online":{"date-parts":[[2023,8,22]]},"reference":[{"key":"e_1_3_5_2_2","doi-asserted-by":"publisher","DOI":"10.1016\/S1470-2045(13)70076-7"},{"key":"e_1_3_5_3_2","doi-asserted-by":"publisher","DOI":"10.1200\/JCO.2002.09.018"},{"key":"e_1_3_5_4_2","doi-asserted-by":"publisher","DOI":"10.4137\/CMO.S6389"},{"key":"e_1_3_5_5_2","doi-asserted-by":"publisher","DOI":"10.1200\/JCO.2008.16.3725"},{"key":"e_1_3_5_6_2","doi-asserted-by":"publisher","DOI":"10.3322\/caac.20001"},{"key":"e_1_3_5_7_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1524-4741.2006.00342.x"},{"key":"e_1_3_5_8_2","doi-asserted-by":"publisher","DOI":"10.1097\/COC.0b013e3181f47955"},{"key":"e_1_3_5_9_2","doi-asserted-by":"publisher","DOI":"10.1200\/JCO.19.02896"},{"key":"e_1_3_5_10_2","article-title":"Risk of lymphedema following contemporary treatment for breast cancer","author":"Byun HK","year":"2019","unstructured":"Byun HK, , Chang JS, , Im SH, et al. Risk of lymphedema following contemporary treatment for breast cancer. Ann Surg, 2019; doi: 10.1097\/sla.0000000000003491","journal-title":"Ann Surg"},{"key":"e_1_3_5_11_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10549-013-2715-7"},{"key":"e_1_3_5_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijrobp.2018.08.036"},{"key":"e_1_3_5_13_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10549-016-4089-0"},{"issue":"2","key":"e_1_3_5_14_2","article-title":"Surgical interventions for the prevention or treatment of lymphoedema after breast cancer treatment","volume":"2","author":"Markkula SP","year":"2019","unstructured":"Markkula SP, , Leung N, , Allen VB, et al. Surgical interventions for the prevention or treatment of lymphoedema after breast cancer treatment. Cochrane Database Syst Rev, 2019; 2(2);CD011433; doi: 10.1002\/14651858.CD011433.pub2","journal-title":"Cochrane Database Syst Rev"},{"key":"e_1_3_5_15_2","doi-asserted-by":"publisher","DOI":"10.1097\/PRS.0000000000007783"},{"key":"e_1_3_5_16_2","doi-asserted-by":"publisher","DOI":"10.1097\/PRS.0000000000005993"},{"key":"e_1_3_5_17_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1524-4741.2012.01252.x"},{"key":"e_1_3_5_18_2","doi-asserted-by":"publisher","DOI":"10.3322\/caac.21583"},{"key":"e_1_3_5_19_2","doi-asserted-by":"publisher","DOI":"10.1007\/s12282-018-0830-3"},{"key":"e_1_3_5_20_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.breast.2017.09.006"},{"key":"e_1_3_5_21_2","doi-asserted-by":"publisher","DOI":"10.1089\/lrb.2018.0033"},{"key":"e_1_3_5_22_2","doi-asserted-by":"publisher","DOI":"10.1089\/lrb.2014.0035"},{"key":"e_1_3_5_23_2","doi-asserted-by":"publisher","DOI":"10.1002\/cncr.31873"},{"issue":"1","key":"e_1_3_5_24_2","first-page":"2","article-title":"Early diagnosis of lymphedema using multiple frequency bioimpedance","volume":"34","author":"Cornish BH","year":"2001","unstructured":"Cornish BH, , Chapman M, , Hirst C, et al. Early diagnosis of lymphedema using multiple frequency bioimpedance. Lymphology, 2001; 34(1):2\u201311.","journal-title":"Lymphology"},{"key":"e_1_3_5_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijrobp.2010.01.001"},{"key":"e_1_3_5_26_2","doi-asserted-by":"publisher","DOI":"10.1002\/jso.24365"},{"key":"e_1_3_5_27_2","doi-asserted-by":"publisher","DOI":"10.1111\/tbj.12647"},{"key":"e_1_3_5_28_2","doi-asserted-by":"publisher","DOI":"10.1245\/s10434-019-07344-5"},{"key":"e_1_3_5_29_2","first-page":"2","article-title":"The impact of L-Dex\u00ae measurements in assessing breast cancer-related lymphedema as part of routine clinical practice","volume":"7","author":"Laidley A","year":"2016","unstructured":"Laidley A, , Anglin B. The impact of L-Dex\u00ae measurements in assessing breast cancer-related lymphedema as part of routine clinical practice. Front Oncol, 2016; 7(Sep):2\u20137; doi: 10.3389\/fonc.2016.00192","journal-title":"Front Oncol"},{"key":"e_1_3_5_30_2","doi-asserted-by":"publisher","DOI":"10.1089\/lrb.2018.0028"},{"key":"e_1_3_5_31_2","doi-asserted-by":"publisher","DOI":"10.1089\/lrb.2021.0084"},{"key":"e_1_3_5_32_2","doi-asserted-by":"publisher","DOI":"10.1089\/lrb.2017.0070"},{"key":"e_1_3_5_33_2","doi-asserted-by":"publisher","DOI":"10.1002\/cam4.3188"},{"issue":"1","key":"e_1_3_5_34_2","first-page":"43","article-title":"The third circulation: Radionuclide lymphoscintigraphy in the evaluation of lymphedema","volume":"44","author":"Szuba A","year":"2003","unstructured":"Szuba A, , Shin WS, , Strauss HW, et al. The third circulation: Radionuclide lymphoscintigraphy in the evaluation of lymphedema. J Nucl Med, 2003; 44(1):43\u201357.","journal-title":"J Nucl Med"},{"key":"e_1_3_5_35_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jamcollsurg.2017.06.005"},{"key":"e_1_3_5_36_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00268-004-7252-4"},{"key":"e_1_3_5_37_2","doi-asserted-by":"publisher","DOI":"10.1055\/s-0035-1564608"},{"key":"e_1_3_5_38_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.surg.2022.08.026"},{"key":"e_1_3_5_39_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.surg.2022.04.015"},{"key":"e_1_3_5_40_2","doi-asserted-by":"publisher","DOI":"10.1097\/MD.0000000000020432"},{"key":"e_1_3_5_41_2","doi-asserted-by":"publisher","DOI":"10.3390\/cancers12010135"},{"key":"e_1_3_5_42_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejso.2019.06.009"},{"key":"e_1_3_5_43_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bjps.2013.02.023"},{"key":"e_1_3_5_44_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0038182"},{"key":"e_1_3_5_45_2","doi-asserted-by":"publisher","DOI":"10.1186\/s12885-019-6192-1"},{"key":"e_1_3_5_46_2","doi-asserted-by":"publisher","DOI":"10.1097\/PRS.0b013e3182a4d626"},{"issue":"2","key":"e_1_3_5_47_2","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1097\/PSN.0000000000000306","article-title":"Bioimpedance spectroscopy for assessment of breast cancer-related lymphedema: A systematic review","volume":"40","author":"Forte AJ","year":"2020","unstructured":"Forte AJ, , Huayllani MT, , Boczar D, et al. Bioimpedance spectroscopy for assessment of breast cancer-related lymphedema: A systematic review. Plast Surg Nurs: official journal of the American Society of Plastic and Reconstructive Surgical Nurses, 2020; 40(2):86\u201390; doi: 10.1097\/PSN.0000000000000306","journal-title":"Plast Surg Nurs: official journal of the American Society of Plastic and Reconstructive Surgical Nurses"},{"key":"e_1_3_5_48_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bjps.2018.02.012"},{"key":"e_1_3_5_49_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.bjps.2019.06.041"},{"key":"e_1_3_5_50_2","doi-asserted-by":"publisher","DOI":"10.1007\/s10549-015-3357-8"},{"key":"e_1_3_5_51_2","doi-asserted-by":"publisher","DOI":"10.1245\/s10434-015-4683-0"},{"key":"e_1_3_5_52_2","doi-asserted-by":"publisher","DOI":"10.1089\/lrb.2020.0097"},{"key":"e_1_3_5_53_2","doi-asserted-by":"publisher","DOI":"10.1089\/lrb.2020.0090"}],"container-title":["Lymphatic Research and Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.sagepub.com\/doi\/full-xml\/10.1089\/lrb.2022.0066","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1089\/lrb.2022.0066","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.sagepub.com\/doi\/pdf\/10.1089\/lrb.2022.0066","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,1]],"date-time":"2026-05-01T20:14:46Z","timestamp":1777666486000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.sagepub.com\/doi\/10.1089\/lrb.2022.0066"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,1]]},"references-count":52,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2023,8,1]]}},"alternative-id":["10.1089\/lrb.2022.0066"],"URL":"https:\/\/doi.org\/10.1089\/lrb.2022.0066","relation":{},"ISSN":["1539-6851","1557-8585"],"issn-type":[{"value":"1539-6851","type":"print"},{"value":"1557-8585","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,1]]}}}