Abstract
Cancer-related secondary lymphedema (LE) is a widespread issue, which markedly affects patients’ quality of life. Its diagnosis is mainly clinical since there is no consensus on the best imaging technique that should be used to assess this pathology. Even if lymphedema treatment has been traditionally conservative and mainly based on compressive bandages and decongestive therapy, new surgical techniques are proving their effectiveness in the management of the disease and made proper assessment and characterization of lymphedema necessary. In this scenario, non-contrast magnetic resonance lymphography (NCMRL) is acquiring an increasing role, as a non-invasive imaging technique, useful for the analysis of LE. NCMRL is an effective tool in diagnosis confirmation, in providing information about the structural changes of the affected limbs, in grading this disorder, and provides a guide for LE management and treatment planning. This article aims to provide an overview of the literature regarding this examination, analyzing the acquisition technique, the interpretation of the imaging findings and their usefulness, the advantages and limits of this technique, to help the radiologist approach this relatively new investigation in cases of cancer-related LE.
Similar content being viewed by others
References
Lee BB, Antignani PL, Baroncelli TA, Boccardo FM, Brorson H, Campisi C, Damstra RJ, Flour M, Giannoukas A, Laredo J, Liu NF, Michelini S, Piller N, Rockson SG, Scuderi A, Szolnoky G (2015) Yamamoto T (2015) Iua-Isvi consensus for diagnosis guideline of chronic lymphedema of the limbs. Int Angiol 34(4):311–332
Grada AA, Phillips TJ (2017) Lymphedema: Pathophysiology and clinical manifestations. J Am Acad Dermatol 77(6):1009–1020
Warren AG, Brorson H, Borud LJ, Slavin SA (2007) Lymphedema: a comprehensive review. Ann Plast Surg 59(4):464–472
Vignes S (2010) Lymphœdèmes secondaires des membres [Secondary limb lymphedema]. Presse Med 39(12):1287–1291
Newman B, Lose F, Kedda MA, Francois M, Ferguson K, Janda M, Yates P, Spurdle AB, Hayes SC (2012) Possible genetic predisposition to lymphedema after breast cancer. Lymphat Res Biol 10(1):2–13
Gould DJ, Mehrara BJ, Neligan P, Cheng MH, Patel KM (2018) Lymph node transplantation for the treatment of lymphedema. J Surg Oncol 118(5):736–742
Garza RM, Chang DW (2018) Lymphovenous bypass for the treatment of lymphedema. J Surg Oncol 118(5):743–749
O’Donnell TF Jr, Rasmussen JC, Sevick-Muraca EM (2017) New diagnostic modalities in the evaluation of lymphedema. J Vasc Surg 5(2):261–273
Lee YW, Lee SH, You HJ, Jung JA, Yoon ES, Kim DW (2018) Lymphatic vessel mapping in the upper extremities of a healthy Korean population. Arch Plast Surg 45(2):152–157
Mazzei MA, Gentili F, Mazzei FG, Gennaro P, Guerrieri D, Nigri A, Gabriele G, Weber E, Fausto A, Botta G, Volterrani L (2017) High-resolution MR lymphangiography for planning lymphaticovenous anastomosis treatment: a single-centre experience. Radiol Med 122(12):918–927
Bordonaro V, Ciancarella P, Ciliberti P, Curione D, Napolitano C, Santangelo TP, Natali GL, Rollo M, Guccione P, Pasquini L, Secinaro A (2021) Dynamic contrast-enhanced magnetic resonance lymphangiography in pediatric patients with central lymphatic system disorders. Radiol Med 126(5):737–743. https://doi.org/10.1007/s11547-020-01309-5
Mitsumori LM, McDonald ES, Neligan PC, Maki JH (2016) Peripheral magnetic resonance lymphangiography: techniques and applications. Tech Vasc Interv Radiol 19(4):262–272. https://doi.org/10.1053/j.tvir.2016.10.007
Cellina M, Martinenghi C, Panzeri M, Soresina M, Menozzi A, Daniele G, Oliva G (2021) Noncontrast MR lymphography in secondary lower limb lymphedema. J Magn Reson Imaging 53(2):458–466
Arrivé L, Derhy S, Dahan B, El Mouhadi S, Monnier-Cholley L, Menu Y, Becker C (2018) Primary lower limb lymphoedema: classification with non-contrast MR lymphography. Eur Radiol 28(1):291–300
Cellina M, Oliva G, Menozzi A, Soresina M, Martinenghi C, Gibelli D (2019) Non-contrast Magnetic Resonance Lymphangiography: an emerging technique for the study of lymphedema. Clin Imaging 53:126–133
Cellina M, Martinenghi C, Gibelli D, Menozzi A, Soresina M, Boccanera D, Giardini D, Oliva G (2020) secondary lymphedema following radical prostatectomy: noncontrast magnetic resonance lymphangiography assessment and vascularized lymph node transfer. Ann Plast Surg 85(5):e12–e18
Liu N, Wang C, Sun M (2005) Noncontrast three-dimensional magnetic resonance imaging vs lymphoscintigraphy in the evaluation of lymph circulation disorders: a comparative study. J Vasc Surg 41(1):69–75
Arrivé L, Derhy S, Dlimi C, El Mouhadi S, Monnier-Cholley L, Becker C (2017) Noncontrast magnetic resonance lymphography for evaluation of lymph node transfer for secondary upper limb lymphedema. Plast Reconstr Surg 140(6):806e–811e
Franconeri A, Ballati F, Panzuto F, Raciti MV, Smedile A, Maggi A, Asteggiano C, Esposito M, Stoppa D, Lungarotti L, Bortolotto C, Giardini D, De Silvestri A, Calliada F (2020) A proposal for a semiquantitative scoring system for lymphedema using Non-contrast Magnetic Resonance Lymphography (NMRL): Reproducibility among readers and correlation with clinical grading. Magn Reson Imaging 68:158–166
Crescenzi R, Donahue PMC, Hartley KG, Desai AA, Scott AO, Braxton V, Mahany H, Lants SK, Donahue MJ (2017) Lymphedema evaluation using noninvasive 3T MR lymphangiography. J Magn Reson Imaging 46(5):1349–1360
Lu Q, Xu J, Liu N (2010) Chronic lower extremity lymphedema: a comparative study of high-resolution interstitial MR lymphangiography and heavily T2-weighted MRI. Eur J Radiol 73(2):365–373
Dayan JH, Wiser I, Verma R, Shen J, Talati N, Goldman D, Mehrara BJ, Smith ML, Dayan MDE, CoriddiKagan MDMA (2020) Regional patterns of fluid and fat accumulation in patients with lower extremity lymphedema using magnetic resonance angiography. Plast Reconstr Surg 145(2):555–563
Borri M, Gordon KD, Hughes JC, Scurr ED, Koh DM, Leach MO, Mortimer PS, Schmidt MA (2017) Magnetic resonance imaging-based assessment of breast cancer-related lymphoedema tissue composition. Invest Radiol 52(9):554–561
Kim G, Smith MP, Donohoe KJ, Johnson AR, Singhal D, Tsai LL (2020) MRI staging of upper extremity secondary lymphedema: correlation with clinical measurements. Eur Radiol 30(8):4686–4694
Cellina M, Gibelli D, Floridi C, Oliva G (2020) Volumetric analysis of Non-contrast Magnetic Resonance Lymphangiography in patients affected by lower extremities primary lymphedema. Radiol Med 125(4):432–435
Gentili F, Guerrini S, Mazzei FG, Volterrani L, Mazzei MA (2020) MRL as one-shot examination for patients suffering from lymphedema. Radiol Med 125(8):798–799
Miseré RML, Wolfs JAGN, Lobbes MBI, van der Hulst RRWJ, Qiu SS (2020) A systematic review of magnetic resonance lymphography for the evaluation of peripheral lymphedema. J Vasc Surg Venous Lymphat Disord 8(5):882-892.e2
Sheng L, Zhang G, Li S, Jiang Z, Cao W (2020) Magnetic resonance lymphography of lymphatic vessels in upper extremity with breast cancer-related lymphedema. Ann Plast Surg 84(1):100–105
Arrivé L, Derhy S, El Mouhadi S, Monnier-Cholley L, Menu Y, Becker C (2016) Noncontrast Magnetic Resonance Lymphography. J Reconstr Microsurg 32(1):80–86
Tashiro K, Feng J, Wu SH, Mashiko T, Kanayama K, Narushima M, Uda H, Miyamoto S, Koshima I, Yoshimura K (2017) Pathological changes of adipose tissue in secondary lymphoedema. Br J Dermatol 177(1):158–167
Hadjis NS, Carr DH, Banks L, Pflug JJ (1985) The role of CT in the diagnosis of primary lymphedema of the lower limb. AJR Am J Roentgenol 144(2):361–364
Idy-Peretti I, Bittoun J, Alliot FA, Richard SB, Querleux BG, Cluzan RV (1998) Lymphedematous skin and subcutis: in vivo high resolution magnetic resonance imaging evaluation. J Invest Dermatol 110(5):782–787
Montag E, Okada AY, Arruda EGP, Fonseca AS, Bromley M, Munhoz AM, Busnardo FF, Gemperli R (2019) Influence of vascularized lymph node transfer (VLNT) flap positioning on the response to breast cancer-related lymphedema treatment. Rev Col Bras Cir 46(2):e2156
Beederman M, Garza RM, Agarwal S, Chang DW (2020) Outcomes for Physiologic Microsurgical Treatment of Secondary Lymphedema Involving the Extremity. Ann Surg. Epub ahead of print.
Mortimer P (2013) Arm lymphoedema after breast cancer. Lancet Oncol 14:442–443
Zampell JC, Aschen S, Weitman ES, Yan A, Elhadad S, De Brot AM, Mehrara BJ (2012) Regulation of adipogenesis by lymphatic fluid stasis: part I. Adipogenesis, fibrosis, and inflammation. Plast Reconstr Surg 129:825–834
Schneider M, Conway EM, Carmeliet P (2005) Lymph makes you fat. Nat Genet 37:1023–1024
Li Y, Lu Q, Chen TW, Yao Y, Zhao Z, Li Y, Xu J, Hu J, Haacke M (2015) Thickness of soft tissue of lower extremities measured with magnetic resonance imaging as a new indicator for staging unilateral secondary lower extremity lymphedema. Acta Radiol 56(8):1016–1024
Framework L (2006) Best practice for the management of lymphoedema. International consensus. http://old.ewma.org/fileadmin/user_upload/EWMA/Wound_Guidelines/Lymphoedema_Framework_Best_Practice_for_the_Management_of_Lymphoedema.pdf. Accessed May 9, 2021.
Brorson H (2016) Liposuction in lymphedema treatment. J Reconstr Microsurg 32:56–65
Kayıran O, De La Cruz C, Tane K, Soran A (2017) Lymphedema: from diagnosis to treatment. Turk J Surg 33(2):51
Garza R, Skoracki R, Hock K, Povoski SP (2017) A comprehensive overview on the surgical management of secondary lymphedema of the upper and lower extremities related to prior oncologic therapies. BMC Cancer 17(1):468
Ruddle NH (2014) Lymphatic vessels and tertiary lymphoid organs. J Clin Investig 124(3):953–959
Guerrini S, Gentili F, Mazzei FG, Gennaro P, Volterrani L, Mazzei MA (2020) Magnetic resonance lymphangiography: with or without contrast? Diagn Interv Radiol 26(6):587–595
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
The images used in this article belong to an IRB-approved study.
Informed consent
Patients provided informed written consent for the use of their anonymized images.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cellina, M., Gibelli, D., Martinenghi, C. et al. Non-contrast magnetic resonance lymphography (NCMRL) in cancer-related secondary lymphedema: acquisition technique and imaging findings. Radiol med 126, 1477–1486 (2021). https://doi.org/10.1007/s11547-021-01410-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11547-021-01410-3