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Lymphatic Imaging Techniques
Journal of Radiology Nursing xxx (2019) 1e8
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Lymphatic Imaging Techniques Natosha Monfore, DO a, Trevor Downing, MD b, Mamadou L. Sanogo, MD a, Nima Kokabi, MD c, Minhaj S. Khaja, MD, MBA a, Bill S. Majdalany, MD c,* a
Division of Vascular and Interventional Radiology, Department of Radiology, University of Michigan Health System, Ann Arbor, MI Division of Vascular and Interventional Radiology, Department of Radiology, Wake Forest Baptist Medical Center, Medical Center Boulevard, Winston-Salem, NC c Division of Vascular and Interventional Radiology, Department of Radiology and Imaging Sciences, Division of Vascular and Interventional Radiology, Emory University Hospital, Atlanta, GA b
a b s t r a c t Keywords: Lymphangiography Lymphoscintigraphy Magnetic resonance lymphangiography Thoracic duct Lymph nodes
The lymphatic system is a poorly understood and historically under-recognized component of the overall circulatory system. Lymphatic vessels have been difficult to study, given their small size relative to arteries and veins. Consequently, for centuries, little was known about the complex anatomy and physiology of the lymphatic system. Lymphatic pathophysiology and complications of lymphatic injury have underscored the importance of lymph nodes, lymphatic vasculature and their role in immune regulation, transportation of metabolites, and fluid balance. Innovation and refinement in advanced imaging has allowed for higher resolution imaging of the lymphatic circulation which in turn has led to improved understanding and targeted therapies. The imaging modalities that have permitted the evaluation, diagnosis, and treatment of lymphatic disorders are reviewed. © 2019 Association for Radiologic & Imaging Nursing. Published by Elsevier Inc. All rights reserved.
Introduction The existence of the lymphatic fluid and vessels has been suspected since the time of the ancient Greeks, but lymphatic anatomy and function remained a mystery until their discovery in the 1600s (Aalami et al., 2000). There has been substantial progress in medical science since the discovery of lymphatics which led to further understanding of many other body processes, pioneering imaging techniques, and innovative therapeutics to improve the outcomes of many diseases. However, progress in the understanding of lymphatic disorders has lagged. Until recently, treatment for lymphatic disorders consisted of supportive care or highly morbid surgeries resulting in suboptimal patient outcomes (Merigliano et al., 2000). A breakthrough in minimally invasive lymphatic therapy occurred in 1998 when Constantine Cope pioneered and refined percutaneous thoracic duct cannulation and embolization to treat chylothorax (Cope, 1998). In 2002, a case series of 42 patients was published with clinical success achieved in over 70% of patients All authors have read and contributed to this manuscript. The authors have no relevant disclosures. There was no grant funding or financial support for this manuscript. * Corresponding author: Bill S. Majdalany, Department of Radiology and Imaging Sciences, Emory University Hospital, 1364 Clifton Road NE, Suite AG05, Atlanta, GA 30322. Tel.: þ1-404-712-7115; Fax: þ1-404-686-2226. E-mail address: [email protected] (B.S. Majdalany).
(Cope and Kaiser, 2002). This has since become the standard of care for traumatic and high-output nontraumatic chylothorax (Majdalany et al., 2017). Thoracic duct embolization has also been applied for pediatric chylothorax and plastic bronchitis, a condition where patients expectorate plastic-like casts of their bronchial tree (Dori et al., 2016; Majdalany et al., 2018c). Continuously evolving and innovative techniques in lymphatic interventions have also been applied to the treatment of chylous ascites, lymphoceles, and protein-losing enteropathy (Itkin et al., 2017; Karcaaltincaba and Akhan, 2005; Majdalany et al., 2018a). In addition, although the long-term patency of endolymphatic thoracic duct stent grafts remains unknown, these have also been placed with clinical success for patients (Majdalany et al., 2018b). By applying these new approaches in lymphangiography and advances in magnetic resonance imaging (MRI) for lymphatic diseases, there is a renewed interest in the lymphatic circulation as a frontier in disease treatment. Herein, the anatomy and physiology of lymphatics are discussed, followed by a review of current imaging techniques. Anatomy and physiology Despite dramatic advances in medical knowledge, the lymphatic circulation remains mysterious and difficult to study. Gaspare Aselli of Cremona is credited with their discovery in the 1620s while performing vivisection of a dog (Aalami et al., 2000). Subsequent,
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Figure 1. 62-year-old patient's status after right lower lobectomy who has a persistent right pleural effusion. Thoracentesis resulted in turbid, opaque fluid with a triglyceride level of 692 mg/dL, which is typical of chyle.
separate studies by Pecquet, Bartholin, Rudbeck, Swammerdam, Ruysch, and others through the 1640s and onward contributed to the further understanding of lymphatic anatomy. This included identifying the cisterna chyli, the course of the thoracic duct and intestinal lymphatics, communications between the lymphatic and venous systems, and the existence of lymphatic valves (Natale et al., 2017). The 19th century was filled with knowledge gains centered around the physiology and pathophysiology of lymphatic fluid creation and flow. Ernest Starling described the relationship between the balancing roles of hydrostatic and oncotic pressure
Figure 2. A 62-year-old patient's status after right lower lobectomy who has a persistent right pleural effusion. Fluoroscopic image during lymphangiography reveals a rounded focus overlying a chest tube in the right thoracic cavity, which is a leak. The thoracic duct otherwise has a typical caliber and course, terminating as a single channel in the left venous angle (black arrowhead).
Figure 3. Digital subtraction lymphangiogram showing a variation of the thoracic duct (black arrowhead), which dilates in the upper chest (black arrow) and divides into multiple channels (white arrowheads).
resulting in the formation of lymphatic fluid as a form of diffusion across blood vessels. This was followed by an understanding of the interplay between lymph nodes, lymphatic vessels, and the
Figure 4. Digital subtraction lymphangiogram showing a variation in the termination of the thoracic duct (black arrowhead), which continues into the chest with a normal caliber before becoming plexiform in the midchest (black arrow) and then courses to the right venous angle where it terminates as a single channel.
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Figure 5. A 40-year-old female with bilateral leg swelling undergoing lymphoscintigraphy. Injection of radiotracer occurred at each foot, and imaging was performed at 5 minutes showing symmetric transit to each groin.
Figure 6. A 40-year-old female with bilateral leg swelling undergoing lymphoscintigraphy. At 90 minutes, the radiotracer has reached the termination of the thoracic duct (right arrowhead) and recirculated systemically with uptake in the liver. This is a normal examination.
realization that lymphatics return nutrient-rich fluid from tissues to the venous system (Taylor, 1981). Three subdivisions of the lymphatic circulation are recognized: soft tissue/extremity, hepatic, and enteral lymphatics. Approximately 80% of lymphatic fluid arises in equal parts from the hepatic and enteral lymphatics, which are rich in proteins and fats, respectively (Hsu and Itkin, 2016). The liver has both superficial and deep lymphatic vessels with a core function of returning liverderived proteins into the systemic circulation. While the superficial hepatic lymphatics drain to regional lymph nodes, the deep hepatic lymphatics drain along the portal vein in the hepatoduodenal ligament. The function of the enteral lymphatics is to absorb digested lipids and return them to the central circulation. Lymph fluid from the enteral lymphatic circulation is referred to as chyle and has an appearance similar to buttermilk (Figure 1). Soft tissue or extremity lymphatics make up the remaining 20% of the fluid which is nutrient poor but rich in lymphocytes and has the appearance of clear straw-colored fluid similar to simple ascites. The soft tissue lymphatics arise predominately from the periphery and include the axillary, inguinal, and iliac lymphatics. The inguinal lymphatics are inferior to the inguinal ligament and serve as a communication between the lower extremity, groin, genital
regions, and pelvis. The iliac lymphatics include the external and internal iliac chains and connect the lymphatics of the lower extremities to the abdomen (Hsu and Itkin, 2016). The lymphatics from each subdivision coalesce in the retroperitoneum to form a dilated sac-like structure, the cisterna chyli, which is in the retrocrural space to the right of the abdominal aorta. The cisterna chyli then gives rise to the thoracic duct at approximately L1 (Ross, 1961). The thoracic duct is the largest lymphatic vessel in the body, measuring between 2 and 6 mm in width and approximately 4050 cm in length (Figure 2). The thoracic duct is located in the posterior mediastinum between the aorta and azygos vein, posterior to the esophagus and overlying the spine (Ross, 1961). As it ascends in the chest, it most commonly crosses from right to left across midline between T5-7 and ends at the junction of the left internal jugular and subclavian veins. Two long flap-like cusps extend obliquely from the vein to create an ostial valve at the termination of the thoracic duct. This functions to prevent the reflux of blood into the duct which can be thrombogenic and obstruct the flow of lymphatic fluid. Anatomical variability is common in the lymphatic circulation and only 50% of the population exhibit the standard anatomy (Figures 3 and 4) (Van Pernis,
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Figure 7. A 45-year-old male with left leg swelling undergoing lymphoscintigraphy. Injection of radiotracer was performed in each foot, and isolated lymphatic vessels are seen in the right lower extremity (white arrow) but not the left.
1949). All lymphatic fluid flows through the thoracic duct with the exception of lymphatic fluid from the right head, neck, thorax, and upper extremity, which drain through minor right-sided ducts.
Figure 8. A 45-year-old male with left leg swelling undergoing lymphoscintigraphy. At 5 hours, the radiotracer in the right leg has reached the right groin (white arrow) and the thoracic duct terminus (white arrowhead). In the left leg, the radiotracer remains in the lower leg with dermal uptake, pathognomonic for lymphedema.
are those that are the first visualized lymph nodes draining in the vicinity of the radiotracer injection site (Figure 9). The radiotracer can be detected with a modified Geiger counter during surgery to
Lymphoscintigraphy Lymphoscintigraphy was first introduced in 1953 and can be used to evaluate lymphedema or more commonly to isolate sentinel lymph nodes in patients with breast cancer or melanoma (Sherman and Ter-Pogossian, 1953). This technique involves the interstitial injection of radiopharmaceuticals and is a study performed in nuclear medicine. Generally, it is a simple and noninvasive examination which involves injecting a radiotracer into the hand or foot for lymphedema or retroareolar or periareolar in the setting of breast cancer. The flow of particles is then imaged with a gamma camera while the tracer migrates into the lymphatic circulation. Lymphatic dysfunction on lymphoscintigraphy is defined by delayed, asymmetric, or absent visualization of regional lymph nodes, asymmetric visualization of lymphatic channels, or dermal backflow (Figures 5-8) (Moshiri et al., 2002). Sentinel lymph nodes
Figure 9. A 52-year-old female undergoing sentinel lymph node mapping for melanoma. Radiotracer was injected around the known malignancy (white arrowhead) and two draining lymph nodes (white arrows) were identified for surgical excision.
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Figure 10. Fluoroscopy of pedal lymphangiography. A 30-gauge needle (black arrowhead) was used to cannulate a dorsal foot lymphatic after a cutdown on the dorsum of the foot. A subsequent slow injection of contrast reveals a normal appearing lymphatic vessel (black arrow), which is ascending from the foot.
guide lymphadenectomy as these lymph nodes would be the most likely to reflect regional cancer spread. Lymphoscintigraphy can be used as a screening tool for disorders of central and peripheral lymphatic systems by demonstrating regions of abnormal
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Figure 12. Spot radiograph of the thigh reveals multiple lymphatic vessels coursing cephalad together (arrowheads) and coalescing into groin lymph nodes.
lymphatic perfusion and provide lymphatic flow information. Unfortunately, the spatial resolution is poor, thus limiting its use in procedural planning and treatment of lymphatic dysfunction (Yoshida et al., 2016). Newer techniques incorporating crosssectional imaging and single-photon emission computed tomography (CT) may improve sensitivity and localization of lymphatic leaks and lymph nodes (Valdes-Olmos et al., 2014). Conventional lymphangiography Conventional lymphangiography is the technique of injecting contrast dye directly into the lymphatic system with concomitant radiography. Historically, Fischer tested different contrast agents in
Figure 11. Spot radiograph of the lower leg reveals multiple lace-like lymphatic vessels (black arrowheads) coursing cephalad.
Figure 13. Spot radiograph of the pelvis reveals lymphatic vessels (black arrowheads) interspersed with lymph nodes (black arrows) as they course along and around the iliac vasculature.
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Figure 14. An ultrasonographic image of an inguinal lymph node (between white arrowheads) with a 25-gauge needle (white arrow) coursing through it in preparation for nodal lymphangiography.
the lymphatic system including ethiodized oil, which is the current contrast agent of choice (Fischer and Zimmerman, 1959). The injection of ethiodized oil can be performed either through a pedal or nodal approach. The initial technique of pedal lymphangiography was described in 1955 by Kinmoth et al., who used it to study the lower extremity lymphatics. To begin the procedure, methylene blue dye was injected into the web spaces of the toes and massaged until the dye filled lymphatic vessels (Kinmoth et al., 1955). Next, Kinmoth described surgical exposure and isolation of the small lymphatic vessels in the dorsum of the foot. The vessels were then cannulated with a small catheter and ethiodized oil was slowly injected. Serial spot radiographs were obtained as contrast flowed up the legs, into the pelvis, and eventually to the retroperitoneal and central lymphatics (Figures 10-13). For decades, this technique was used for lymphoma diagnosis and staging, differentiation of inflammatory and neoplastic processes, detection of metastatic disease, and determination of chemotherapy response. Although this technique provides highresolution images and potential therapeutic benefit, it is challenging to cannulate the dorsal foot lymphatics. In addition, this is a time-consuming study often taking several hours to follow the contrast from the feet to the abdomen. This relatively involved examination was ultimately supplanted as a diagnostic test by ultrasound (US), CT, and MRI. The utility of lymphangiography has not been discounted with the improvement of diagnostic modalities. The potential applications of lymphangiography to guide lymphatic interventions
Figure 15. Fluoroscopic image of nodal lymphangiography with a 25-gauge needle (black arrowhead) positioned within a lymph node. Initial injection of contrast material reveals the typical arborizing appearance of lymphatic vessels (black arrow).
Figure 16. Fluoroscopic image of nodal lymphangiography. The arborizing lymphatic vessels which were seen in Figure 15 (black arrow) had transmitted the contrast through a second lymph node and subsequently have continued to opacify additional lymphatic vessels (black arrowheads) in the inguinal region.
spurred the advent of nodal lymphangiography, first described in 2011 (Rajebi et al., 2011). Rather than cannulating a lymphatic vessel in the dorsum of the foot, US can be used to target a lymph node (most often inguinal) with a 25- to 30-gauge needle. With the needle positioned within the hilum of a lymph node, a steady and slow injection of ethiodized oil is performed, allowing for transmission of the contrast further into the lymphatic system (Figures 14-16). Serial spot radiographs are then used to image the flow of contrast from the inguinal nodes, through the pelvis, and into the retroperitoneal lymphatics. Intranodal lymphangiography is less complicated and cumbersome than pedal lymphangiography. By beginning the process in the inguinal lymphatics, there is a substantial reduction in overall procedural time. Typically, intranodal lymphangiography carries a higher success rate and is more readily available to lessexperienced practitioners or those with intraprocedural time constraints. The addition of sequential compression devices placed on
Figure 17. Hepatic lymphangiogram. A 22-gauge needle (black arrow) was slowly withdrawn from the liver while simultaneously injecting contrast. Multiple lace-like lymphatic vessels are opacified (black arrowheads), which coalesce in the hepatic hilum into larger vessels and eventually course through the hepatoduodenal ligament.
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Figure 18. Coronal noncontrast MRI image of a heavily T2-weighted sequence with fat saturation reveals the thoracic duct (white arrow) right of the midline and adjacent to the abdominal aorta, in the expected location. MRI ¼ magnetic resonance imaging.
the legs can further increase the rate of transmission of ethiodized oil into the central lymphatics (Meisinger et al., 2017). Conventional pedal or nodal lymphangiography can image the peripheral and retroperitoneal lymphatics and has led to the advent of previously discussed therapies. To identify and treat other lymphatic disorders, a technique to visualize hepatic and mesenteric lymphatics is necessary. Hepatic lymphangiography dates to initial experiences in percutaneous cholangiography. Okuda et al. noted that they could incidentally visualize hepatic lymphatics in a minority of cases (Okuda et al., 1976). Cope was able to visualize a larger proportion of these after refining the technique (Cope, 2003). Simply, a 21- to 22-gauge needle is directed transhepatically from inferolaterally to superomedially and is angled toward the porta hepatis. While slowly withdrawing the needle, contrast is simultaneously injected. Using this technique, the deep hepatic lymphatics can be visualized and studied as they exit the liver and enter the hepatoduodenal ligament (Figure 17). Most recently, this technique has been applied to protein-losing enteropathy and was shown to be successful in identifying the leakage of protein-rich lymph into the intestinal lumen before performing embolization therapy of the leaking lymphatics (Itkin et al., 2017). Robust
Figure 19. Axial noncontrast MRI image of a heavily T2-weighted sequence with fat saturation reveals the thoracic duct (white arrow) right of midline an adjacent to the abdominal aorta, in the expected location. MRI ¼ magnetic resonance imaging.
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Figure 20. Coronal dynamic contrast-enhanced MRI image of a newborn with congenital chylous ascites. Dilute gadolinium contrast was injected through nodal lymphangiography in each groin (*), and sequential images were repeated acquired after the ascension of contrast through the retroperitoneal lymphatics (white arrowheads) to the termination of the thoracic duct (white arrow), consistent with a normal examination. MRI ¼ magnetic resonance imaging.
reproducible techniques to perform mesenteric lymphangiography without surgical exposure remain to be described. Noncontrast and dynamic contrast magnetic resonance lymphangiography Of the cross-sectional imaging modalities, MRI is inherently superior to CT at differentiating soft tissue and fluid characteristics. CT is generally not useful in the study of lymphatic disorders, whereas magnetic resonance lymphangiography (MRL) has been used to study lymphatic disorders since the late 1990s and can be performed with or without contrast. Using T2 fat-saturation sequences, slow moving or stagnant nonbloody fluid-filled structures appear bright, whereas most other structures will appear dark (Hayashi and Miyazaki, 1999). Visualization of larger central lymphatic structures, dilated lymphatic collections, or diffuse subcutaneous edema is possible with this technique, which is best suited to patients with lymphedema or lymphatic malformations (Figures 18 and 19) (Laor et al., 1998). However, in the absence of contrast, visualization of smaller lymphatic vessels is limited as MRL does not provide information on lymphatic flow physiology. The injection of contrast into the lymphatic system allows for dynamic contrast-enhanced MRL, providing insight into the pathophysiology of lymphatic flow and allowing for more consistent imaging as a precursor to planned procedures. The initial approach was intradermal injection of gadolinium-based contrast in the feet, which is readily absorbed into the lymph nodes and vessels (Ruehm et al., 2001). Although this technique allows for the delineation of peripheral lymphatic abnormalities, the injected contrast becomes more dilute as it flows centrally, thus limiting evaluation of the central lymphatics. To improve the evaluation of central lymphatics and decrease the dilutional effects of the contrast, intranodal injection of gadolinium-based contrast is now more commonly performed (Figure 20) (Krishnamurthy et al., 2016). Dynamic contrast-enhanced MRL is particularly useful to delineate abnormalities in patients with nontraumatic chylothorax,
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complicated traumatic chylous leaks, plastic bronchitis, congenital lymphatic flow disorders, and suspected secondary lymphatic flow abnormalities. Moreover, MRL excels at evaluating the anatomy of the central lymphatic system before surgery, is more sensitive than conventional lymphangiography in detecting lymphatic leaks, and can assist in procedural planning for lymphatic interventions. Future directions Dynamic contrast MRL, conventional lymphangiography, and lymphoscintigraphy are minimally invasive and allow for the evaluation of extremity and retroperitoneal lymphatics. However, without the direct injection of the liver or enteral lymphatics, there are no other ways to visualize this portion of the lymphatic circulation. The development of imaging techniques and contrast agents for the evaluation of liver and intestinal lymphatics is underway and could provide further insight into disease processes such as chylous ascites, ascitic fluid formation in hepatic cirrhosis, heart failure, and congenital lymphatic disorders. Moreover, as the production and distribution of lymph is better understood in each distinct lymphatic circulation and in various organs, it could provide targets for intervention previously unrealized. Conclusion The recent evolution and advanced knowledge in lymphatic imaging have contributed to the understanding of lymphatic anatomy, physiology, and multiple disease processes allowing for successful diagnosis and lymphatic intervention in a growing number of patients. References Aalami, O.O., Allen, D.B., & Organ, C.H., Jr. (2000). Chylous ascites: a collective review. Surgery, 128(5), 761-778. Cope, C. (1998). Diagnosis and treatment of postoperative chyle leakage via percutaneous transabdominal catheterization of the cisterna chyli: a preliminary study. Journal of Vascular and Interventional Radiology, 9, 727-734. Cope, C. (2003). Usefulness of a percutaneous transhepatic coaxial micropuncture needle technique in patients with nondilated peripheral intrahepatic ducts. American Journal of Roentgenology, 181, 1017-1020. Cope, C., & Kaiser, L.R. (2002). Management of unremitting chylothorax by percutaneous embolization and blockage of retroperitoneal lymphatic vessels in 42 patients. Journal of Vascular and Interventional Radiology, 13, 1139-1148. Dori, Y., Keller, M.S., Rome, J.J., Gillespie, M.J., Glatz, A.C., Dodds, K., et al. (2016). Percutaneous lymphatic embolization of abnormal pulmonary lymphatic flow as treatment of plastic bronchitis in patients with congenital heart disease. Circulation, 133, 1160-1170. Fischer, H.W., & Zimmerman, G.R. (1959). Roentgenographic visualization of lymph nodes and lymphatic channels. American Journal of Roentgenology, 81, 517-534. Hayashi, S., & Miyazaki, M. (1999). Thoracic duct: Visualization at nonenhanced MR lymphographydinitial experience. Radiology, 212, 598-600.
Hsu, M.C., & Itkin, M. (2016). Lymphatic anatomy. Techniques in Vascular and Interventional Radiology, 10(3), 247-254. Itkin, M., Piccoli, D.A., Nadolski, G., Rychik, J., DeWitt, A., Pinto, E., et al. (2017). Protein-losing enteropathy in patients with congenital heart disease. Journal of the American College of Cardiology, 69(24), 2929-2937. Karcaaltincaba, M., & Akhan, O. (2005). Radiologic imaging and percutaneous treatment of pelvic lymphocele. European Journal of Radiology, 55, 340-354. Kinmonth, J.B., Taylor, G.W., & Harper, R.A.K. (1955). Lymphangiography: a technique for its clinical use in the lower limb. British Medical Journal, 1, 940-942. Krishnamurthy, R., Hernandez, A., Kavuk, S., Annam, A., & Pimpalwar, S. (2015). Imaging the central conducting lymphatics: initial experience with dynamic MR lymphangiography. Radiology, 274, 871-878. Laor, T., Hoffer, F.A., Burrows, P.E., & Kozakewich, H.P. (1998). MR lymphangiography in infants, children, and young adults. American Journal of Roentgenology, 171, 1111-1117. Majdalany, B.S., Murrey, D.A., Jr., Kapoor, B.S., Cain, T.R., Ganguli, S., Kent, M.S., et al. (2017). ACR appropriateness criteria: chylothorax treatment planning. Journal of the American College of Radiology, 14(5S), S118-S126. Majdalany, B.S., Khayat, M., Downing, T., Killoran, T.P., El-Haddad, G., Khaja, M.S., et al. (2018a). Lymphatic interventions for isolated, iatrogenic chylous ascites: a multi-institution experience. European Journal of Radiology, 109, 41-47. Majdalany, B.S., Khayat, M., Sanogo, M.L., Saad, W.E., & Khaja, M.S. (2018b). Direct trans-cervical endolymphatic thoracic duct stent-graft for plastic bronchitis. Lymphology, 51(3), 97-101. Majdalany, B.S., Saad, W.A., Chick, J.F.B., Khaja, M.S., Cooper, K.J., & Srinivasa, R.N. (2018c). Pediatric lymphangiography, thoracic duct embolization, and thoracic duct disruption: a single institution experience in 11 patients with chylothorax. Pediatric Radiology, 48(2), 235-240. Meisinger, Q.C., O’Brien, S., Itkin, M., & Nadolski, G.J. (2017). Use of sequential pneumatic compression devices to facilitate propagation of contrast during intranodal lymphangiography. Journal of Vascular and Interventional Radiology, 28, 1544-1547. Merigliano, S., Molena, D., Ruol, A., Zaninotto, G., Cagol, M., Scappin, S., & Ancona, E. (2000). Chylothorax complicating esophagectomy for cancer: a plea for early thoracic duct ligation. The Journal of Thoracic and Cardiovascular Surgery, 119(3), 453-457. Moshiri, M., Katz, D.S., Boris, M., & Yung, E. (2002). Using lymphoscintigraphy to evaluate suspected lymphedema of the extremities. American Journal of Roentgenology, 178(2), 405-412. Natale, G., Bocci, G., & Ribatti, D. (2017). Scholars and scientists in the history of the lymphatic system. Journal of Anatomy, 231, 417-429. Okuda, K., Sumikoshi, T., Kanda, Y., Fukuyama, Y., & Koen, H. (1976). Hepatic lymphatics as opacified by percutaneous intrahepatic injection of contrast medium: analysis of hepatic lymphangiograms in 125 cases. Radiology, 120, 321-326. Rajebi, M.R., Chaudry, G., Padua, H.M., et al. (2011). Intranodal Lymphangiography: feasibility and preliminary experience in children. Journal of Vascular and Interventional Radiology, 22(9), 1300-1305. Ross, J.K. (1961). A review of the surgery of the thoracic duct. Thorax, 16, 12-21. Ruehm, S.G., Schroeder, T., & Debatin, J.F. (2001). Interstitial MR lymphography with gadoterate meglumine: initial experience in humans. Radiology, 220(3), 816821. Sherman, A., & Ter-Pogossian, M. (1953). Lymph node concentration of radioactive colloidal gold following interstitial injection. Cancer, 6, 1238-1240. Taylor, A.E. (1981). Capillary fluid filtration: startling forces and lymph flow. Circ Res, 49, 557-575. Valdes-Olmos, R.A., Rietbergen, D.D.D., & Vidal-Sicart, S. (2014). SPECT/CT and sentinel node lymphoscintigraphy. Clinical and Translational Imaging, 2, 491504. Van Pernis, P.A. (1949). Variations of the thoracic duct. Surgery, 26, 806-809. Yoshida, R.Y., Kariya, S., Ha-Kawa, S., & Tanigawa, N. (2016). Lymphoscintigraphy for imaging of the lymphatic flow disorders. Techniques in Vascular and Interventional Radiology, 19(4), 273-276.
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Lymphatic Imaging Techniques Natosha Monfore, DO a, Trevor Downing, MD b, Mamadou L. Sanogo, MD a, Nima Kokabi, MD c, Minhaj S. Khaja, MD, MBA a, Bill S. Majdalany, MD c,* a
Division of Vascular and Interventional Radiology, Department of Radiology, University of Michigan Health System, Ann Arbor, MI Division of Vascular and Interventional Radiology, Department of Radiology, Wake Forest Baptist Medical Center, Medical Center Boulevard, Winston-Salem, NC c Division of Vascular and Interventional Radiology, Department of Radiology and Imaging Sciences, Division of Vascular and Interventional Radiology, Emory University Hospital, Atlanta, GA b
a b s t r a c t Keywords: Lymphangiography Lymphoscintigraphy Magnetic resonance lymphangiography Thoracic duct Lymph nodes
The lymphatic system is a poorly understood and historically under-recognized component of the overall circulatory system. Lymphatic vessels have been difficult to study, given their small size relative to arteries and veins. Consequently, for centuries, little was known about the complex anatomy and physiology of the lymphatic system. Lymphatic pathophysiology and complications of lymphatic injury have underscored the importance of lymph nodes, lymphatic vasculature and their role in immune regulation, transportation of metabolites, and fluid balance. Innovation and refinement in advanced imaging has allowed for higher resolution imaging of the lymphatic circulation which in turn has led to improved understanding and targeted therapies. The imaging modalities that have permitted the evaluation, diagnosis, and treatment of lymphatic disorders are reviewed. © 2019 Association for Radiologic & Imaging Nursing. Published by Elsevier Inc. All rights reserved.
Introduction The existence of the lymphatic fluid and vessels has been suspected since the time of the ancient Greeks, but lymphatic anatomy and function remained a mystery until their discovery in the 1600s (Aalami et al., 2000). There has been substantial progress in medical science since the discovery of lymphatics which led to further understanding of many other body processes, pioneering imaging techniques, and innovative therapeutics to improve the outcomes of many diseases. However, progress in the understanding of lymphatic disorders has lagged. Until recently, treatment for lymphatic disorders consisted of supportive care or highly morbid surgeries resulting in suboptimal patient outcomes (Merigliano et al., 2000). A breakthrough in minimally invasive lymphatic therapy occurred in 1998 when Constantine Cope pioneered and refined percutaneous thoracic duct cannulation and embolization to treat chylothorax (Cope, 1998). In 2002, a case series of 42 patients was published with clinical success achieved in over 70% of patients All authors have read and contributed to this manuscript. The authors have no relevant disclosures. There was no grant funding or financial support for this manuscript. * Corresponding author: Bill S. Majdalany, Department of Radiology and Imaging Sciences, Emory University Hospital, 1364 Clifton Road NE, Suite AG05, Atlanta, GA 30322. Tel.: þ1-404-712-7115; Fax: þ1-404-686-2226. E-mail address: [email protected] (B.S. Majdalany).
(Cope and Kaiser, 2002). This has since become the standard of care for traumatic and high-output nontraumatic chylothorax (Majdalany et al., 2017). Thoracic duct embolization has also been applied for pediatric chylothorax and plastic bronchitis, a condition where patients expectorate plastic-like casts of their bronchial tree (Dori et al., 2016; Majdalany et al., 2018c). Continuously evolving and innovative techniques in lymphatic interventions have also been applied to the treatment of chylous ascites, lymphoceles, and protein-losing enteropathy (Itkin et al., 2017; Karcaaltincaba and Akhan, 2005; Majdalany et al., 2018a). In addition, although the long-term patency of endolymphatic thoracic duct stent grafts remains unknown, these have also been placed with clinical success for patients (Majdalany et al., 2018b). By applying these new approaches in lymphangiography and advances in magnetic resonance imaging (MRI) for lymphatic diseases, there is a renewed interest in the lymphatic circulation as a frontier in disease treatment. Herein, the anatomy and physiology of lymphatics are discussed, followed by a review of current imaging techniques. Anatomy and physiology Despite dramatic advances in medical knowledge, the lymphatic circulation remains mysterious and difficult to study. Gaspare Aselli of Cremona is credited with their discovery in the 1620s while performing vivisection of a dog (Aalami et al., 2000). Subsequent,
https://doi.org/10.1016/j.jradnu.2019.07.010 1546-0843/$36.00/© 2019 Association for Radiologic & Imaging Nursing. Published by Elsevier Inc. All rights reserved.
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Figure 1. 62-year-old patient's status after right lower lobectomy who has a persistent right pleural effusion. Thoracentesis resulted in turbid, opaque fluid with a triglyceride level of 692 mg/dL, which is typical of chyle.
separate studies by Pecquet, Bartholin, Rudbeck, Swammerdam, Ruysch, and others through the 1640s and onward contributed to the further understanding of lymphatic anatomy. This included identifying the cisterna chyli, the course of the thoracic duct and intestinal lymphatics, communications between the lymphatic and venous systems, and the existence of lymphatic valves (Natale et al., 2017). The 19th century was filled with knowledge gains centered around the physiology and pathophysiology of lymphatic fluid creation and flow. Ernest Starling described the relationship between the balancing roles of hydrostatic and oncotic pressure
Figure 2. A 62-year-old patient's status after right lower lobectomy who has a persistent right pleural effusion. Fluoroscopic image during lymphangiography reveals a rounded focus overlying a chest tube in the right thoracic cavity, which is a leak. The thoracic duct otherwise has a typical caliber and course, terminating as a single channel in the left venous angle (black arrowhead).
Figure 3. Digital subtraction lymphangiogram showing a variation of the thoracic duct (black arrowhead), which dilates in the upper chest (black arrow) and divides into multiple channels (white arrowheads).
resulting in the formation of lymphatic fluid as a form of diffusion across blood vessels. This was followed by an understanding of the interplay between lymph nodes, lymphatic vessels, and the
Figure 4. Digital subtraction lymphangiogram showing a variation in the termination of the thoracic duct (black arrowhead), which continues into the chest with a normal caliber before becoming plexiform in the midchest (black arrow) and then courses to the right venous angle where it terminates as a single channel.
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Figure 5. A 40-year-old female with bilateral leg swelling undergoing lymphoscintigraphy. Injection of radiotracer occurred at each foot, and imaging was performed at 5 minutes showing symmetric transit to each groin.
Figure 6. A 40-year-old female with bilateral leg swelling undergoing lymphoscintigraphy. At 90 minutes, the radiotracer has reached the termination of the thoracic duct (right arrowhead) and recirculated systemically with uptake in the liver. This is a normal examination.
realization that lymphatics return nutrient-rich fluid from tissues to the venous system (Taylor, 1981). Three subdivisions of the lymphatic circulation are recognized: soft tissue/extremity, hepatic, and enteral lymphatics. Approximately 80% of lymphatic fluid arises in equal parts from the hepatic and enteral lymphatics, which are rich in proteins and fats, respectively (Hsu and Itkin, 2016). The liver has both superficial and deep lymphatic vessels with a core function of returning liverderived proteins into the systemic circulation. While the superficial hepatic lymphatics drain to regional lymph nodes, the deep hepatic lymphatics drain along the portal vein in the hepatoduodenal ligament. The function of the enteral lymphatics is to absorb digested lipids and return them to the central circulation. Lymph fluid from the enteral lymphatic circulation is referred to as chyle and has an appearance similar to buttermilk (Figure 1). Soft tissue or extremity lymphatics make up the remaining 20% of the fluid which is nutrient poor but rich in lymphocytes and has the appearance of clear straw-colored fluid similar to simple ascites. The soft tissue lymphatics arise predominately from the periphery and include the axillary, inguinal, and iliac lymphatics. The inguinal lymphatics are inferior to the inguinal ligament and serve as a communication between the lower extremity, groin, genital
regions, and pelvis. The iliac lymphatics include the external and internal iliac chains and connect the lymphatics of the lower extremities to the abdomen (Hsu and Itkin, 2016). The lymphatics from each subdivision coalesce in the retroperitoneum to form a dilated sac-like structure, the cisterna chyli, which is in the retrocrural space to the right of the abdominal aorta. The cisterna chyli then gives rise to the thoracic duct at approximately L1 (Ross, 1961). The thoracic duct is the largest lymphatic vessel in the body, measuring between 2 and 6 mm in width and approximately 4050 cm in length (Figure 2). The thoracic duct is located in the posterior mediastinum between the aorta and azygos vein, posterior to the esophagus and overlying the spine (Ross, 1961). As it ascends in the chest, it most commonly crosses from right to left across midline between T5-7 and ends at the junction of the left internal jugular and subclavian veins. Two long flap-like cusps extend obliquely from the vein to create an ostial valve at the termination of the thoracic duct. This functions to prevent the reflux of blood into the duct which can be thrombogenic and obstruct the flow of lymphatic fluid. Anatomical variability is common in the lymphatic circulation and only 50% of the population exhibit the standard anatomy (Figures 3 and 4) (Van Pernis,
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Figure 7. A 45-year-old male with left leg swelling undergoing lymphoscintigraphy. Injection of radiotracer was performed in each foot, and isolated lymphatic vessels are seen in the right lower extremity (white arrow) but not the left.
1949). All lymphatic fluid flows through the thoracic duct with the exception of lymphatic fluid from the right head, neck, thorax, and upper extremity, which drain through minor right-sided ducts.
Figure 8. A 45-year-old male with left leg swelling undergoing lymphoscintigraphy. At 5 hours, the radiotracer in the right leg has reached the right groin (white arrow) and the thoracic duct terminus (white arrowhead). In the left leg, the radiotracer remains in the lower leg with dermal uptake, pathognomonic for lymphedema.
are those that are the first visualized lymph nodes draining in the vicinity of the radiotracer injection site (Figure 9). The radiotracer can be detected with a modified Geiger counter during surgery to
Lymphoscintigraphy Lymphoscintigraphy was first introduced in 1953 and can be used to evaluate lymphedema or more commonly to isolate sentinel lymph nodes in patients with breast cancer or melanoma (Sherman and Ter-Pogossian, 1953). This technique involves the interstitial injection of radiopharmaceuticals and is a study performed in nuclear medicine. Generally, it is a simple and noninvasive examination which involves injecting a radiotracer into the hand or foot for lymphedema or retroareolar or periareolar in the setting of breast cancer. The flow of particles is then imaged with a gamma camera while the tracer migrates into the lymphatic circulation. Lymphatic dysfunction on lymphoscintigraphy is defined by delayed, asymmetric, or absent visualization of regional lymph nodes, asymmetric visualization of lymphatic channels, or dermal backflow (Figures 5-8) (Moshiri et al., 2002). Sentinel lymph nodes
Figure 9. A 52-year-old female undergoing sentinel lymph node mapping for melanoma. Radiotracer was injected around the known malignancy (white arrowhead) and two draining lymph nodes (white arrows) were identified for surgical excision.
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Figure 10. Fluoroscopy of pedal lymphangiography. A 30-gauge needle (black arrowhead) was used to cannulate a dorsal foot lymphatic after a cutdown on the dorsum of the foot. A subsequent slow injection of contrast reveals a normal appearing lymphatic vessel (black arrow), which is ascending from the foot.
guide lymphadenectomy as these lymph nodes would be the most likely to reflect regional cancer spread. Lymphoscintigraphy can be used as a screening tool for disorders of central and peripheral lymphatic systems by demonstrating regions of abnormal
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Figure 12. Spot radiograph of the thigh reveals multiple lymphatic vessels coursing cephalad together (arrowheads) and coalescing into groin lymph nodes.
lymphatic perfusion and provide lymphatic flow information. Unfortunately, the spatial resolution is poor, thus limiting its use in procedural planning and treatment of lymphatic dysfunction (Yoshida et al., 2016). Newer techniques incorporating crosssectional imaging and single-photon emission computed tomography (CT) may improve sensitivity and localization of lymphatic leaks and lymph nodes (Valdes-Olmos et al., 2014). Conventional lymphangiography Conventional lymphangiography is the technique of injecting contrast dye directly into the lymphatic system with concomitant radiography. Historically, Fischer tested different contrast agents in
Figure 11. Spot radiograph of the lower leg reveals multiple lace-like lymphatic vessels (black arrowheads) coursing cephalad.
Figure 13. Spot radiograph of the pelvis reveals lymphatic vessels (black arrowheads) interspersed with lymph nodes (black arrows) as they course along and around the iliac vasculature.
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Figure 14. An ultrasonographic image of an inguinal lymph node (between white arrowheads) with a 25-gauge needle (white arrow) coursing through it in preparation for nodal lymphangiography.
the lymphatic system including ethiodized oil, which is the current contrast agent of choice (Fischer and Zimmerman, 1959). The injection of ethiodized oil can be performed either through a pedal or nodal approach. The initial technique of pedal lymphangiography was described in 1955 by Kinmoth et al., who used it to study the lower extremity lymphatics. To begin the procedure, methylene blue dye was injected into the web spaces of the toes and massaged until the dye filled lymphatic vessels (Kinmoth et al., 1955). Next, Kinmoth described surgical exposure and isolation of the small lymphatic vessels in the dorsum of the foot. The vessels were then cannulated with a small catheter and ethiodized oil was slowly injected. Serial spot radiographs were obtained as contrast flowed up the legs, into the pelvis, and eventually to the retroperitoneal and central lymphatics (Figures 10-13). For decades, this technique was used for lymphoma diagnosis and staging, differentiation of inflammatory and neoplastic processes, detection of metastatic disease, and determination of chemotherapy response. Although this technique provides highresolution images and potential therapeutic benefit, it is challenging to cannulate the dorsal foot lymphatics. In addition, this is a time-consuming study often taking several hours to follow the contrast from the feet to the abdomen. This relatively involved examination was ultimately supplanted as a diagnostic test by ultrasound (US), CT, and MRI. The utility of lymphangiography has not been discounted with the improvement of diagnostic modalities. The potential applications of lymphangiography to guide lymphatic interventions
Figure 15. Fluoroscopic image of nodal lymphangiography with a 25-gauge needle (black arrowhead) positioned within a lymph node. Initial injection of contrast material reveals the typical arborizing appearance of lymphatic vessels (black arrow).
Figure 16. Fluoroscopic image of nodal lymphangiography. The arborizing lymphatic vessels which were seen in Figure 15 (black arrow) had transmitted the contrast through a second lymph node and subsequently have continued to opacify additional lymphatic vessels (black arrowheads) in the inguinal region.
spurred the advent of nodal lymphangiography, first described in 2011 (Rajebi et al., 2011). Rather than cannulating a lymphatic vessel in the dorsum of the foot, US can be used to target a lymph node (most often inguinal) with a 25- to 30-gauge needle. With the needle positioned within the hilum of a lymph node, a steady and slow injection of ethiodized oil is performed, allowing for transmission of the contrast further into the lymphatic system (Figures 14-16). Serial spot radiographs are then used to image the flow of contrast from the inguinal nodes, through the pelvis, and into the retroperitoneal lymphatics. Intranodal lymphangiography is less complicated and cumbersome than pedal lymphangiography. By beginning the process in the inguinal lymphatics, there is a substantial reduction in overall procedural time. Typically, intranodal lymphangiography carries a higher success rate and is more readily available to lessexperienced practitioners or those with intraprocedural time constraints. The addition of sequential compression devices placed on
Figure 17. Hepatic lymphangiogram. A 22-gauge needle (black arrow) was slowly withdrawn from the liver while simultaneously injecting contrast. Multiple lace-like lymphatic vessels are opacified (black arrowheads), which coalesce in the hepatic hilum into larger vessels and eventually course through the hepatoduodenal ligament.
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Figure 18. Coronal noncontrast MRI image of a heavily T2-weighted sequence with fat saturation reveals the thoracic duct (white arrow) right of the midline and adjacent to the abdominal aorta, in the expected location. MRI ¼ magnetic resonance imaging.
the legs can further increase the rate of transmission of ethiodized oil into the central lymphatics (Meisinger et al., 2017). Conventional pedal or nodal lymphangiography can image the peripheral and retroperitoneal lymphatics and has led to the advent of previously discussed therapies. To identify and treat other lymphatic disorders, a technique to visualize hepatic and mesenteric lymphatics is necessary. Hepatic lymphangiography dates to initial experiences in percutaneous cholangiography. Okuda et al. noted that they could incidentally visualize hepatic lymphatics in a minority of cases (Okuda et al., 1976). Cope was able to visualize a larger proportion of these after refining the technique (Cope, 2003). Simply, a 21- to 22-gauge needle is directed transhepatically from inferolaterally to superomedially and is angled toward the porta hepatis. While slowly withdrawing the needle, contrast is simultaneously injected. Using this technique, the deep hepatic lymphatics can be visualized and studied as they exit the liver and enter the hepatoduodenal ligament (Figure 17). Most recently, this technique has been applied to protein-losing enteropathy and was shown to be successful in identifying the leakage of protein-rich lymph into the intestinal lumen before performing embolization therapy of the leaking lymphatics (Itkin et al., 2017). Robust
Figure 19. Axial noncontrast MRI image of a heavily T2-weighted sequence with fat saturation reveals the thoracic duct (white arrow) right of midline an adjacent to the abdominal aorta, in the expected location. MRI ¼ magnetic resonance imaging.
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Figure 20. Coronal dynamic contrast-enhanced MRI image of a newborn with congenital chylous ascites. Dilute gadolinium contrast was injected through nodal lymphangiography in each groin (*), and sequential images were repeated acquired after the ascension of contrast through the retroperitoneal lymphatics (white arrowheads) to the termination of the thoracic duct (white arrow), consistent with a normal examination. MRI ¼ magnetic resonance imaging.
reproducible techniques to perform mesenteric lymphangiography without surgical exposure remain to be described. Noncontrast and dynamic contrast magnetic resonance lymphangiography Of the cross-sectional imaging modalities, MRI is inherently superior to CT at differentiating soft tissue and fluid characteristics. CT is generally not useful in the study of lymphatic disorders, whereas magnetic resonance lymphangiography (MRL) has been used to study lymphatic disorders since the late 1990s and can be performed with or without contrast. Using T2 fat-saturation sequences, slow moving or stagnant nonbloody fluid-filled structures appear bright, whereas most other structures will appear dark (Hayashi and Miyazaki, 1999). Visualization of larger central lymphatic structures, dilated lymphatic collections, or diffuse subcutaneous edema is possible with this technique, which is best suited to patients with lymphedema or lymphatic malformations (Figures 18 and 19) (Laor et al., 1998). However, in the absence of contrast, visualization of smaller lymphatic vessels is limited as MRL does not provide information on lymphatic flow physiology. The injection of contrast into the lymphatic system allows for dynamic contrast-enhanced MRL, providing insight into the pathophysiology of lymphatic flow and allowing for more consistent imaging as a precursor to planned procedures. The initial approach was intradermal injection of gadolinium-based contrast in the feet, which is readily absorbed into the lymph nodes and vessels (Ruehm et al., 2001). Although this technique allows for the delineation of peripheral lymphatic abnormalities, the injected contrast becomes more dilute as it flows centrally, thus limiting evaluation of the central lymphatics. To improve the evaluation of central lymphatics and decrease the dilutional effects of the contrast, intranodal injection of gadolinium-based contrast is now more commonly performed (Figure 20) (Krishnamurthy et al., 2016). Dynamic contrast-enhanced MRL is particularly useful to delineate abnormalities in patients with nontraumatic chylothorax,
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complicated traumatic chylous leaks, plastic bronchitis, congenital lymphatic flow disorders, and suspected secondary lymphatic flow abnormalities. Moreover, MRL excels at evaluating the anatomy of the central lymphatic system before surgery, is more sensitive than conventional lymphangiography in detecting lymphatic leaks, and can assist in procedural planning for lymphatic interventions. Future directions Dynamic contrast MRL, conventional lymphangiography, and lymphoscintigraphy are minimally invasive and allow for the evaluation of extremity and retroperitoneal lymphatics. However, without the direct injection of the liver or enteral lymphatics, there are no other ways to visualize this portion of the lymphatic circulation. The development of imaging techniques and contrast agents for the evaluation of liver and intestinal lymphatics is underway and could provide further insight into disease processes such as chylous ascites, ascitic fluid formation in hepatic cirrhosis, heart failure, and congenital lymphatic disorders. Moreover, as the production and distribution of lymph is better understood in each distinct lymphatic circulation and in various organs, it could provide targets for intervention previously unrealized. Conclusion The recent evolution and advanced knowledge in lymphatic imaging have contributed to the understanding of lymphatic anatomy, physiology, and multiple disease processes allowing for successful diagnosis and lymphatic intervention in a growing number of patients. References Aalami, O.O., Allen, D.B., & Organ, C.H., Jr. (2000). Chylous ascites: a collective review. Surgery, 128(5), 761-778. Cope, C. (1998). Diagnosis and treatment of postoperative chyle leakage via percutaneous transabdominal catheterization of the cisterna chyli: a preliminary study. Journal of Vascular and Interventional Radiology, 9, 727-734. Cope, C. (2003). Usefulness of a percutaneous transhepatic coaxial micropuncture needle technique in patients with nondilated peripheral intrahepatic ducts. American Journal of Roentgenology, 181, 1017-1020. Cope, C., & Kaiser, L.R. (2002). Management of unremitting chylothorax by percutaneous embolization and blockage of retroperitoneal lymphatic vessels in 42 patients. Journal of Vascular and Interventional Radiology, 13, 1139-1148. Dori, Y., Keller, M.S., Rome, J.J., Gillespie, M.J., Glatz, A.C., Dodds, K., et al. (2016). Percutaneous lymphatic embolization of abnormal pulmonary lymphatic flow as treatment of plastic bronchitis in patients with congenital heart disease. Circulation, 133, 1160-1170. Fischer, H.W., & Zimmerman, G.R. (1959). Roentgenographic visualization of lymph nodes and lymphatic channels. American Journal of Roentgenology, 81, 517-534. Hayashi, S., & Miyazaki, M. (1999). Thoracic duct: Visualization at nonenhanced MR lymphographydinitial experience. Radiology, 212, 598-600.
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