Cisterna Chyli Ablation with Thoracic Duct Ligation for Chylothorax: Results in Eight Dogs
Abstract
Objective— To report use of combined cisterna chyli ablation (CCA) and thoracic duct ligation (TDL) for treatment of spontaneously occurring chylothorax in dogs.
Study Design— Retrospective study.
Animals— Eight dogs with chylothorax.
Methods— TDL was performed through a right caudal intercostal thoracotomy and CCA through a left flank paracostal approach or ventral median celiotomy. Long-term outcome (range, 2–48 months; median, 11.5 months) was evaluated by telephone communication with owners.
Results— Seven dogs were free of clinical signs related to chylothorax at last follow-up (range, 4–48 months; median, 15.5 months). One dog was euthanatized 2 months after surgery because of lack of improvement. No major complications occurred from CCA.
Conclusion— CCA and TDL resolved chylothorax in most dogs (88%).
Clinical Relevance— CCA combined with TDL may improve the outcome of chylothorax in dogs.
INTRODUCTION
CHYLOTHORAX IS a devastating condition that affects dogs and cats of any age, sex, size, and breed. Chylothorax develops when chyle gains access to the pleural space, presumably because of leakage from the intrathoracic thoracic duct lymphatic system. The therapeutic strategy for treatment of chylothorax is based on its cause, physical status of the patient, and the advantages and limitations of the treatment approach. Chylothorax can occur after trauma but in animals more commonly occurs spontaneously without known trauma. When a putative cause is identified, such as an intrathoracic mass, a heartworm infestation, heart failure, infectious agents, or pancreatic disease, treatment is directed at the presumptive underlying cause. In most animals the cause is not apparent, so the disease is considered idiopathic. Numerous dietary, medical, and surgical treatment options have been described for idiopathic chylothorax in dogs and cats.1–7
When the animal is unresponsive to conservative treatment, surgical options like thoracic duct ligation (TDL) or embolization, pleurodesis, pleurovenous shunting, pleuroperitoneal shunting, thoracic omentalization, and pericardiectomy have been proposed. Of these, TDL is the most commonly performed procedure1; although, more recently, pericardectomy has been proposed for the treatment of chylothorax.8
The rationale for TDL is based on the hypothesis that chylothorax occurs because of leakage from the thoracic duct, most likely because of terminal obstruction of the thoracic duct with subsequent lymphangiectasis or from pathologic changes in duct permeability.2,3 Ligation of the caudal portion of the thoracic duct blocks the flow of chyle to the area of leakage and ideally results in the formation of new lymphaticovenous anastomoses within 5–14 days, permanently diverting chyle away from the thoracic duct and thoracic cavity.1 Although TDL is believed to be the most effective procedure, complete resolution of chylothorax is only obtained in 50–60% of dogs,4 even when lymphangiography, before and after ligation, is performed to ensure a complete ligation of all channels of the thoracic duct.4,5 Alternative methods such as en bloc ligation of all structures in the caudal mediastinum dorsal to the aorta,6 or obstruction of the thoracic duct by embolization with a mixture of isobutyl 2-cyanoacrylate and iophendylate injected through a cannulated mesenteric lymphatic vessel7 have been described, but they have not improved on the efficacy of TDL in achieving resolution of chylothorax.
The cause for the frequent failure of TDL is unknown. Hypotheses regarding failure include the formation of collateral lymphatics that bypass the ligature site instead of the desired formation of new lymphaticovenous drainage routes outside the thoracic cavity and the failure to ligate all channels of the thoracic duct at surgery. Collateral lymphatics may potentially be stimulated by the development of caudal thoracic duct and cisterna chyli hypertension from the ligature-induced obstruction of the thoracic duct. Observation of distension of the thoracic duct and cisterna chyli after ligation supports this theory although objective measurements of changes in lymphatic pressure after TDL have not been reported. In theory, lymphatic hypertension, induced by TDL caudal to the ligation site, could be a primary stimulus resulting in lymphangiectasis with development of collateral lymphatics and promote recurrence of chylothorax.9
The cisterna chyli is an elongated saccular reservoir receiving lymph from the lumbar and mesenteric lymphatic trunks that then empties into the thoracic duct, approximately at the level of the dorsal diaphragm. We hypothesized that concurrent ablation of the cisterna chyli, along with TDL, would impact the proposed pathogenesis of chylothorax recurrence in several ways and better promote resolution of chylous pleural effusion. First, cisterna chyli ablation (CCA) would relieve any putative lymphatic hypertension and, at least transiently, remove this hypothesized stimulus for development of collateral lymphatics around the TDL site during the critical period of healing when new lymphaticovenous anastomoses are forming. Further, ablation of the connections between the source of the chyle and thoracic duct forces the disrupted lymphatic channels to form new drainage connections at the site of the lymphatic ablation, outside of the thoracic cavity, and thus may prevent chyle accumulation in the thorax. This procedure was first successfully performed in a cat with idiopathic chylothorax in 1997 (J.F. McAnulty, unpublished results) and subsequently applied to the dog. A recent experimental study has demonstrated that these hypothesized effects on chylous drainage do occur after CCA combined with TDL (CCA–TDL) in normal dogs.10 Our purpose was to report preliminary clinical evidence on the efficacy of this surgical treatment approach for the resolution of spontaneously occurring idiopathic chylothorax in dogs.
MATERIALS AND METHODS
Animals
Eight dogs, diagnosed (1999–2003) with idiopathic chylothorax, had CCA–TDL. All dogs had clinical signs related to chylothorax: abnormal breathing with radiographic evidence of pleural effusion, without any history of trauma or evidence of intrathoracic neoplasia. Diagnosis was confirmed by chemical analysis of the relative concentrations of triglycerides and cholesterol in the pleural fluid in comparison to serum.11 Cytologic examination and bacterial culture of the pleural fluid were performed. Two dogs had been administered variable doses of benzopyrone for 1 month (dog 5) and for 14 days (dog 7) before surgery. Dog 3 had been administered benzopyrone at various doses for 5 months and a somatostatin analogue (octreotide) at various doses for 10 days before surgery without improvement in chylous fluid accumulation. All dogs had an ECG and echocardiogram, and abnormal findings were noted (Table 1).
| Dog | Signalment | PreOperative Findings Other Than Chylothorax | Time After CCA–TDL | Postoperative Course | Outcome |
|---|---|---|---|---|---|
| 1 | 9 years F/S, Golden Retriever | No significant findings | 3–5 days | Pancreatitis, no pleural fluid | |
| 14 days | Bile duct obstruction, cholecystojejunostomy | ||||
| 36 months | No pleural fluid, no clinical signs | Excellent | |||
| 2 | 9 years F/S, Standard Poodle | Tricuspid regurgitation | 2 months | Multiple thoracocentesis (every 8–10 days); no improvement | Euthanatized |
| 3 | 1.5 years M, Mastiff | Tricuspid regurgitation, hypertension | 14 days | Abdominal fluid accumulation; resolved without intervention | |
| 16 months | No pleural fluid, no clinical signs | Excellent | |||
| 4 | 3 years F, Saint Bernard | No significant findings | 15 months | No pleural fluid, no clinical signs | Excellent |
| 5 | 5 years M/N, Borzoi | Hypertension; right middle lung lobe torsion; lung lobectomy 25 days prior to CCA-TDL | 7, 13, 17 days | Thoracocentesis | |
| 5 months | No pleural fluid; sudden death, cause unknown | Death; resolved chylothorax | |||
| 6 | 7 years M/N, Rhodesian Ridge Back | No significant findings | 14 days | Thoracocentesis | |
| 8 months | No pleural fluid, no clinical signs | Excellent | |||
| 7 | 4 years M/N, Border Collie | No significant findings | 4 months | No pleural fluid, no clinical signs | Excellent |
| 8 | 7 years F/S, Shetland Sheep Dog | No significant findings | 48 months | No pleural fluid, no clinical signs | Excellent |
- F/S, female spayed; F, female; M, male; M/N, Male neutered; CCA–TDL, cisterna chyli ablation-thoracic duct ligation.
CCA–TDL procedure
The first 7 dogs had lymphangiography and CCA performed through a left flank paracostal incision. In dog 8, a median celiotomy was used because it provided superior exposure of the surgical sites. Lymphangiography was performed using digital subtraction radiography. Lymphangiography was facilitated by the injection of a mesenteric lymph node with 0.5–1 mL methylene blue dye (USP) to facilitate identification of the lymphatics followed by cannulation of a visible mesenteric lymphatic channel for injection of contrast (Hypaque, Amersham Health, Princeton, NJ, USA, diluted 50% with 0.9% saline [NaCl] to reduce viscosity; 3–10 mL/injection; 300–400 mg/kg maximum dose). Each dog had 2–4 lymphangiograms during surgery, the number depending on the quality of the studies obtained and the need for additional radiographic views. The follow-up injection of methylene blue facilitated dissection of the cisterna chyli and thoracic duct. A lymphangiogram was performed after TDL, but before CCA, to confirm complete TDL.
TDL, using 2 ligatures of 5-0 polypropylene, was performed through a caudal right lateral thoracotomy incision (either 9th, 10th, or 11th intercostal space). Through the abdominal incision, the cisterna chyli was exposed by incision of the peritoneum lateral to the left kidney and elevation of the kidney and perirenal fat to expose the aorta with its intimate association with the cisterna chyli. CCA was achieved by the sharp excision of all visible cisternal membranes as well as any visible lymphatic connections to the cranial cisterna chyli or caudal thoracic duct at the level of the diaphragm. In the first 7 dogs, the CCA site was packed with omentum that was tacked into place using 3-0 polyglyconate sutures. This omentalization step was subsequently abandoned based on results obtained in a controlled experimental study.10 A chest tube was then placed, and the incisions closed. Dogs were administered supportive and analgesic therapy. Chest tubes were removed within 2 days, and thoracocentesis, pleural fluid analysis, and thoracic radiography were performed when indicated. Clinical outcomes were evaluated by recheck examination when feasible and by telephone communication with the owner and referring veterinarian.
RESULTS
Lymphangiography revealed 1–3 channels of the thoracic duct at the ligation. Follow-up intraoperative lymphangiograms after TDL showed a complete obstruction of flow of chyle in 7 dogs. In the other dog, further exploration revealed a channel of the thoracic duct on the left lateral surface of the aorta. After ligation of this channel, a complete obstruction of chyle flow was confirmed by radiography.
Duration between onset of clinical signs and surgery was 10–330 days (median, 30 days). Mean dog age (±SD) at surgery was 6.0±2.7 years (Table 1), and mean body weight was 30.1±20.4 kg. Preoperative cardiology examination revealed tricuspid regurgitation in 2 dogs (dogs 2 and 3) and hypertension in 2 dogs (dogs 3 and 5; Table 1). Dog 5 had right lateral thoracotomy and right middle lung lobectomy for lung lobe torsion with concurrent chylothorax 25 days before CCA–TDL.
Chylous pleural effusion was resolved at the time of death or at follow-up (range, 2–48 months; median, 11.5 months; mean, 16.8±16.6 months) in 7 dogs. Dogs 2 and 5 required multiple thoracocenteses because of recurrence of clinical signs after hospital discharge. Dog 2 required thoracocentesis every 8–10 days for 2 months until euthanasia was requested by the owner because of lack of improvement. Dog 3 had an abdominal chylous effusion noted at 5 days postoperatively but showed no ill effects and the effusion resolved without intervention. Dog 5 required thoracocentesis every 7 days for 1 month, after which no clinical signs were noted for the next 4 months. This dog died suddenly 5 months postoperatively after coughing up a blood clot; necropsy was not performed.
In the 6 long-term survivors, there were no clinical signs related to chylothorax and thoracocentesis was not required (range, 4–48 months; median, 15.5 months; mean, 21.3±16.9 months; Table 1). Four dogs were not administered any medication for chylothorax during the follow-up period. Dog 3 was administered a somatostatin analogue (octreotide) for 1 week postoperatively at the clients request. Dog 1 was treated for pancreatitis and had cholecystojejunostomy for bile duct obstruction secondary to pancreatitis, 14 days after CCA–TDL. Dog 3 was examined for peripheral edema at 17 days but no treatment was required. On recheck radiography (dog 4, 4 months; dog 3, 5 months, dog 1, 8 months) there was no pleural effusion. In a telephonic follow-up, owners of the surviving dogs rated the outcome as excellent.
DISCUSSION
Our results from this preliminary clinical study suggest that CCA in combination with TDL improved outcome for treatment of idiopathic chylothorax in dogs. Resolution of chylothorax occurred in 7 dogs (88%). Long-term survival occurred in 6 dogs with 1 dog dying of an acute event, seemingly unrelated to chylothorax or CCA but which was not confirmed by necropsy. Although our case numbers were small, our outcome for resolution of chylothorax in dogs appears to be substantially better than the reported success rate with TDL alone4 and provides encouraging evidence to support a larger controlled clinical trial to determine CCA–TDL efficacy.
TDL, the most commonly performed surgical procedure for chylothorax, can potentially cause lymphatic hypertension in lymphatics caudal to the ligation site. This consequence supported by readily observable distension of the caudal duct after ligation has not been measured. One hypothesis for failure of TDL alone is that this lymphatic hypertension presents a stimulus for the development of collateral lymphatics, which may bypass the ligation site, to reestablish the flow of chyle and chylous fluid accumulation within the thorax. The rationale for our clinical study was based on the hypothesis that CCA both relieves lymphatic hypertension in the caudal thoracic duct and promotes new routes of lymphatic drainage within the abdominal cavity.
In the short term, while new venous connections for lymph drainage are being formed, the abdominal cavity may be more tolerant to chylous fluid accumulation because accumulation of substantial volumes of fluid in the abdomen has no life-threatening consequence, in contrast to its effect in the pleural space. Only 1 of our dogs had substantial abdominal chylous effusion, detected by abdominal distension and confirmed by paracentesis, and the effusion resolved without further treatment. It seems likely that all dogs had some degree of chyloabdomen after CCA; however, this was not externally apparent and thus was not pursued by diagnostic testing.
The abdomen may also provide more sites for lymphatic to venous anastomoses, compared with the thoracic cavity. In an experimental study in normal dogs, we showed that combining CCA with TDL resulted in formation of lymphaticovenous connections in the mesentery and omentum, and in direct connections to large abdominal veins (vena cava, phrenicoabdominal).10 Our results indicate that CCA may be similarly effective in dogs with spontaneously occurring disease.
The designation of chylothorax as idiopathic is not always clear and may confound the interpretation of results obtained in clinical studies. Chylothorax may occur because of relatively easily detectable causes, such as intrathoracic masses or heartworm disease, or it may be diagnosed in conjunction with cardiac anomalies, which may or may not play a causative role in induction of chylothorax. Thus, evaluation of the efficacy of a therapeutic procedure can be complicated by the potential for differing success rates in idiopathic chylothorax versus chylothorax secondary to heart disease or other causes. In fact, one proposed hypothesis suggests that the cause of idiopathic chylothorax is mainly cardiogenic, related to elevated systemic venous pressure.12 Thus, elevations in systemic venous pressure, secondary to right-sided congestive heart failure, tricuspid dysplasia, cardiomyopathy, or pericardial disease, may contribute to lymphatic hypertension and chylothorax.13 However, objective data to support this hypothesis have not been reported. Further, this hypothesis does not address the reasons why myriad patients with heart failure do not develop chylothorax, an observation that would suggest that other factors must be involved, possibly in conjunction with heart disease.
In our cases, 3 dogs had a cardiovascular disease related to either tricuspid regurgitation or hypertension. Thus, it might be argued that the chylothorax may not have been idiopathic in these dogs and that they represent a subset of patients that could have a different response to CCA–TDL. Included in this subgroup were the dog that died suddenly, 5 months after surgery and 1 dog where chylothorax was not alleviated. Further, the dog that died suddenly had, on admission, recently had a lung lobe torsion (with concurrent chylothorax) 25 days before admission for CCA–TDL. Thus, in this dog it could not be determined if the chylothorax was truly idiopathic, related to cardiac disease, or if it was developed subsequent to lung lobe torsion. Regardless, the chylothorax resolved before death at 5 months postoperatively and a longer-term follow-up was not possible.
The only major perioperative complication that occurred was development of postoperative pancreatitis in dog 1. This may have been related to omentalization of the CCA site and the limited exposure provided by the abdominal approach. In this dog, CCA was performed by flank paracostal incision, an approach that limits broad exposure of the intrabdominal contents. Mobilization of the omentum proved difficult; a problem likely caused by omental adhesions from a previous ovariohysterectomy. It is feasible that excessive traction on the omental pedicle caused damage which triggered pancreatitis. Thus, because of the difficulty encountered in this dog, findings from our experimental study that did not show any drainage via the omental pedicle,10 and superior exposure obtained for lymphangiography and CCA by median celiotomy, we discontinued the practice of omentalizing the ablation site and changed our abdominal approach.
Summarizing, our results support the use of CCA–TDL for treatment of idiopathic chylothorax in the dog. CCA was relatively simple to perform without requiring special surgical settings or prolonged operative times, and no major complications were caused by this procedure. Although the results are promising, a clarification of the advantages and disadvantages of this approach to chylothorax needs to be determined in a larger population of affected dogs.
