The British Journal of Radiology, 82 (2009), 286290

The effectiveness of lymphangiography as a treatment method for various chyle leakages

1

T MATSUMOTO, MD, 1T YAMAGAMI, MD, PhD, 1,2T KATO, MD, PhD, 1,3T HIROTA, 1 R YOSHIMATSU, MD, 1T MASUNAMI, MD and 1T NISHIMURA, MD, PhD
1

MD, PhD,

Department of Radiology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine 465 Kajiicho, Kawaramachi Hirokoji, Kamigyo-ku, 6028566, Kyoto, 2Department of Radiology, Matsushita Memorial Hospital, Sotojima-cho 5-55, Moriguchi, 5708540, Osaka and 3Department of Radiology, Kyoto First Red Cross Hospital, 15749 Honmachi, Higashiyama, 6050981, Kyoto, Japan

ABSTRACT. The purpose of this study was to assess the effectiveness of lymphangiography as a treatment for various chyle leakages. Pedal lymphangiography was performed in 9 patients (6 men and 3 women; mean age, 59 years) who were unlikely to be cured only by conservative treatment a low-fat medium-chain triglyceride diet, total parenteral nutrition and insertion of a drainage tube and in whom chylothorax (n55), chylous ascites (n52) and lymphatic fistulae (n52) were refractory to conservative treatment. In 7 of these 9 patients (78%), we could detect the chyle leakage sites. In 8 of the 9 patients (89%), lymphatic leakage was stopped after lymphangiography, and surgical re-intervention was avoided. No cases had a recurrence of chyle leakage during follow-up (range, 154 months). Lymphangiography is effective not only for diagnosis but also as treatment for various chyle leakages. Early lymphangiography is therefore recommended for patients with chyle leakages who are unlikely to be cured by conservative treatment only.

Received 18 October 2007 Revised 1 February 2008 Accepted 5 March 2008 DOI: 10.1259/bjr/64849421
2009 The British Institute of Radiology

The use of conventional lymphangiography has become much less frequent since improvements have been made in the diagnostic ability of CT imaging and MRI. Lymphangiography has been the method of choice for imaging the lymphatic nodes and lymphatics. In addition, lymphangiography has been a valuable tool for the detection of various chyle leakages, such as chylothorax, chylous ascites, chyluria and lymphatic fistulae [1]. Recently, a case was reported in which lymphangiography played an important role in not only the diagnosis but also the approach to chyle leakage therapy. After retroperitoneal lymphadectomy, chylous ascites refractory to conservative therapy disappeared spontaneously after lymphangiography [2]. In our present study, we investigated the effectiveness of lymphangiography as a treatment for various chyle leakages refractory to conservative therapy using a larger number of subjects.

Methods and materials

9 patients (6 men, 3 women; age range, 3483 years; mean age, 59 years) who were unlikely to be cured by conservative treatment only, i.e. a low-fat medium-chain triglyceride diet, total parenteral nutrition and insertion of a drainage tube, underwent pedal lymphangiography between January 2003 and March 2006. All patients were known or suspected to have chylothorax (n55), chylous
Address correspondence to: Tomohiro Matsumoto, Department of Radiology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine 465 Kajiicho, Kawaramachi Hirokoji, Kamigyo-ku, 6028566, Kyoto, Japan. E-mail: t-matsu@koto.kpum. ac.jp

ascites (n52) or a lymphatic fistula (n52). The chyle leakages occurred (i) after oesophagectomy for oesophageal cancer (n54), (ii) after axillary lymphadectomy for breast cancer (n51), (iii) idiopathically (n51), (iv) after pelvic lymphadectomy for ovarian cancer (n51), (v) after retroperitoneal lymphadectomy for testicular cancer (n51) and (vi) after aortic root replacement for annuloaortic ectasia (n51). Chyle leakage had persisted for between 10 days and 6 weeks, when lymphangiography was performed. In all cases, a thoracic, abdominal, mediastinal or axillary drainage tube was put into place. The daily amount of drainage ranged between 150 ml and 1500 ml (mean, 533 ml) (Table 1). Lymphangiography was performed after written informed consent was obtained from each patient. First, 2.5 ml of indigocarmine (Daiichi Pharmaceutical, Tokyo, Japan), a dye that stains the lymphatics, was injected into the web space between the first and second toes of each foot. 30 min later, linear cut-down was performed on the dorsum of the foot below the ankle, and the lymphatic vessel was isolated. After cannulation of a lymphatic vessel on the dorsum of each foot using a 30 gauge needle, iodized oil (lipiodol; Laboratoire Guerbet, Roissy, France), which is a contrast agent for lymphangiography, was injected at a rate of 0.1 ml min21, not exceeding a total volume of 12 ml. Abdominal and chest radiographs were obtained 2 h later to confirm that lipiodol had been injected through the 30 gauge needle into the lymphatic vessels in all patients and to detect the chyle leakage site. Additionally, transaxial CT images without oral or intravenous contrast material were obtained 528 h (mean, 20 h) after starting the injection of contrast
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The effectiveness of lymphangiography as a treatment method

Table 1. Characteristics of each patient in whom lymphangiography was performed and the course of chyle leakage after lymphangiography
Age/ gender Cause of chyle leakage Underlying disease Leakage type Amount of drainage before lymphangiography (ml day21) Time between Usage of diagnosis and iodized oil (ml) lymphangiography Leakage site Amount of drainage the day after lymphangiography (ml day21) Time between lymphangiography and cure (days) Follow-up period (months)

1 2 3 4 5 6 7 8 9

61/M 83/F 74/M 42/Fa 34/M 53/M 55/M 71/M 55/F

Oesophagectomy Axillary lymphadectomy Idiopathic chylothorax Pelvic lymphadenectomy Retroperitoneal lymphadenectomy Aortic root replacement Oesophagectomy Oesophagectomy Oesophagectomy

Oesophageal cancer Breast cancer

Chylothorax Lymphatic fistula Chylothorax Chylous ascites Chylous ascites Lymphatic fistula Chylothorax Chylothorax Chylothorax

500 150 500 1500 1000 200 500 300 150

3 weeks 10 weeks 6 weeks 2 weeks 6 weeks 2 weeks 10 days 5 weeks 5 weeks

7 6 8 8 12 12 12 12 11

Thoracic Left axilla Thoracic Abdominal Abdominal Unknown Thoracic Unknown Thoracic

100 50 100 1500 200 200 50 50 60

14 4 21 NA 21 25 9 31 14

26 1 54 NA 3 22 11 10 17

Ovarian cancer Testicular cancer Annuloaortic ectasia Oesophageal cancer Oesophageal cancer Oesophageal cancer

M, male; F, female; NA, not applicable. a Surgical occlusion was finally performed 7 days after lymphangiography.

T Matsumoto, T Yamagami, T Kato et al

material for lymphangiography. In the first four patients, contiguous transaxial images of 10 mm thickness throughout the entire chest or abdomen were obtained with single-slice CT. In the last five patients, contiguous transaxial images of 1 mm thickness of the entire chest or abdomen were obtained with multidetector row CT. We investigated the following retrospectively: (i) the usage of iodized oil on lymphangiography, (ii) the frequency of detecting the leakage site on post-lymphangiographic abdominal or chest radiograph and postlymphangiographic CT images, (iii) the length of time between the day of lymphangiography and the day when chyle leakage disappeared, (iv) whether surgical ligation was performed after lymphangiography and (v) the duration of symptom-free follow-up in each case.

Results
Five of the nine patients underwent monopedal lymphangiography and four underwent bipedal lymphangiography.

Lymphangiography in all nine patients was successful, with no related complications. The mean amount of iodized oil used was 9.8 ml (range, 612 ml). In 7 of the 9 (78%) patients, we could detect the chyle leakage sites on both the post-lymphangiographic abdominal or chest radiographs and the postlymphangiographic CT images (Figure 1). Lymphatic leakage was not identified in two of the nine patients on post-lymphangiographic abdominal or chest radiographs, or on post-lymphangiographic CT images. In 7 of the 9 patients (78%), the daily amount of drainage decreased the day after lymphangiography. For this reason, conservative treatment was continued in the seven patients. In one of the remaining two patients, the daily amount of drainage remained the same on the day after lymphangiography (Case no 6), but conservative treatment was continued because the daily amount of chyle leakage was relatively small. The daily amount of drainage began to decrease and reached 70 ml day21 10 days after lymphangiography, and then finally stopped. 8 of the 9 patients (89%) needed no surgical reintervention and lymphatic leakage stopped after

Figure 1. A 55-year-old woman with chylothorax after oesophagectomy (Case 9). (a) Post-lymphangiographic chest radiograph
shows abnormal contrast pooling below the bifurcation of the trachea (arrows). (b) Post-lymphangiographic unenhanced CT image revealed abnormal contrast pooling in the posterior mediastinal space between Th6 and Th7 (arrowheads) and communication between the left the pleural space and lymphatic system at the superior border of Th7 vertebrae (arrow). (c) Enhanced CT image obtained 2 months after lymphangiography shows no fluid collected in the pleural space and an encapsulated cystic mass containing some contrast agent peripherally in the posterior mediastinal space at the ventral site of the thoracic vertebrae (arrow). The area of the encapsulated cystic mass is consistent with the area of leakage from the lymphatic system, as shown on previous lymphangiography.

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The effectiveness of lymphangiography as a treatment method

lymphangiography. The mean length of time between the day of lymphangiography and the day when chyle leakage disappeared was 17 days (range, 431 days) (Table 1). The mean duration of follow-up was 18 months (range, 154 months). No cases had a recurrence of chyle leakage during follow-up. One patient needed surgical ligation because the daily amount of drainage remained at more than 1500 ml for 7 days after lymphangiography.

Discussion
Chyle leakage may manifest clinically as chylothrax, chylous ascites, chyluria or lymphatic fistulae. There are multiple causes of chyle leakage, such as lymphoma, surgery, tuberculosis, radiation, sarcoidosis and lymphangiomatosis [38]. Loss of chyle can be life-threatening because of the significant loss of fluid, plasma protein, fats and immunoregulatory lymphocytes, and exhibits clinical features of severe malnutrition, hyponatraemia, acidosis, hypocalcaemia and susceptibility to infection [911]; therefore, mortality is high in patients with uncontrolled or untreated chyle leakage. There are two major classes of treatment for chyle leakage: conservative treatment and surgical intervention. Conservative treatment includes a low-fat mediumchain triglyceride diet, total parenteral nutrition and drainage of chyle leakage [1215]. In addition, somatostatin treatment [1618] and percutaneous embolisation [1921] can be included. If chyle leakage cannot be controlled with conservative treatment, surgical intervention should be adopted. Surgical intervention is usually indicated when the chyle drainage rate is more than 1 l day21 for a period of more than 5 days [22]. Lymphangiography has been used in pre-operative studies to help delineate the anatomy of the lymphatic channels and the leakage site [23]. The usefulness of post-lymphangiographic CT images is controversial. Sachs et al [24] reported that the leakage site of the thoracic duct could be diagnosed and localized accurately with lymphangiography, but that post-lymphangiographic CT was of little additional value in diagnosis. Conversely, Guermazi et al [1] reported that postlymphangiographic CT was useful for determining the exact level of chyle leakage or for demonstrating communication between the pleural space and lymphatic system by revealing lymphangiographic contrast material within the pleural space. Recently, it was suggested that lymphangiography could be a therapeutic tool for the treatment of chyle leakage. Yamagami et al [2] reported a case in which chyle ascites after retroperitoneal surgery was refractory to conservative therapy but disappeared spontaneously after lymphangiography. The speculated mechanism of attenuation of chyle leakage was thought to be as follows. Firstly, lipiodol infused during lymphangiography accumulated at the point of leakage outside the lymphatic vessel. Secondly, a regional inflammatory reaction occurred in the soft tissue adjacent to the area of lipiodol retention. Thirdly, the point of leakage of the lymphatic vessel was obstructed. Finally, lipiodol retention inside the lymphatic vessel on the distal side of the point of leakage played a role as a therapeutic embolic
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agent, as was demonstrated by the fact that lipiodol did not advance beyond that point on a radiograph obtained 1 day after lymphangiography. In addition, compression by the cystic mass formed from the leaked chyle may have influenced the obstruction at the point of leakage of the lymphatic vessel. In our study, we performed lymphangiography for all 9 patients with damage to lymphatic vessels, and in 7 of the 9 (78%) patients we could detect the sites of chyle leakage. In the remaining two patients in whom lymphatic leakage was not identified, we speculated that we could not visually detect leakage sites because they had only minimal injury to the lymphatics. Although it might have been more logical to cannulate the lymphatics in the hand or forearm in Case 2, as listed in Table 1, the leakage site in the left axilla was identified on pedal lymphangiography. It was speculated that lymph flowed from the thoracic duct to the arm lymphatics because of continuous negative pressure by a drainage tube, although its flow was not physiological. In fact, we obtained the expected result that the daily amount of drainage decreased the day after lymphangiography. The daily amount of drainage began to decrease the day after lymphangiography in 78% of patients; lymphatic leakage finally stopped by continuing conservative treatment, thus avoiding surgical reintervention in 89% of patients. This confirmed that lymphangiography might play an important role not only in the diagnosis but also in conservative therapy for chyle leakage. It can be suggested from the results of the present study that lymphangiography is effective not only in the diagnosis and identification of leakage sites but also in their treatment. Early lymphangiography is recommended for patients with chyle leakages who are unlikely to be cured by conservative treatment only. A limitation of this study is its small patient number. Eight patients had chyle leakages secondary to surgery. Only one patient had an idiopathic leak. No patients with chyle leakages due to other causes (e.g. malignancy) were present in this population. To obtain conclusive information, a larger study with a more heterogeneous population is obviously necessary as the next step.

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