{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,14]],"date-time":"2026-06-14T17:21:58Z","timestamp":1781457718621,"version":"3.54.1"},"reference-count":38,"publisher":"Public Library of Science (PLoS)","issue":"7","license":[{"start":{"date-parts":[[2021,7,9]],"date-time":"2021-07-09T00:00:00Z","timestamp":1625788800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:sec id=\"sec001\"><jats:title>Introduction<\/jats:title><jats:p>The classical lymphoscintigraphic investigations of lower-limb lymphatic edema [LLLE] sometimes reveal either no or few lymph nodes [LNs] at the root of the limb[s] and\/or in the abdomen. The aim of the present paper is to report the results of performing one additional injection at the root of the edematous limb[s] to force the visualization of the LNs and\/or to demonstrate the collateral lymphatic pathways in such patients.<\/jats:p><\/jats:sec><jats:sec id=\"sec002\"><jats:title>Methods and findings<\/jats:title><jats:p>We retrospectively reviewed our database and found 99 patients [44 primary LLLE with 47 limbs injected and 55 with LLLE secondary to treatments for cancer with 64 limbs injected] where such an additional injection had been performed.<\/jats:p><jats:p>In the 43 LLLE patients where no LNs were seen at the end of the classical exam [15 primary LLLE and 28 secondary LLLE], the extra injection showed lymphatic drainage toward LN[s] in all except 3 and when at least one LN was seen, the injection showed lymphatic drainage in every case toward the same ipsilateral [inguinal and\/or iliac] LNs [as shown by the classical injection] and\/or toward additional LNs.<\/jats:p><jats:p>In 40.7% of patients, we observed one or more additional lymphatic pathways: prepubic superficial lymphatic vessels [LV] crossing the midline anteriorly toward contralateral inguinal LNs in 21 [18.9%], \u201cposterior\u201d LV [toward contralateral inguinal LNs and\/or ipsi- or contralateral lumbo-aortic and\/or para-renal LNs] in 14 [12.6%], but deep LV toward the ipsilateral common iliac LNs passing between the gluteal muscles in 32 [28.8%].<\/jats:p><\/jats:sec><jats:sec id=\"sec003\"><jats:title>Conclusion<\/jats:title><jats:p>Our work pinpoints one limitation of classical bipedal radionuclide lymphangiography. In patients with primary and secondary LLLE where inguinal and\/or iliac LNs cannot be seen on bipedal radionuclide lymphangiography, this additional injection reveals the true lympho-nodal status and shows unexpected collateral lymphatic pathways in 40% of cases. Such information is of the utmost importance in LLLE management and its acquisition is consequently recommended in these patients.<\/jats:p><\/jats:sec>","DOI":"10.1371\/journal.pone.0253900","type":"journal-article","created":{"date-parts":[[2021,7,9]],"date-time":"2021-07-09T18:00:48Z","timestamp":1625853648000},"page":"e0253900","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":6,"title":["Value of one additional injection at the root of the limb in the lymphoscintigraphic evaluation and management of primary and secondary lower-limb lymphedemas"],"prefix":"10.1371","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7349-4334","authenticated-orcid":true,"given":"Pierre","family":"Bourgeois","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olivier","family":"Leduc","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2021,7,9]]},"reference":[{"key":"pone.0253900.ref001","first-page":"43","article-title":"The third circulation: radionuclide lymphoscintigraphy in the evaluation of lymphedema","volume":"44","author":"A Szuba","year":"2003","journal-title":"J Nucl Med"},{"key":"pone.0253900.ref002","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-319-14493-1","volume-title":"Lymphedema: presentation, diagnosis and treatment","author":"AK Green","year":"2015"},{"key":"pone.0253900.ref003","volume-title":"Lymphedema: a concise compendium of theory and practice","author":"BB Lee","year":"2018"},{"key":"pone.0253900.ref004","first-page":"367","volume-title":"Lymphedema: a concise compendium of theory and practice","author":"P Bourgeois","year":"2011"},{"key":"pone.0253900.ref005","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1007\/978-3-319-14493-1_15","volume-title":"Lymphedema: presentation, diagnosis and treatment","author":"P Bourgeois","year":"2015"},{"key":"pone.0253900.ref006","first-page":"278","article-title":"Lymph nodes and vessels in primary lymphoedema. Their relative importance in aetiology","volume":"58","author":"JB Kinmonth","year":"1976","journal-title":"Ann R Coll Surg Engl"},{"issue":"7","key":"pone.0253900.ref007","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1002\/micr.30501","article-title":"SPECT-CT and fusion ultrasound to target the efferent groin lymph node for lymphatic surgery","volume":"39","author":"S Gentileschi","year":"2019","journal-title":"Microsurgery"},{"issue":"1","key":"pone.0253900.ref008","first-page":"1976","article-title":"Les anastomoses lympho-lymphatiques: incidences th\u00e9rapeutiques","volume":"IV","author":"A Leduc","journal-title":"Travaux de la Soci\u00e9t\u00e9 Scientifique Belge de Kin\u00e9sith\u00e9rapie"},{"key":"pone.0253900.ref009","unstructured":"Belnuc | Methodological protocol for lymphoscintigraphy in limb edema [Prof. Bourgeois]\u2014Belnuc."},{"key":"pone.0253900.ref010","first-page":"22","article-title":"Evaluation of a three-phase lymphoscintigraphic investigation protocol of the lower limbedema.","volume":"21","author":"P Bourgeois","year":"1997","journal-title":"Eur J Lymphol"},{"key":"pone.0253900.ref011","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1016\/j.mednuc.2010.10.008","article-title":"La lymphoscintigraphie dans la prise en charge th\u00e9rapeutique des \u0153d\u00e8mes des membres par les soins de sant\u00e9 en Belgique Lymphoscintigraphy in the management of lymphedemas and their health costs","volume":"34","author":"P. Bourgeois","year":"2010","journal-title":"M\u00e9decine Nucl\u00e9aire"},{"issue":"1","key":"pone.0253900.ref012","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1186\/s12957-018-1379-5","article-title":"Use of lymphoscintigraphy to differentiate primary versus secondary lower extremity lymphedema after surgical lymphadenectomy: a retrospective analysis","volume":"16","author":"MM Roman","year":"2018","journal-title":"World J Surg Oncol"},{"issue":"1","key":"pone.0253900.ref013","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1148\/radiol.2019191169","article-title":"Lower-Limb Lymphatic Drainage Pathways and Lymph Nodes: A CT Lymphangiography Cadaver Study","volume":"294","author":"A A Shinaoka","year":"2020","journal-title":"Radiology"},{"issue":"4","key":"pone.0253900.ref014","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1097\/MNM.0b013e32831bec4d","article-title":"Scintigraphic investigations of the superficial lymphatic system: quantitative differences between intradermal and subcutaneous injections.","volume":"30","author":"P Bourgeois","year":"2009","journal-title":"Nucl Med Commun"},{"key":"pone.0253900.ref015","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1001\/archsurg.1981.01380210037007","article-title":"The prognosis of primary lymphedema of the lower limb","volume":"116","author":"JH Wolfe","year":"1981","journal-title":"Arch Surg"},{"key":"pone.0253900.ref016","first-page":"5","article-title":"Adenolympho-saphenous anastomosis using the Nielubowicz-Olszewski-Sakolowski method","volume":"24","author":"E Moreno Gonzalez","year":"1972","journal-title":"Angiologia"},{"key":"pone.0253900.ref017","first-page":"11","article-title":"Lymphedema and lymphonodovenous anastomosis. Proposal of a technical modification","volume":"41","author":"GB Languasco","year":"1989","journal-title":"Angiologia"},{"key":"pone.0253900.ref018","doi-asserted-by":"crossref","first-page":"923","DOI":"10.1002\/jso.24170","article-title":"Lymphedema surgery: Patient selection and an overview of surgical techniques","volume":"113","author":"RJ Allen","year":"2016","journal-title":"J Surg Oncol"},{"key":"pone.0253900.ref019","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1097\/SLA.0000000000002917","article-title":"Validity of the Novel Taiwan Lymphoscintigraphy Staging and Correlation of Cheng Lymphedema Grading for Unilateral Extremity Lymphedema","volume":"268","author":"MH Cheng","year":"2018","journal-title":"Annals of Surgery"},{"key":"pone.0253900.ref020","first-page":"19","article-title":"Homologous and autologous experimental lymph vessel transplantation: initial experience","volume":"3","author":"RG Baumeister","year":"1981","journal-title":"Int J Microsurg"},{"key":"pone.0253900.ref021","first-page":"34","article-title":"Microsurgical Lymphatic Vessel Transplantation","volume":"32","author":"RG Baumeister","year":"2016","journal-title":"J Reconstr Microsurg"},{"issue":"83","key":"pone.0253900.ref022","doi-asserted-by":"crossref","first-page":"2835","DOI":"10.1002\/(SICI)1097-0142(19981215)83:12B+<2835::AID-CNCR36>3.0.CO;2-V","article-title":"The physical treatment of upper limb edema","volume":"15","author":"O Leduc","year":"1998","journal-title":"Cancer"},{"key":"pone.0253900.ref023","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.ejogrb.2017.12.023","article-title":"Protocol of a randomised controlled trial regarding the effectiveness of fluoroscopy-guided manual lymph drainage for the treatment of breast cancer-related lymphoedema [EFforT-BCRL trial]","volume":"221","author":"T De Vrieze","year":"2018","journal-title":"Eur J Obstet Gynecol Reprod Biol"},{"issue":"3","key":"pone.0253900.ref024","first-page":"363","article-title":"Romero de Barros Marques A","volume":"5","author":"C Alcofordo de Almeaida","year":"2017","journal-title":"J Vasc Surg Venous Lymphat Sisord"},{"key":"pone.0253900.ref025","article-title":"Lymphoscintigraphic bilateral disease in patients with clinically unilateral primary lower limb lymphedemas","author":"P Bourgeois","year":"2020","journal-title":"Lymphat Res Biol"},{"key":"pone.0253900.ref026","first-page":"106","article-title":"Contributions of SPECT\/CT imaging to the lymphoscintigraphic investigations of the lower limb lymphedema","volume":"46","author":"F Baulieu","year":"2013","journal-title":"Lymphology"},{"key":"pone.0253900.ref027","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1016\/j.jvs.2007.01.023","article-title":"Preliminary experience with a novel fluorescence lymphography using indocyanine green in patients with secondary lymphedema","volume":"45","author":"N Unno","year":"2007","journal-title":"J Vasc Surg"},{"key":"pone.0253900.ref028","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.ejvs.2014.10.023","article-title":"Indocyanine Green Lymphography Findings in Primary Leg Lymphedema","volume":"49","author":"T Yamamoto","year":"2015","journal-title":"Eur J Vasc Endovasc Surg"},{"key":"pone.0253900.ref029","first-page":"72","article-title":"Indocyanine Green Lymphography Findings in Limb Lymphedema","volume":"32","author":"M Narushima","year":"2016","journal-title":"J Reconstr Microsurg"},{"issue":"8","key":"pone.0253900.ref030","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1002\/micr.30247","article-title":"Lymphatic mapping of the upper limb with lymphedema before lymphatic supermicrosurgery by mirroring of the healthy limb","volume":"37","author":"S Gentileschi","year":"2017","journal-title":"Microsurgery"},{"issue":"2","key":"pone.0253900.ref031","doi-asserted-by":"crossref","first-page":"306","DOI":"10.3390\/jcm9020306","article-title":"Changes in Indocyanine Green Lymphography Patterns after Physical Treatment in Secondary Upper Limb Lymphedema","volume":"9","author":"ME Medina-Rodr\u00edguez","year":"2020","journal-title":"J Clin Med"},{"key":"pone.0253900.ref032","unstructured":"HCPCS Code C9756."},{"key":"pone.0253900.ref033","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1089\/lrb.2010.0005","article-title":"Indocyanine Green and Lymphatic Imaging: Current Problems","volume":"2","author":"AA Gashev","year":"2010","journal-title":"Lymphatics Research Biology"},{"key":"pone.0253900.ref034","first-page":"1","article-title":"Differential transport function of lymphatic vessels in the rat tail model and the long-term effects of indocyanine Green as assessed with near-infrared imaging","volume":"4","author":"M Weiler","year":"2013","journal-title":"Frontier in Physiology"},{"key":"pone.0253900.ref035","doi-asserted-by":"crossref","first-page":"190","DOI":"10.3413\/Nukmed-0649-14-03","article-title":"Magnetic resonance imaging versus lymphoscintigraphy for the assessment of focal lymphatic transport disorders of the lower limb: first experiences","volume":"53","author":"M Weiss","year":"2014","journal-title":"Nuklearmedizin"},{"issue":"5","key":"pone.0253900.ref036","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1016\/j.jvsv.2020.03.007","article-title":"A systematic review of magnetic resonance lymphography for the evaluation of peripheral lymphedema","volume":"8","author":"RLM Miser\u00e9","year":"2020","journal-title":"J Vasc Surg Venous Lymphat Disord"},{"key":"pone.0253900.ref037","doi-asserted-by":"crossref","first-page":"190","DOI":"10.3413\/Nukmed-0649-14-03","article-title":"Magnetic resonance imaging versus lymphoscintigraphy for the assessment of focal lymphatic 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