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Bringing Lymphangiography into the 21st Century

2019; Radiological Society of North America; Volume: 294; Issue: 1 Linguagem: Inglês

10.1148/radiol.2019192368

1527-1315

Clifford R. Weiss, Robert P. Liddell,

Lymphatic Disorders and Treatments

HomeRadiologyVol. 294, No. 1 PreviousNext Reviews and CommentaryFree AccessEditorialBringing Lymphangiography into the 21st CenturyClifford R. Weiss , Robert P. LiddellClifford R. Weiss , Robert P. LiddellAuthor AffiliationsFrom the Department of Radiology and Radiological Sciences, Johns Hopkins School of Medicine, Sheik Zayed Tower, Suite 7203, 1800 Orleans St, Baltimore, MD 21287.Address correspondence to C.R.W. (e-mail: [email protected]).Clifford R. Weiss Robert P. LiddellPublished Online:Nov 19 2019https://doi.org/10.1148/radiol.2019192368MoreSectionsPDF ToolsImage ViewerAdd to favoritesCiteTrack CitationsPermissionsReprints ShareShare onFacebookTwitterLinked In See also the article by Shinaoka et al in this issue.Dr Weiss is an associate professor in the division of vascular and interventional radiology in the Russell H. Morgan Department of Radiology and Radiological Science at the Johns Hopkins University School of Medicine. He also holds appointments in surgery and biomedical engineering. Dr Weiss' clinical focus is on the treatment of complex vascular malformations, and his research is focused on the development of new embolic therapies and of interventional devices.Download as PowerPointOpen in Image Viewer Dr Liddell is an assistant professor in the division of vascular and interventional radiology in the Russell H. Morgan Department of Radiology and Radiological Science at the Johns Hopkins University School of Medicine. He also holds appointments in the Kimmel Cancer Center, Gastrointestinal Cancer Program. Dr Liddell's clinical and research interests focus on interventional oncology and new interventional radiology devices and procedures.Download as PowerPointOpen in Image Viewer Lymphedema is a chronic pathologic condition characterized by swelling of one or more limbs as a result of an impaired lymphatic drainage system. It affects approximately 250 million people worldwide (1). In developed countries, lymphedema usually occurs secondary to treatments for malignancy, such as lymph node biopsies and nodal dissections. For decades, lymphedema received little attention, mainly due to limited knowledge of lymphatic anatomy and physiology. Efforts to better understand the pathophysiology and clinical management of lymphedema have focused on developing improved lymphatic imaging and lymphatic bypass techniques. Diagnosis of lymphedema at an early stage is not only crucial for the prevention of disease progression but may also allow better outcomes from newly developed surgical techniques such as lymphovenous bypass. In particular, this technique has been shown to be more effective in the early rather than later, more severe, stages of lymphedema (2).For many years, lymphoscintigraphy was the reference standard imaging technique for lymphedema as it provided a reliable overall evaluation of lymphatic function. In lymphoscintigraphy, a radiotracer (technetium 99m) is injected into the interdigital web spaces and images are obtained at 60, 120, and 180 minutes (3). In patients with lymphedema, parameters obtained include (a) time-elapsed images to track the radiotracer as it traverses the affected limb, (b) the presence or absence of major collections, (c) lymph node visualization, and (d) the presence of dermal backflow. Although proven reliable, the primary downside of lympho-scintigraphy is the low image resolution. Other disadvantages include the cost, radiation exposure, and long examination time. As a result, lymphoscintigraphy has in recent years been relegated to a second-line imaging investigation in centers treating high volumes of patients with lymphedema.Transpedal and transnodal lymphangiography are used by interventional radiologists to visualize the lymphatic system (4). Most often these techniques are used to localize and treat iatrogenic and idiopathic lymphatic leakage. In transpedal lymphangiography, dye is injected into the first, second, and third interdigital spaces. Superficial lymphatic vessels within the dorsum of the foot are then identified, cannulated, and infused with iodized oil. During and at different time points after iodized oil injection, dependent on the progression of iodized oil in the lymphatic system, fluoroscopy, radiography, and CT can be used to visualize the lymphatic system. Compared with transpedal lymphangiography, transnodal lymphangiography offers a less technically challenging alternative and has therefore become increasingly used. Transnodal lymphangiography involves gaining US-guided access into a superficial lymph node, after which iodized oil is infused. As with transpedal lymphangiography, images at different time points are obtained in an effort to localize and treat lymphatic abnormalities. Both transpedal and transnodal lymphangiography provide detailed images of the lymphatic vessels and an ability to successfully localize and treat lymphatic abnormalities such as chylothorax, chylous ascites, chyluria, and lymphoceles. Disadvantages of these techniques include the fact that they are relatively invasive and time consuming and involve radiation. In addition, little is known of their role in the diagnosis of lymphedema.Currently, indocyanine green (ICG) lymphography is considered the most informative lymphatic imaging technique. ICG lymphography consists of administration of ICG into the region of interest by means of intradermal or subcutaneous injection. The region of interest is then illuminated with a light source emitting 760–780 nm while simultaneously imaging in the near-infrared spectrum at 830 nm. ICG lymphography is relatively simple to perform, is minimally invasive, is highly sensitive, involves no radiation, and accurately reflects the lymphatic system in real time. It provides (a) the precise location of functional lymphatic vessels, (b) the transport capacity of lymphatic vessels, (c) the presence of dermal backflow, and (d) the location of collateral lymphatic vessels. It is now part of the standard approach for lymphatic surgery. Among the available diagnostic methods, ICG lymphography has been shown to detect lymphedema earlier, even before patients become symptomatic (5). Major disadvantages of ICG lymphography include the fact that it cannot depict lymphatic vessels deeper than 1.5–2 cm under the skin and does not provide any significant soft-tissue anatomic information. A recent study using ICG lymphography showed that the lower extremity lymphatic vessels are divided into four distinct anatomic and functional groups (anteromedial, anterolateral, posteromedial, and posterolateral) (6). Limitations of that study and of ICG lymphography studies in general are that the relationship between a lymphatic group and its regional lymph nodes could not be determined due to its limited penetration depth. For similar reasons, ICG lymphography can depict the lymphatic vessels below the knee but often cannot be used to consistently identify those in the thigh.CT lymphangiography has recently been described as an imaging modality useful in the diagnosis of lymphedema. Advantages of CT lymphangiography for studying lymphedema include (a) excellent imaging resolution, (b) three-dimensional lymphatic architecture, (c) ability to image large areas of the body, and (d) short scanning time. In addition, imaging devices are widely distributed. However, CT lymphangiography has a disadvantage in its associated radiation exposure. Injection of small volumes of water-soluble, nonionic contrast material into interstitial tissues has been shown to enable the visualization of the lymphatic system in patients with lymphedema (7). As opposed to lymphoscintigraphy, individual lymphatic vessels can be visualized and anatomic information is provided. However, CT lymphangiography is less sensitive than ICG lymphography in the depiction and classification of dermal backflow, a hallmark of lymphedema.In this issue of Radiology, Shinaoka and colleagues (8) performed CT lymphangiography in 130 cadaveric lower extremities and in doing so provided high-definition maps of lymphatic vessels and, unlike prior ICG lymphography studies, their associated lymph nodes. The authors used a microscope to cannulate and infuse iodized oil into each individual lymphatic vessel at multiple locations around the foot. The resultant CT lymphangiography images were successfully used to map all four lower-extremity lymphatic groups and the specific regional lymph nodes they drained into (see fig 4). Interestingly, the authors demonstrated that just three lymph nodes in the lower extremity (two inguinal lymph nodes and one popliteal lymph node) receive 73% of the lymphatic drainage of the lower extremity, labeled as inferior lateral 1, inferior lateral 2, and superficial popliteal (figs 5, 6). These findings may have potential clinical implications with regard to not only the development of lymphedema, but potentially a better understanding of the spread of cancer via the lymphatic system. Furthermore, these findings illuminate a significant shortcoming of current lymphoscintigraphy and ICG lymphography techniques. Namely, that the most common tracer injection site for lymphatic imaging, the interdigital web spaces (sites 7–10 in fig 1), provides imaging of the anteromedial lymphatic pathway only. Based on their results, Shinaoka et al suggest additional injection sites in the lateral foot (sites 14 and 16 in fig 1) to visualize the anterolateral pathway and its regional lymph nodes (inferior lateral 2) and the posterolateral group and its node (superficial popliteal). A combination of injection sites including sites 7, 1, 14, and 16 would therefore be appropriate for analyzing the four lymphatic groups and the three specific lymph nodes for the lower extremity and would provide more complete and accurate lymphatic mapping. This work should allow for a more complete understanding of pathologic lymphatic conditions such as lymphedema and may guide surgical planning and radiation therapy planning to help reduce the incidence of lymphedema.As with lymphedema, efforts to better understand the relationship between lymphatic vessels and lymph nodes as they relate to the spread of cancer have traditionally relied on low-resolution imaging techniques. Sentinel lymph node (SNL) biopsy has become standard practice in patients with many forms of cancer, such as early stage breast cancer and melanoma, and is arguably the most important determinant of clinical outcomes. Reliable identification of SLNs is therefore crucial when properly staging cancers. Unfortunately, lymphoscintigraphy cannot clearly depict the lymphatic vessels between primary tumors and SNLs, and ICG lymphography requires significant technical skill to trace the dye-stained lymphatic connections to SNLs, and is again limited by issues with tissue penetration. Likewise, MR lymphangiography, which offers advantages with regard to soft-tissue resolution and three-dimensional anatomy, has been shown to suffer from venous contamination and motion artifacts when attempting to map SNLs. Originally developed as a means of examining sentinel lymph nodes, CT lymphangiography has been shown to enable the accurate detection and localization of SNLs and afferent lymphatic vessels in 96% of patients with breast cancer before surgery (9). Similarly, the findings reported by Shinaoka et al could guide appropriate SNL biopsy in patients with lower extremity melanoma. One might also imagine a future study designed to map the lymphatic drainage of the breast to specific lymph nodes within the axilla, better guiding SNL biopsies in patients with breast cancer.Disclosures of Conflicts of Interest: C.R.W. disclosed no relevant relationships. R.P.L. disclosed no relevant relationships.References1. McLaughlin SA. Lymphedema: separating fact from fiction. Oncology (Williston Park) 2012;26(3):242–249. Medline, Google Scholar2. Chang DW, Suami H, Skoracki R. A prospective analysis of 100 consecutive lymphovenous bypass cases for treatment of extremity lymphedema. Plast Reconstr Surg 2013;132(5):1305–1314. Crossref, Medline, Google Scholar3. Liu NF, Lu Q, Liu PA, Wu XF, Wang BS. Comparison of radionuclide lymphoscintigraphy and dynamic magnetic resonance lymphangiography for investigating extremity lymphoedema. Br J Surg 2010;97(3):359–365. Crossref, Medline, Google Scholar4. Pieper CC, Hur S, Sommer CM, et al. Back to the Future: Lipiodol in Lymphography-From Diagnostics to Theranostics. Invest Radiol 2019;54(9):600–615. Crossref, Medline, Google Scholar5. Yamamoto T, Yamamoto N, Yoshimatsu H, Narushima M, Koshima I. Factors Associated with Lower Extremity Dysmorphia Caused by Lower Extremity Lymphoedema. Eur J Vasc Endovasc Surg 2017;54(1):69–77. Crossref, Medline, Google Scholar6. Shinaoka A, Koshimune S, Yamada K, et al. Correlations between Tracer Injection Sites and Lymphatic Pathways in the Leg: A Near-Infrared Fluorescence Lymphography Study. Plast Reconstr Surg 2019;144(3):634–642. Crossref, Medline, Google Scholar7. Yamada K, Shinaoka A, Kimata Y. Three-Dimensional Imaging of Lymphatic System in Lymphedema Legs Using Interstitial Computed Tomography-lymphography. Acta Med Okayama 2017;71(2):171–177. Medline, Google Scholar8. Shinaoka A, Koshimune S, Suami H, et al. Lower limb lymphatic drainage pathways and lymph nodes: a CT lymphangiography cadaver study. Radiology 2020;294:223–229. Link, Google Scholar9. Yamamoto S, Suga K, Maeda K, Maeda N, Yoshimura K, Oka M. Breast sentinel lymph node navigation with three-dimensional computed tomography-lymphography: a 12-year study. Breast Cancer 2016;23(3):456–462. Crossref, Medline, Google ScholarArticle HistoryReceived: Oct 22 2019Revision requested: Oct 29 2019Revision received: Oct 30 2019Accepted: Oct 30 2019Published online: Nov 19 2019Published in print: Jan 2020 FiguresReferencesRelatedDetailsCited ByStandardizing lymphangiography and lymphatic interventions: a preclinical in vivo approach with detailed procedural stepsFengPan, Thuy D.Do, NiclasSchmitt, Dominik F.Vollherbst, MarkusMöhlenbruch, ParhamTinoush, AlexanderBrobeil, VitaliKoch, Götz M.Richter, Philippe L.Pereira, Hans U.Kauczor, Christof M.Sommer2023 | CVIR Endovascular, Vol. 6, No. 1[email protected]‐Based NIR‐II Lymphography Enables the Supersensitive Visualization of Lymphedema and Tumor Lymphatic MetastasisJiajunXu, YijingDu, TianyangHan, NingningZhu, ShoujunZhu2023 | Advanced Healthcare MaterialsDiagnostic Water-Soluble Contrast CT Lymphangiogram on Conventional CT Scanner with Local Anesthetic for Therapeutic PlanningNingchengLi, AlexDabrowiecki, Brett C.Sheppard, John A.Kaufman2022 | CardioVascular and Interventional Radiology, Vol. 45, No. 7Recent advancement of imaging strategies of the lymphatic system: Answer to the decades old questionsPriyankaBanerjee, SukanyaRoy, SanjuktaChakraborty2022 | Microcirculation, Vol. 29, No. 6-7Indocyanine green lymphography as novel tool to assess lymphatics in patients with lipedemaGiacomoBuso, LucieFavre, MarioMaufus, MarcellaHonorati, ClaudiaLessert, MichèleDepairon, WassimRaffoul, DidierTomson, LuciaMazzolai2022 | Microvascular Research, Vol. 140Visualization of Lymphatic Vessels Using Photoacoustic ImagingHirokiKajita, YushiSuzuki, HisashiSakuma, NobuakiImanishi, TetsuyaTsuji, MasahiroJinzaki, SadakazuAiso, KazuoKishi2020 | The Keio Journal of Medicine, Vol. 70, No. 4Accompanying This ArticleLower-Limb Lymphatic Drainage Pathways and Lymph Nodes: A CT Lymphangiography Cadaver StudyNov 19 2019RadiologyRecommended Articles Lower-Limb Lymphatic Drainage Pathways and Lymph Nodes: A CT Lymphangiography Cadaver StudyRadiology2019Volume: 294Issue: 1pp. 223-229Subcutaneous Lymphatic Vessels in the Lower Extremities: Comparison between Photoacoustic Lymphangiography and Near-Infrared Fluorescence LymphangiographyRadiology2020Volume: 295Issue: 2pp. 469-474Lymphatic Mapping Using US Microbubbles before Lymphaticovenous Anastomosis Surgery for LymphedemaRadiology2022Volume: 304Issue: 1pp. 218-224Photoacoustic Imaging Addresses a Long-standing Challenge in LymphedemaRadiology2020Volume: 295Issue: 2pp. 475-477Use of Pretreatment Breast MRI to Predict Failed Sentinel Lymph Node Identification after Neoadjuvant ChemotherapyRadiology2020Volume: 295Issue: 2pp. 283-284See More RSNA Education Exhibits Imaging of the Lymphatic System: Current Perspective with Multi-Modality Imaging and New HorizonDigital Posters2019Lymphangiography – Techniques and Uses in Clinical PracticeDigital Posters2020Secondary Lymphedema in Oncologic Patients: What Can Non-Contrast Magnetic Resonance Lymphangiography (NCMRL) Tell Us?Digital Posters2019 RSNA Case Collection "Cold" Sentinel Lymph Node in Cutaneous Melanoma RSNA Case Collection2020Tattoo pigment deposition in axillary lymph nodeRSNA Case Collection2020Diffuse pulmonary lymphangiomatosisRSNA Case Collection2020 Vol. 294, No. 1 Metrics Altmetric Score PDF download