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DOI: 10.1148/rg.236035704
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(Radiographics. 2003;23:1541-1558.)
© RSNA, 2003

EDUCATION EXHIBIT

Lymphography: An Old Technique Retains Its Usefulness1

Ali Guermazi, MD, Pauline Brice, MD, Christophe Hennequin, MD and Emile Sarfati, MD

1 From the Departments of Radiology (A.G.), Hematology (P.B.), Radiation Therapy (C.H.), and Surgery (E.S.), Saint-Louis University Hospital AP-HP, Paris, France. Received February 28, 2003; revision requested April 9 and received May 1; accepted May 2. Address correspondence to A.G., Department of Radiology, University of California, 350 Parnassus Ave, Suite 150, San Francisco, CA 94117 (e-mail: ali.guermazi@oarg.ucsf.edu).


   Abstract
Top
 Abstract
Introduction
 Technique and Complications
 Normal Appearances and...
 Abnormal Lymphatics
 Neoplasms
 Conclusions
 References
 
Conventional lymphography has long been the method of choice for imaging the lymphatic system. However, the number of lymphographic studies performed in oncology centers has declined markedly since the introduction of cross-sectional imaging techniques, especially computed tomography (CT). Therefore, levels of expertise in both performing lymphography and interpreting lymphograms are falling. The unique ability of lymphography to demonstrate derangements of the internal architecture of normal-sized lymph nodes can be valuable and makes it more accurate than CT in evaluation of some lymphomas (especially Hodgkin disease) and genitourinary malignancies. In fact, lymphography and CT are complementary rather than mutually exclusive techniques for the staging of some lymphomas and genitourinary malignancies. In addition, lymphography opacifies the lymphatic channels and therefore may be a valuable tool for detection of lymphatic fistulas or lymphatic leakage. Finally, lymphography helps guide subsequent therapy in patients with lymphomas, genitourinary malignancies, or disorders of lymphatic flow.

© RSNA, 2003

Index Terms: Chyloperitoneum, 99.87 • Chylothorax, 99.87 • Chyluria, 99.87 • Lymphatic system, diseases, 99.84, 99.85 • Lymphography, 99.125, 99.80 • Lymphoma, staging, 99.834 • Testis, neoplasms, 99.8316 • Uterine neoplasms, staging, 99.8311


   Introduction
Top
 Abstract
 Introduction
Technique and Complications
 Normal Appearances and...
 Abnormal Lymphatics
 Neoplasms
 Conclusions
 References
 
For decades, conventional lymphography has been considered the standard of reference for diagnosing pathologic conditions of the lymph nodes and lymphatics. During the past several years, technological innovations, especially computed tomography (CT), have severely curtailed its use. However, lymphography has the unique capability of demonstrating internal architectural derangements within normal-sized lymph nodes. This highly valuable advantage makes lymphography diagnostically more accurate than CT (which demonstrates size rather than architecture) in some lymphomas and genitourinary malignancies. Lymphography still has a cornerstone role in diagnosis and management of lymphatic circulatory disorders.

In this article, we describe the technique of lymphography and complications that may occur, the normal lymphographic appearances and normal variations, and the residual uses of lymphography in diagnosis of lymphatic flow disorders and in staging of some lymphomas and genitourinary malignancies. We also emphasize the contribution of lymphography to therapeutic management.


   Technique and Complications
Top
 Abstract
 Introduction
 Technique and Complications
Normal Appearances and...
 Abnormal Lymphatics
 Neoplasms
 Conclusions
 References
 
Lymphography is an outpatient procedure. The first step is to verify the absence of contraindications, which are cardiovascular or pulmonary disease, especially in patients with pulmonary insufficiency or right-to-left cardiac shunt. At our institution, a mixture of 3 mL of 1% Xylocaine (lidocaine; AstraZeneca, London, England) and 2 mL of methylene blue dye (2.5% Patent Blue V dye; Guerbet Laboratories, Aulnay-sous-Bois, France) is injected into the tissues on the dorsal aspect of the foot between the toes. The lymphatic is therefore identified just after it has been filled with the dye. The site on the foot chosen to expose and cannulate a lymphatic is very important. It is best to select a vessel just lateral to the base of the first metatarsal. The incision should be vertical. If the first attempt is unsuccessful, a vessel higher up near the ankle may be chosen. The vessel is exposed, and fat and loose areolar tissue are stripped off of the lymphatic. A fine catheter is then inserted into the lymphatic vessel. The catheter and needle are secured with adhesive strips. The patient remains supine during the procedure but may be given fluids and additional medication if necessary.

The standard material used for lymphography is Ethiodol (an iodinated ethyl ester of the fatty acids of poppy seed oil) (Savage Laboratories, Melville, NY); nevertheless, at our institution we prefer injecting Lipiodol ultrafluid (a 48% iodinated glycerol ester) (Guerbet Laboratories). These contrast media provide excellent opacification of the lymph vessels and nodes because they do not diffuse through the vessel wall like water-soluble contrast media. They remain in the nodes for months and sometimes years, allowing one to evaluate the effects of treatment or progression of the disease. After cannulation of one lymphatic vessel, intralymphatic injection of the contrast agent with an adequate injector is performed. The normal dose is 6–7 mL of contrast medium injected into the lymphatics of each extremity. The rate of injection is 4–10 mL/h, depending on the size of the lymphatic. Too rapid a rate of injection will rupture the lymphatic. After the injection is complete, the wound is thoroughly cleansed, sutured, and covered with adhesive bandages. The sutures are removed after 10–12 days.

Six views are routinely obtained after the injection has been terminated and repeated 24 hours later for lymph node detail. Follow-up film images of the abdomen are obtained to evaluate progress of treatment or recurrent disease, until the amount of contrast material remaining in the node is insufficient for evaluation (1–3).

The major complications of lymphography are caused by the vital dye and contrast materials rather than the technique. Indeed, all authors report only infrequent and minor complications. Among all complications, pulmonary oil embolization is the most frequent. It usually does not produce clinical symptoms unless there is an underlying cardiopulmonary disorder, excess amounts (>20 mL) of contrast material are given, there are patent lymphovenous communications, or the patient is hypersensitive to the oil. Pulmonary infarction is most probably due to mechanical obstruction of the lung capillaries by oil droplets. The injection speed in lymphography with oily contrast media is not an important factor in the cause of pulmonary embolism, since pulmonary infarction may occur some days after lymphography. However, the large amount of contrast medium needed considerably increases the risk of pulmonary infarction. The total amount of oily contrast medium injected on each side should never exceed 10 mL (usually 1 mL/10 kg per foot, not exceeding a total volume of 14 mL) (2). These asymptomatic pulmonary oil embolisms are usually found on chest CT scans obtained 24 hours after lymphography (Fig 1) (4).



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  		Figure 1a.  Pulmonary oil embolism in an 18-year-old woman with Hodgkin disease. (a) Staging chest CT scan obtained 24 hours after lymphography shows several peripheral areas of pulmonary consolidation (arrowheads), which are due to pulmonary infarction. (b) Anteroposterior chest radiograph shows subtle, asymmetric, peripheral areas of increased opacity in the lungs (greater on the left than on the right).

 


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  		Figure 1b.  Pulmonary oil embolism in an 18-year-old woman with Hodgkin disease. (a) Staging chest CT scan obtained 24 hours after lymphography shows several peripheral areas of pulmonary consolidation (arrowheads), which are due to pulmonary infarction. (b) Anteroposterior chest radiograph shows subtle, asymmetric, peripheral areas of increased opacity in the lungs (greater on the left than on the right).

 
Other complications have also been described, such as hypersensitivity to methylene blue dye and ethiodized oil (5), intraalveolar hemorrhage with complete reversibility (6), hypothyroidism (7), and systemic arterial embolization to the brain or kidney, which is a rare complication in patients with right-to-left cardiac shunts (8,9).


   Normal Appearances and Variations
Top
 Abstract
 Introduction
 Technique and Complications
 Normal Appearances and...
Abnormal Lymphatics
 Neoplasms
 Conclusions
 References
 
The normal lymphographic appearance is characterized by a homogeneous, even-textured, fine granularity that is due to the relationship between the opacified sinus system and the nonopacified lymphoid follicles. The margin of the node is well defined, with the hilar area usually demarcated by a smooth indentation (Fig 2) (10). The phenomenon of a slight increase in the dimensions of lymph nodes 24–48 hours after lymphography is well known, but this effect should be minimal a few weeks later (11). Thus, large nodes with uniform distribution of contrast material are considered hyperplastic, individually and as a group (10).



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  		Figure 2a.  Normal appearance of lymph nodes. (a) Lymphogram obtained during the filling phase shows a homogeneous appearance of the lymph nodes. (b) Lymphogram obtained during the nodal phase shows a smooth peripheral indentation (arrowheads), which corresponds to the hilar area.

 


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  		Figure 2b.  Normal appearance of lymph nodes. (a) Lymphogram obtained during the filling phase shows a homogeneous appearance of the lymph nodes. (b) Lymphogram obtained during the nodal phase shows a smooth peripheral indentation (arrowheads), which corresponds to the hilar area.

 
Filling of the inguinal lymphatics with contrast material demonstrates wide variations in the number, size, and appearance of the nodes. This significant variability of nonmalignant nodes can simulate malignancy in this region. Therefore, it is quite tenuous to interpret the inguinal nodes as containing primary or secondary malignant disease without substantial abnormality in higher regions (10). In contrast, paraaortic nodes have proved to be the most reliable group for showing features of high diagnostic accuracy (Fig 3) (3). Lymph flow enters the blood system as the thoracic duct usually ends its course in the left subclavian vein. The cisterna chyli is usually asaccular structure less than 5 cm in length but of greater width than the adjacent thoracic duct (Fig 4). The thoracic duct sharply merges into the junction of the left subclavian vein and left internal jugular vein (Fig 5) (12).



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  		Figure 3a.  Anteroposterior (a) and lateral (b) drawings show the anatomy of the pelvic and retroperitoneal lymphatics.

 


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  		Figure 3b.  Anteroposterior (a) and lateral (b) drawings show the anatomy of the pelvic and retroperitoneal lymphatics.

 


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  		Figure 4.  Normal appearance of the cisterna chyli. Lymphogram shows the cisterna chyli and the abdominal segment of the thoracic duct.

 


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  		Figure 5.  Normal appearance of the thoracic duct. Lymphogram shows the termination of the thoracic duct at the left subclavian-jugular venous anastomosis at the base of the neck. At the termination, several powerful valves are seen.

 
Some rarely seen nodes are situated extrinsically to the usual lymphographic regions, such as the popliteal, posterior intercostal, mediastinal, bilateral hilar, paratracheal, and supraclavicular nodes and even nodes in the axilla (13,14). The cisterna chyli usually lies at the midline of the body of L1 but may also be situated on either side of the midline. The thoracic duct may comprise two or more branches and may even empty into the junction of the right subclavian vein and right internal jugular vein (12).

Interpretation of lymphograms depends on careful scrutiny of both the lymphatic and nodal phases (15,16). If both lymphography and CT are to be performed, lymphography should precede CT, as contrast material in the lymph nodes may facilitate interpretation of the CT scans, particularly in patients with little retroperitoneal fat (11,16,17).


   Abnormal Lymphatics
Top
 Abstract
 Introduction
 Technique and Complications
 Normal Appearances and...
 Abnormal Lymphatics
Neoplasms
 Conclusions
 References
 
Chylous Syndromes
Chylous Ascites.— Chylous ascites is a rare clinical condition that occurs as a result of disruption of the abdominal lymphatics. The primary form may be fistulous or exudative. The fistulous type demonstrates dilated lymphatic vessels, which lead to formation of a fistula associated with large capacious megalymphatics demonstrated at lymphography. In contrast, the exudative type is associated with a hypoplastic pattern. Before treatment of chylous ascites is begun, lymphography should be performed to demonstrate the type of chylous ascites. The fistulous form may be corrected by closure of the defect in the lymphatic vessel, its level being localized with lymphography. Postlymphographic CT may be useful for determining the exact level of the lymphatic vessel leakage. The exudative form may require a lymphovenous shunt.

Multiple causes have been reported, including abdominal surgery (retroperitoneal lymphadenectomy, surgery for abdominal aortic aneurysm, genitourinary oncologic surgery, pancreaticoduodenectomy, vagotomy), malignant neoplasms (the most common cause in adults), blunt abdominal trauma, spontaneous bacterial peritonitis, cirrhosis, pelvic irradiation, peritoneal dialysis, abdominal tuberculosis (Fig 6), and congenital defects in lacteal formation. There is high mortality in untreated cases. By contrast, most patients who are treated recover (18–21).



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  		Figure 6a.  Chylous ascites in a 43-year-old human immunodeficiency virus-positive man with peritoneal tuberculosis. (a) Lymphogram obtained during the filling phase shows peritoneal extravasation of contrast material. The site of the leakage is seen immediately to the left of L4 (arrow). Multiple lympholymphatic anastomoses between both sides of the lymphatic system are also evident. (b) CT scan obtained after lymphography shows the exact level of the damage to the lymphatic vessels (arrowhead). It also shows a dysmorphic liver and ascites. (c) Lymphogram obtained during the storage phase shows extensive leakage in the form of oily droplets within the peritoneal cavity.

 


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  		Figure 6b.  Chylous ascites in a 43-year-old human immunodeficiency virus-positive man with peritoneal tuberculosis. (a) Lymphogram obtained during the filling phase shows peritoneal extravasation of contrast material. The site of the leakage is seen immediately to the left of L4 (arrow). Multiple lympholymphatic anastomoses between both sides of the lymphatic system are also evident. (b) CT scan obtained after lymphography shows the exact level of the damage to the lymphatic vessels (arrowhead). It also shows a dysmorphic liver and ascites. (c) Lymphogram obtained during the storage phase shows extensive leakage in the form of oily droplets within the peritoneal cavity.

 


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  		Figure 6c.  Chylous ascites in a 43-year-old human immunodeficiency virus-positive man with peritoneal tuberculosis. (a) Lymphogram obtained during the filling phase shows peritoneal extravasation of contrast material. The site of the leakage is seen immediately to the left of L4 (arrow). Multiple lympholymphatic anastomoses between both sides of the lymphatic system are also evident. (b) CT scan obtained after lymphography shows the exact level of the damage to the lymphatic vessels (arrowhead). It also shows a dysmorphic liver and ascites. (c) Lymphogram obtained during the storage phase shows extensive leakage in the form of oily droplets within the peritoneal cavity.

 
Chylothorax.— Chylothorax is a rare condition characterized by accumulation of a fluid containing chylomicrons within the pleural cavity. It may be caused by primary lymphatic disease but is more often secondary to intrathoracic malignancy, trauma, or surgery (22) or is rarely associated with sarcoidosis (23). Lymphography not only assists in localizing the site of fistulous formation but also demonstrates the anatomy of the thoracic duct, a highly variable structure. Moreover, lymphography has been shown to be useful in demonstrating the nature of lymphatic damage, assisting in selection of patients for surgery, and helping determine the type of surgery to be performed (12,24,25).

Cases following trauma, which may be as varied as esophageal, cardiac, pulmonary, mediastinal, or thoracic spinal surgery, subclavian catheterization, scalene node biopsy, radial neck surgery, or gunshot wounds, require the most judgment. For patients who have already had the thoracic duct clipped during esophagectomy, lymphography will demonstrate whether the clipping was complete or whether leakage was occurring from collateral vessels, branches of the thoracic duct, or variant lymphatic channels (24). Postlymphographic CT is of additional value in demonstrating the communication between the pleural space and the lymphatic system by revealing lymphographic contrast material within the pleural space (Fig 7) (25,26).



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  		Figure 7a.  Laceration of the thoracic duct in a 59-year-old woman with chylothorax after esophagectomy. (a) Lymphogram shows extravasation of contrast material from the thoracic duct with accumulation in the pleural space (arrow). (b) Chest CT scan obtained after lymphography shows extensive leakage from the thoracic duct at the T7-8 level (arrowhead) and accumulation of contrast material in the posterior right pleural space.

 


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  		Figure 7b.  Laceration of the thoracic duct in a 59-year-old woman with chylothorax after esophagectomy. (a) Lymphogram shows extravasation of contrast material from the thoracic duct with accumulation in the pleural space (arrow). (b) Chest CT scan obtained after lymphography shows extensive leakage from the thoracic duct at the T7-8 level (arrowhead) and accumulation of contrast material in the posterior right pleural space.

 
Chyluria.— Chyluria is an abnormal condition in which chyle appears in the urine because of a fistulous communication between the lymphatics and the urinary tract. Although the most common cause is parasitic with infestation by Wuchereria bancrofti, nonparasitic chyluria may arise due to thoracic duct stricture or direct injury to the kidney with formation of lymphatic-urinary fistulas. Obstruction of the larger lymphatic vessels may be caused by trauma, tuberculosis, abscess, or neoplasms, such as malignant lymphoma. Other infrequent causes include lymphangiectasy, pelvic lipomatosis, compression of the thoracic duct by a pseudoaneurysm of the thoracic aorta, or even pregnancy (27,28).

Lymphography is effective for diagnosis, demonstrating the lymphaticopelvic fistulization around the renal pedicle. Moreover, lymphography in patients with unilateral chyluria often reveals contralateral collateral lymph vessels (29–31). It is important to consider the possibility of contralateral lesions or an incipient stage of bilateral disease when selecting treatment for chyluria (30). Lymphographic findings of chyluria include marked dilatation, multiplication, winding, and tortuosity of the lymphatic vessels around the hilar region of the kidneys. Opacification of the caliceal systems, ureter, and bladder appears in about 40% of patients (27). Postlymphographic CT findings may be useful in determining the exact level of the lymphatic vessel lesion (Fig 8) (29). The treatment may be medical, endoscopic, or surgical. Lymphography may be therapeutic as well as diagnostic (27–30,32).



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  		Figure 8a.  Chyluria in an 84-year-old woman with W bancrofti filariasis. (a) Lymphogram obtained during   the filling phase shows numerous collateral lymphatic vessels around the left kidney. Numerous lympholymphatic anastomoses are seen between both sides of the lymphatic system, a finding indicative of stasis.     (b) Lymphogram shows that the thoracic duct is obliterated and appears tortuous and expanded. These    findings are typical of filariasis. (c) CT scan obtained after lymphography shows that contrast material has flowed off into pyelocaliceal structures and shows the exact site of the leakage at the level of the left kidney. (d) Lymphogram obtained during the nodal phase at 24 hours shows contrast material in the calices of the left kidney.

 


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  		Figure 8b.  Chyluria in an 84-year-old woman with W bancrofti filariasis. (a) Lymphogram obtained during   the filling phase shows numerous collateral lymphatic vessels around the left kidney. Numerous lympholymphatic anastomoses are seen between both sides of the lymphatic system, a finding indicative of stasis.     (b) Lymphogram shows that the thoracic duct is obliterated and appears tortuous and expanded. These    findings are typical of filariasis. (c) CT scan obtained after lymphography shows that contrast material has flowed off into pyelocaliceal structures and shows the exact site of the leakage at the level of the left kidney. (d) Lymphogram obtained during the nodal phase at 24 hours shows contrast material in the calices of the left kidney.

 


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  		Figure 8c.  Chyluria in an 84-year-old woman with W bancrofti filariasis. (a) Lymphogram obtained during   the filling phase shows numerous collateral lymphatic vessels around the left kidney. Numerous lympholymphatic anastomoses are seen between both sides of the lymphatic system, a finding indicative of stasis.     (b) Lymphogram shows that the thoracic duct is obliterated and appears tortuous and expanded. These    findings are typical of filariasis. (c) CT scan obtained after lymphography shows that contrast material has flowed off into pyelocaliceal structures and shows the exact site of the leakage at the level of the left kidney. (d) Lymphogram obtained during the nodal phase at 24 hours shows contrast material in the calices of the left kidney.

 


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  		Figure 8d.  Chyluria in an 84-year-old woman with W bancrofti filariasis. (a) Lymphogram obtained during   the filling phase shows numerous collateral lymphatic vessels around the left kidney. Numerous lympholymphatic anastomoses are seen between both sides of the lymphatic system, a finding indicative of stasis.     (b) Lymphogram shows that the thoracic duct is obliterated and appears tortuous and expanded. These    findings are typical of filariasis. (c) CT scan obtained after lymphography shows that contrast material has flowed off into pyelocaliceal structures and shows the exact site of the leakage at the level of the left kidney. (d) Lymphogram obtained during the nodal phase at 24 hours shows contrast material in the calices of the left kidney.

 
External Genital Lymphedema.— External genital lymphedema is more frequently secondary. The acquired form of genital lymphedema is frequently due to filariasis and other infectious diseases. Lymphography shows dilated dysfunctional lymphatics with reflux into the scrotum (Fig 9) (33).



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  		Figure 9a.  External genital lymphedema of parasitic origin in a 38-year-old man. (a) Lymphogram obtained during the filling phase shows filling of the scrotum by left-sided lymphatic reflux. (b) Lymphogram obtained during the nodal phase at 24 hours shows accumulation of contrast material in the scrotum (arrowheads). The lymph nodes are normal.

 


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  		Figure 9b.  External genital lymphedema of parasitic origin in a 38-year-old man. (a) Lymphogram obtained during the filling phase shows filling of the scrotum by left-sided lymphatic reflux. (b) Lymphogram obtained during the nodal phase at 24 hours shows accumulation of contrast material in the scrotum (arrowheads). The lymph nodes are normal.

 
Obstruction and Collateral Flow
Lympholymphatic and Lymphovenous Anastomoses.— When the lymphatic system is overwhelmed and edema develops, lympholymphatic and lymphovenous shunts may occur as an attempt at decompression. When one is performing lymphography, especially when obstruction is suspected, it is imperative to obtain images frequently and possibly to perform fluoroscopy to demonstrate lymphovenous communications (Fig 10) and thus prevent extensive oil embolization. The flow in veins is considerably more rapid than in lymphatic vessels, and the contrast material appears as tiny droplets in the dependent portion of the vein (33).



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  		Figure 10.  Lymphovenous shunt in a 42-year-old man with lymphedema of the right leg after surgery for a right-sided inguinocrural hernia. Lymphogram obtained during the filling phase shows complete obliteration of the right lymphatic flow at the level of the right inguinocrural region (arrow) and opacification of the inferior vena cava by contrast material (arrowheads).

 
Perineural and Perivascular Spaces.— Perineural and perivascular spaces are more frequently seen in patients with edema, although they have been demonstrated in patients without lymphatic obstruction. The pattern of opacification follows the contour of the particular vessel and occasionally the nerve (Figs 11, 12).



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  		Figure 11a.  Primary lymphatic aplasia of the left leg in a 12-year-old girl. (a) Lymphogram obtained during the filling phase shows absence of opacification of the left abdominopelvic lymphatic system. (b) Plain radiograph centered on the left knee shows absence of lymphatic collectors in the left leg with filling of superficial lymphatic vessels in the skin (dermal reflux). These findings are consistent with lymphatic aplasia.

 


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  		Figure 11b.  Primary lymphatic aplasia of the left leg in a 12-year-old girl. (a) Lymphogram obtained during the filling phase shows absence of opacification of the left abdominopelvic lymphatic system. (b) Plain radiograph centered on the left knee shows absence of lymphatic collectors in the left leg with filling of superficial lymphatic vessels in the skin (dermal reflux). These findings are consistent with lymphatic aplasia.

 


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  		Figure 12.  Perivascular extravasation in a 28-year-old woman with edema of the left leg as a result of aplasia of the lymphatic vessels in the left leg. Lymphogram obtained immediately after administration of contrast material shows no lymphatic vessels. The contrast material is drained by the lymphatic system, mainly along the venous vessel sheaths.

 
Lymphocele and Lymphatic Fistula.— Injury to lymphatic vessels, such as surgery or blunt trauma, leads to passage of lymph into the soft tissues of body cavities. The lymph may be confined and form a lymphocele (Fig 13) or may exit through a surgical wound. Severe lymphatic fistulas with a large amount of lymphatic drainage may follow thoracic duct injury from radical chest surgery (33).



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  		Figure 13a.  Pelvic lymphoceles in a 48-year-old woman after appendectomy. (a) Pelvic lymphogram obtained during the filling phase shows a right-sided pelvic cavity filled with contrast material (arrow). There is also a smaller cavity filled with contrast material (arrowhead). There is no opacification of lymphatic vessels beyond the large lymphocele. (b) CT scan obtained after lymphography shows that the lymphocele is partially filled with contrast material. (c) Pelvic lymphogram obtained during the nodal phase shows the lymphoceles. It also shows stasis of contrast material prior to the lymphoceles and no opacification of the lymph nodes beyond the large lymphocele.

 


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  		Figure 13b.  Pelvic lymphoceles in a 48-year-old woman after appendectomy. (a) Pelvic lymphogram obtained during the filling phase shows a right-sided pelvic cavity filled with contrast material (arrow). There is also a smaller cavity filled with contrast material (arrowhead). There is no opacification of lymphatic vessels beyond the large lymphocele. (b) CT scan obtained after lymphography shows that the lymphocele is partially filled with contrast material. (c) Pelvic lymphogram obtained during the nodal phase shows the lymphoceles. It also shows stasis of contrast material prior to the lymphoceles and no opacification of the lymph nodes beyond the large lymphocele.

 


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  		Figure 13c.  Pelvic lymphoceles in a 48-year-old woman after appendectomy. (a) Pelvic lymphogram obtained during the filling phase shows a right-sided pelvic cavity filled with contrast material (arrow). There is also a smaller cavity filled with contrast material (arrowhead). There is no opacification of lymphatic vessels beyond the large lymphocele. (b) CT scan obtained after lymphography shows that the lymphocele is partially filled with contrast material. (c) Pelvic lymphogram obtained during the nodal phase shows the lymphoceles. It also shows stasis of contrast material prior to the lymphoceles and no opacification of the lymph nodes beyond the large lymphocele.

 

   Neoplasms
Top
 Abstract
 Introduction
 Technique and Complications
 Normal Appearances and...
 Abnormal Lymphatics
 Neoplasms
Conclusions
 References
 
Selection of appropriate imaging techniques for the staging of malignancy requires consideration of a number of factors beyond a sound knowledge of the pathologic characteristics and behavior of individual diseases, their modes of spread, and their sites of relapse. Although the accuracy, sensitivity, and specificity of a diagnostic test are clearly important, other issues such as the availability of equipment and expertise, the degree of invasiveness of the test, its cost, its contraindications and side effects, and the preferences of both the radiologist and clinician involved must be appreciated. Of paramount importance is whether the result of the investigation undertaken in combination with all other diagnostic information available will influence the staging of a disease and its subsequent treatment. The number of lymphographic studies performed in oncology centers has declined markedly since the introduction of cross-sectional imaging techniques, particularly CT (34). In the following sections, we will try to assess whether this trend is justified and to determine any residual use for lymphography in the investigation and follow-up of cancer.

Lymphomas
Hodgkin Disease.— To a large extent, Hodgkin disease has become a curable disease. At presentation, Hodgkin disease is usually supradiaphragmatic, often spreading predictably from one nodal group contiguously to the next along the lymphatic pathways (35,36). Conversely, overstaging of the disease leads to unnecessary and possibly dangerous overtreatment (37). Hodgkin disease is usually almost entirely confined to the lymph nodes. Lymphography aims to examine the retroperitoneal, common iliac, external iliac, and inguinal lymph nodes; mesenteric nodes are not viewed but are rarely involved in Hodgkin disease (38). Disease is diagnosed when an alteration in appearances of the lymph nodes is seen: focal filling defects or a foamy, licelike appearance. Lymph node size is not the prime diagnostic criterion (16).

Some authors recommend performing staging laparotomy with splenectomy and biopsy of the liver and multiple lymph nodes (36,39–42). Nevertheless, laparotomy is a surgical procedure and is now being given up for two reasons. First, side effects of the procedure are severe, with an overall mortality of 1.5%–3%. Second, since the procedure is itself a prognostic factor for relapse-free survival, it is becoming of lesser value with the improved overall survival (43–45). For these reasons, laparotomy has become obsolete (35,44), and its risk-benefit balance has recently been quantified as unfavorable in a randomized trial conducted in the best possible setting for laparotomy (43). Other authors consider the ultimate arbiter of Hodgkin disease to be CT, thus rendering lymphography superfluous. Although less invasive, abdominal CT requires both oral and intravenous contrast material for good-quality studies. It is appropriate to replace lymphography with CT if lymph node enlargement is detected, even though there is a risk of false-positive results (36,44,46). In such cases, the enlarged lymph nodes of benign hyperplasia can usually be distinguished from tumorous nodes with lymphography (1,38,46).

Lymphography has traditionally been the standard of reference for staging Hodgkin disease due to its ability to demonstrate malignant involvement within nodes that are not enlarged and appear normal at CT (Fig 14) (1,16,44,46,47). The diagnostic superiority of lymphography over CT is statistically significant (16,42). Indeed, involved nodes are generally smaller than those in non-Hodgkin lymphoma and may appear normal at CT (16). According to the literature, the combined use of CT and lymphography in the same patients leads to discrepant findings in 4%–33% of cases. These discrepancies consist mainly of normal CT findings in combination with abnormal lymphographic findings (37). Architecture is frequently the only tip-off (4,48); this has led many centers to reserve lymphography for staging in patients with stage I or II supradiaphragmatic Hodgkin disease and negative results at abdominal and pelvic CT (4,34).



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  		Figure 14a.  Hodgkin disease in a 25-year-old woman. (a) Magnified left oblique lymphogram obtained during the nodal phase shows multiple tumorous lateroaortic lymph nodes with a typical diffuse foamy appearance (arrowheads). (b) Contrast material-enhanced staging abdominal CT scan obtained 2 hours before lymphography shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes (arrowheads) at the level of L3.

 


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  		Figure 14b.  Hodgkin disease in a 25-year-old woman. (a) Magnified left oblique lymphogram obtained during the nodal phase shows multiple tumorous lateroaortic lymph nodes with a typical diffuse foamy appearance (arrowheads). (b) Contrast material-enhanced staging abdominal CT scan obtained 2 hours before lymphography shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes (arrowheads) at the level of L3.

 
Lymphography provides information beyond that of CT or, at present, magnetic resonance (MR) imaging. The only criterion for abnormality with CT and MR imaging is size. One has to be especially careful when the sole criterion for abnormality is size and that size is measured in millimeters. The choice of size is arbitrary and depends on the balance between false-positive and false-negative results desired by the clinicians at a particular institution. For follow-up, to determine response to therapy or relapse, abdominal radiography is considerably less expensive than CT or MR imaging. Moreover, early relapses can be detected by means of subtle changes in the nodes that may not be detectable at CT (Fig 15) (15,46,48). For these reasons, many authors believe that lymphography and CT are complementary and that lymphography has its place in staging in previously untreated patients with Hodgkin disease and normal abdominal CT scans (1,4, 36,48).



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  		Figure 15a.  Hodgkin disease in a 22-year-old woman. (a) Initial lymphogram obtained during the nodal phase shows a normal appearance. (b, c) Follow-up lymphograms obtained at 6 (b) and 12 (c) months show that the lymph nodes are still opacified and have a normal appearance. (d) Follow-up lymphogram obtained at 16 months shows that the oil droplets are farther apart (arrowheads), a finding associated with abdominal recurrence, which was confirmed clinically.

 


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  		Figure 15b.  Hodgkin disease in a 22-year-old woman. (a) Initial lymphogram obtained during the nodal phase shows a normal appearance. (b, c) Follow-up lymphograms obtained at 6 (b) and 12 (c) months show that the lymph nodes are still opacified and have a normal appearance. (d) Follow-up lymphogram obtained at 16 months shows that the oil droplets are farther apart (arrowheads), a finding associated with abdominal recurrence, which was confirmed clinically.

 


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  		Figure 15c.  Hodgkin disease in a 22-year-old woman. (a) Initial lymphogram obtained during the nodal phase shows a normal appearance. (b, c) Follow-up lymphograms obtained at 6 (b) and 12 (c) months show that the lymph nodes are still opacified and have a normal appearance. (d) Follow-up lymphogram obtained at 16 months shows that the oil droplets are farther apart (arrowheads), a finding associated with abdominal recurrence, which was confirmed clinically.

 


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  		Figure 15d.  Hodgkin disease in a 22-year-old woman. (a) Initial lymphogram obtained during the nodal phase shows a normal appearance. (b, c) Follow-up lymphograms obtained at 6 (b) and 12 (c) months show that the lymph nodes are still opacified and have a normal appearance. (d) Follow-up lymphogram obtained at 16 months shows that the oil droplets are farther apart (arrowheads), a finding associated with abdominal recurrence, which was confirmed clinically.

 
To minimize the long-term toxic effects, at least in patients with localized Hodgkin disease, it has been suggested that the aggressiveness of the treatment should be adapted to the patient’s initial characteristics (43,49). Lymphography is considered to be contributive to the good quality of the initial staging and to the choice of the optimal treatment, which combines a high remission rate and a reduction in long-term toxicity, especially in second cancers (50). Indeed, lymphography helps reduce radiation therapy to initially involved fields rather than extended fields when chemotherapy is also performed (Fig 16) (47). Many radiation therapists have demonstrated that lymphography is useful in visualizing and designing the paraaortic and "inverted Y" fields for irradiation. The clear depiction of opacified lymph nodes on lymphograms makes it easier to design appropriate therapy portals that will include abnormal retroperitoneal and pelvic lymph nodes (Fig 17) (1,38,46,51). The disappearance of staging lymphography makes the final stage less secure and requires reassuring treatments, that is, more extensive radiation therapy and chemotherapy (4,52).



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  		Figure 16a.  Hodgkin disease in a 58-year-old man. (a) Lymphogram obtained during the nodal phase shows localized involvement of the abdominoaortic lymph nodes on both sides and of the right pelvic lymph nodes. The left pelvic lymph nodes are normal. (b) Staging abdominal CT scan, obtained with intravenous contrast material 24 hours after lymphography, shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes at the L2-3 level. There was a favorable outcome at 3- and 6-month follow-up lymphography. (c) Follow-up lymphogram obtained at 12 months also shows a favorable outcome. (d) Lymphogram shows that the extent of radiation therapy is reduced to the initially involved field.

 


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  		Figure 16b.  Hodgkin disease in a 58-year-old man. (a) Lymphogram obtained during the nodal phase shows localized involvement of the abdominoaortic lymph nodes on both sides and of the right pelvic lymph nodes. The left pelvic lymph nodes are normal. (b) Staging abdominal CT scan, obtained with intravenous contrast material 24 hours after lymphography, shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes at the L2-3 level. There was a favorable outcome at 3- and 6-month follow-up lymphography. (c) Follow-up lymphogram obtained at 12 months also shows a favorable outcome. (d) Lymphogram shows that the extent of radiation therapy is reduced to the initially involved field.

 


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  		Figure 16c.  Hodgkin disease in a 58-year-old man. (a) Lymphogram obtained during the nodal phase shows localized involvement of the abdominoaortic lymph nodes on both sides and of the right pelvic lymph nodes. The left pelvic lymph nodes are normal. (b) Staging abdominal CT scan, obtained with intravenous contrast material 24 hours after lymphography, shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes at the L2-3 level. There was a favorable outcome at 3- and 6-month follow-up lymphography. (c) Follow-up lymphogram obtained at 12 months also shows a favorable outcome. (d) Lymphogram shows that the extent of radiation therapy is reduced to the initially involved field.

 


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  		Figure 16d.  Hodgkin disease in a 58-year-old man. (a) Lymphogram obtained during the nodal phase shows localized involvement of the abdominoaortic lymph nodes on both sides and of the right pelvic lymph nodes. The left pelvic lymph nodes are normal. (b) Staging abdominal CT scan, obtained with intravenous contrast material 24 hours after lymphography, shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes at the L2-3 level. There was a favorable outcome at 3- and 6-month follow-up lymphography. (c) Follow-up lymphogram obtained at 12 months also shows a favorable outcome. (d) Lymphogram shows that the extent of radiation therapy is reduced to the initially involved field.

 


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  		Figure 17a.  Hodgkin disease in a 46-year-old man. (a) Lymphogram obtained during the nodal phase shows disseminated involvement of the abdominopelvic lymph nodes. (b) Staging abdominal CT scan, obtained with intravenous contrast material 1 hour before lymphography, shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes at the L3 level. There was a favorable outcome at 2- and 6-month follow-up lymphography. (c, d) Lymphograms show that the clear demonstration of opacified lymph nodes makes design of the inverted Y field for irradiation easy and more accurate (c) and considerably reduces the field of radiation therapy (d).

 


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  		Figure 17b.  Hodgkin disease in a 46-year-old man. (a) Lymphogram obtained during the nodal phase shows disseminated involvement of the abdominopelvic lymph nodes. (b) Staging abdominal CT scan, obtained with intravenous contrast material 1 hour before lymphography, shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes at the L3 level. There was a favorable outcome at 2- and 6-month follow-up lymphography. (c, d) Lymphograms show that the clear demonstration of opacified lymph nodes makes design of the inverted Y field for irradiation easy and more accurate (c) and considerably reduces the field of radiation therapy (d).

 


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  		Figure 17c.  Hodgkin disease in a 46-year-old man. (a) Lymphogram obtained during the nodal phase shows disseminated involvement of the abdominopelvic lymph nodes. (b) Staging abdominal CT scan, obtained with intravenous contrast material 1 hour before lymphography, shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes at the L3 level. There was a favorable outcome at 2- and 6-month follow-up lymphography. (c, d) Lymphograms show that the clear demonstration of opacified lymph nodes makes design of the inverted Y field for irradiation easy and more accurate (c) and considerably reduces the field of radiation therapy (d).

 


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  		Figure 17d.  Hodgkin disease in a 46-year-old man. (a) Lymphogram obtained during the nodal phase shows disseminated involvement of the abdominopelvic lymph nodes. (b) Staging abdominal CT scan, obtained with intravenous contrast material 1 hour before lymphography, shows small (short-axis diameter < 10 mm) paraaortic and paracaval lymph nodes at the L3 level. There was a favorable outcome at 2- and 6-month follow-up lymphography. (c, d) Lymphograms show that the clear demonstration of opacified lymph nodes makes design of the inverted Y field for irradiation easy and more accurate (c) and considerably reduces the field of radiation therapy (d).

 
Non-Hodgkin Lymphoma.— In non-Hodgkin lymphomas, patients whose disease is staged with bone marrow biopsy and lymphography have significantly lower relapse rates than those whose disease is staged with less accurate procedures (53). Some authors have demonstrated that lymphographic and CT findings strongly influence Ann Arbor clinical stage, Ann Arbor pathologic stage, and initial management of non-Hodgkin lymphoma. Lymphographic and CT findings are in agreement on the presence or absence of retroperitoneal adenopathy in about 90% of patients. Because of the important individual and combined contributions of lymphography and CT to staging and management of non-Hodgkin lymphoma, authors have concluded that both studies should be performed during initial evaluation of newly diagnosed non-Hodgkin lymphoma. They add that lymphography could be omitted in some patients if the CT results are positive. However, if the CT results are negative for retroperitoneal adenopathy, lymphography will occasionally demonstrate disease (46,54,55). Better acceptance by patients and the ability to perform unlimited repeat studies make CT the preferred procedure. However, the discordant findings between lymphography and CT should caution those who may abandon lymphography completely (46,56,57).

Genitourinary Cancers
The natural history of genitourinary tumors often includes early tumor metastasis to regional lymph nodes. In most instances, the pelvic or paraaortic lymph nodes are the primary sites of nodal metastasis. Under properly selected circumstances, the ability of lymphography to demonstrate the internal architecture of lymph nodes and thereby allow detection of filling defects 5–7 mm in diameter makes it a complement to CT and a useful alternative to surgical lymphadenectomy (3).

Testicular Tumors.— The lymphatics of the testes accompany the internal spermatic artery and vein and drain directly into the paraaortic nodes. At lymphography, six to eight lymphatic vessels course from each testicle, turn medially, and empty into primary drainage sites located variously between T11-12 and L4-5. Crossover of lymphatics from the left chain to the right is unusual, but the drainage on the right frequently crosses to the left paraaortic area, resulting in contralateral nodal metastasis (3,17). Therefore, testicular tumors metastasize commonly via the lymphatics to the paraaortic nodes. Analysis demonstrates that tumors of the right testis most often spread first to the nodes of the interaortocaval zone just below the left renal vein, whereas tumors of the left testis spread predominantly to the preaortic nodes and left paraaortic nodes. The excellent visualization of these primary nodes on a bipedal lymphogram, coupled with the predictable pattern of spread, makes lymphography a useful method for detecting metastases from testis tumors, thereby avoiding the need for staging surgical exploration in cases that might be more appropriately managed otherwise (3).

Lymphography is performed in patients with negative CT results, particularly in seminoma, for which the primary treatment for metastatic nodal disease is radiation therapy rather than chemotherapy (17,52,58–60). Thus, the two techniques are complementary (3,17). It is generally accepted that lymphography provides additional information in "marker-only" patients, assisting the clinician in planning and monitoring therapy (61). Treatment of patients with abnormal lymphograms should reduce the prevalence of a sub-sequent tumor relapse (62). However, lymphadenectomy is widely practiced on the grounds that neither CT nor lymphography is a sufficiently accurate staging technique. Such a practice carries certain morbidity, in particular future sexual problems (loss of seminal emission) for these young patients (3,52). Chylous ascites may occur following lymphadenectomy for a testis tumor (19,21). Furthermore, there is no therapeutic benefit for patients with no nodal metastasis. Approximately five of six patients have no histologic evidence of tumor in the retroperitoneal nodes when the lymphogram is interpreted as normal and thus could have been spared the surgery (3).

Cervical Carcinoma.— Lymphography is routinely performed as an adjunct to CT in patients with clinical stage Ib or IIa cervical carcinoma prior to consideration for Wertheim hysterectomy. CT demonstrates nodes that will not opacify at lymphography. However, CT has a high false-negative rate for paraaortic lymphadenopathy and is unable to demonstrate small volume changes or allow differentiation between reactive and involved nodes (46). The same difficulties arise when MR imaging is used for staging cervical carcinoma (63). In the filling phase, lymphography may show collateral lymph vessels, a relatively reliable sign of metastases (64). Furthermore, nodal phase lymphography can show small-volume nodal involvement that is not demonstrated at CT in stage Ib disease (Fig 18) (65). This directly alters subsequent management to radiation therapy.



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  		Figure 18a.  Stage Ib cervical carcinoma in a 43-year-old woman. (a) Left oblique lymphogram obtained during the nodal phase shows filling defects in several left lateroaortic nodes. (b, c) Abdominopelvic CT scans obtained immediately after lymphography (b obtained at a higher level than c) show that the tumorous lymph nodes are too small to be positively identified.

 


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  		Figure 18b.  Stage Ib cervical carcinoma in a 43-year-old woman. (a) Left oblique lymphogram obtained during the nodal phase shows filling defects in several left lateroaortic nodes. (b, c) Abdominopelvic CT scans obtained immediately after lymphography (b obtained at a higher level than c) show that the tumorous lymph nodes are too small to be positively identified.

 


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  		Figure 18c.  Stage Ib cervical carcinoma in a 43-year-old woman. (a) Left oblique lymphogram obtained during the nodal phase shows filling defects in several left lateroaortic nodes. (b, c) Abdominopelvic CT scans obtained immediately after lymphography (b obtained at a higher level than c) show that the tumorous lymph nodes are too small to be positively identified.

 
Although the presence of lymph node metastases does not change the clinical stage, it is well known that survival and disease-free interval in cervical carcinoma are considerably shortened by the presence of positive nodal involvement (34,47,64,66). Cervical carcinomas with extensive nodal involvement proved at lymphography receive primary irradiation. Pelvic lymphadenectomy is certainly the most accurate method of staging cervical cancer but is associated with postoperative complications such as wound infection, thromboembolic phenomena, and postoperative edema (63,67).


   Conclusions
Top
 Abstract
 Introduction
 Technique and Complications
 Normal Appearances and...
 Abnormal Lymphatics
 Neoplasms
 Conclusions
References
 
Lymphography and CT are complementary, not opposed, in diagnosis and staging of malignancies, especially Hodgkin disease. Unfortunately, it seems that many radiologists and clinicians neglect the potential advantages of lymphography over CT for demonstrating internal architecture in patients with malignancies. A downward trend in the practice of lymphography can be seen in teaching centers all over the world. Such a situation makes it difficult for trainees to gain experience in the technique, particularly with regard to reporting. This vicious cycle contributes to the disappearance of lymphography in the management of cancer. Its use is not controversial for chylous syndromes and obstruction of the lymphatic vessels, and lymphography will probably continue to remain unchallenged as the examination of choice in diagnosis and localization of lymphatic vessel damage.


   Footnotes
 
See the commentary by Winick following this article.


   References
Top
 Abstract
 Introduction
 Technique and Complications
 Normal Appearances and...
 Abnormal Lymphatics
 Neoplasms
 Conclusions
 References
 

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