Chylothorax in the dog and cat

Chylothorax means the accumulation of chyle (that is, lymph) in the pleural cavity. In normal conditions, the lymph passes through the cisterna chyli (retroperitoneal, ventral to the first lumbar vertebrae and medial to the hilum of the left kidney), flows through the thoracic duct (dorsal to the aorta) and finishes, through one or more branches, in the cranial vena cava or one of its tributaries. Chylothorax is a relatively rare, debilitating disease in both dogs and cats. The known causes are listed in Table 1._{^{5,7-10,12,15,17,21-26,33,39,47,50}} When all the known potential causes of chylothorax have been excluded, the condition is defined idiopathic. Idiopathic chylothorax is associated with thoracic lymphangiectasia. It has been suggested that oriental cats and the Afghan Hound are predisposed to idiopathic chylothorax.

Table 1. Possible causes of chylothorax.

CLINICAL SIGNS AND DIAGNOSIS

At presentation, which may occur as an emergency in cases of an abundant accumulation of lymph, the clinical signs are: tachypnoea, shallow and abdominal breathing, even to the point of dyspnoea with cyanosis. The animal’s owner may also report the onset of cough, present for a variable period. These signs are explained not only by the intrapleural accumulation of chyle, but also by a fibrinous serositis (pleura, pericardium) caused by the presence of the lymph itself. The pleural thickening can further limit the excursion of the lungs and is a negative prognostic factor; pericardial thickening, in its turn, if present, prevents normal diastolic filling, ultimately causing venous and, consequently, lymphatic hypertension.

As in all cases of a pleural collection, both respiratory and cardiac sounds are muffled; furthermore, the fluid accumulation can demarcate a horizontal percussion line on the thorax of a standing animal or one in sternal decubitus; at auscultation, stronger (compensatory) breaths can be heard above this line. There may also be more specific signs associated with the underlying condition (see Table 1).

A definitive diagnosis of a pleural fluid collection is obtained by: (i) X-ray films in the two standard views (lateral and dorsoventral – Figs. 1A and 1B), and (ii) direct, or, preferably, ultrasound-guided thoracentesis. Ultrasound-guided drainage of the pleural cavity is helpful if the fluid collection is abundant and the respiratory impairment severe. In this case it is also useful to supply the animal with oxygen. The aims of drainage are: (i) to enable greater expansion of the lungs, thereby giving the animal relief; (ii) to determine the characteristics of the fluid; and (iii) to visualise any intrathoracic lesions, which were previously not visible because of the presence of the fluid, by post-drainage X-rays.

The fluid removed during thoracocentesis is usually milky white (Fig. 2) and should not be confused with a purulent exudate (pyothorax), which is often slightly greenish and foul smelling. Following thoracocentesis, the fluid withdrawn is sent to the laboratory for cytological and biochemical studies. Chyle is a modified transudate with a protein content of ≥2.5 g/dL and a variable number of nucleated cells (in particular lymphocytes and whole neutrophils, but also macrophages and mesothelial cells) and red blood cells (also derived from the thoracocentesis procedure itself). The triglyceride content is high (higher than in serum) while the concentration of cholesterol is lower than that in the serum (the reverse is true for pseudochyle, thus enabling the differential diagnosis). The cholesterol/triglyceride ratio in chyle is <1. Specific stains for fats (e.g. Sudan black, which stains chylomicrons) are positive.

The results of blood tests (full blood count and biochemistry screen) are usually non-specific in idiopathic chylothorax. Mild anaemia, lymphocytopenia, electrolyte disturbances (hyperkalaemia, hyponatraemia) and hypoproteinaemia are sometimes found, especially in the case of repeated thoracocenteses. In this case there is also often variable weight loss and debilitation. In cats it is also advisable to evaluate FIV/FeLV status. More pronounced changes and/or more specific ones may be present in cases of non-idiopathic chylothorax (see Table 1).

After the thoracocentesis, X-rays taken in the standard views may reveal opacities in the anterior mediastinum, changes in the cardiac silhouette, hernias, abnormal pulmonary shadows, etc. (see Table 1).

The diagnostic protocol also includes: (i) ultrasonography to exclude congenital or acquired heart disorders, tumours of the base of the heart, pericardial effusion with or without thickening of the pericardium and constrictive pericarditis; and (ii) ultrasound examination of the anterior mediastinum to evaluate whether any mediastinal masses (lymphoma, thymoma, ectopic carcinomas of the thyroid or parathyroid, etc.) are present and to proceed, if possible, with a fine needle biopsy.

TREATMENT

The decision whether to insert a thoracostomy tube or not is influenced by: (I) the rate of accumulation of chyle in the pleural cavity; (II) any underlying disorders (treatable or not), (III) progressive debilitation of the patient following repeated drainage; and (IV) how difficult it is to manage the patient. It should be emphasized that, in the case of chylothorax, tubes must be placed bilaterally given that the thickening of the mediastinal serous membranes (Fig. 3), which are “permeable” to air and low density fluids in normal conditions, in many cases prevents drainage of both hemithoraces. However, a thoracostomy tube is not usually placed unless it has been demonstrated that the fluid collection has been caused by an iatrogenic/traumatic laceration of the thoracic duct. In this case, healing usually occurs within 1 to 2 weeks after placement of the tube._²⁹

While the treatment in cases with a known aetiology is directed at the underlying disorder (e.g. asportation of mediastinal masses – Figs. 4A and 4B, herniorraphy, pericardiectomy, pulmonary lobectomy, etc), in the case of idiopathic chylothorax the various different surgical procedures that can be used (none of which provides a definitive cure) are aimed exclusively at resolving the chylous effusion by creating an alternative drainage for the lymph.

The medical treatment of idiopathic chylothorax (which should be continued for at least 3-4 weeks) is based on a low-fat diet, repeated thoracocenteses and the administration of rutin and/or octreotide._^34,51 Medical therapy is only occasionally effective_^8,27,51 and surgery is the treatment of choice. Treatments such as pleuroperitoneal shunts,_^42,45 pleurodesis,_^1,8,30,36 embolisation of the thoracic duct with cyano-acrylate,_⁴¹ diaphragmatic fenestration and sclerotherapy (pleurodesis) are only occasionally used in veterinary medicine._¹⁶

The surgical interventions that are able to induce alternative lymphatic drainage in the venous system are:

• pre-diaphragmatic ligation of the thoracic duct with silk thread (Figs. 5A, 5B and 5C) or a vascular clip. Visualisation of the thoracic duct can be facilitated by pre- or intra-operative lymphangiography using an iodinated contrast agent or a small amount of methylene blue (Fig. 6), usually injected into a mesenteric lymphatic vessel_{^{3,4,6,8,20,22,25,33}} or into a popliteal lymph node._^18,40 In order to aid visualisation and catheterisation of a mesenteric vessel (Fig. 7) it is useful to feed the animal with a fat-rich diet for at least 24 hours to make the mesenteric lymph vessels more evident. The thoracic duct can be identified directly, that is, intra-operatively (Figs. 8A and 8B), or by radiography or computed axial tomography;_^19,31 selective ligation may be performed of the thoracic duct alone or of the duct together with its anomalous branches, which may very rarely be present ventrally to the aorta. A post-ligation lymphangiography to confirm complete ligation of the duct may be useful;

• an alternative procedure that can be used to shorten the period of anaesthesia is blunt dissection and en bloc ligation of all structures dorsal to the aorta, therefore also including the azygos vein and any aberrant branches of the thoracic duct, although avoiding the sympathetic trunk. Pre-operative lymphangiography is not necessary in this case;_^11,38,52
• subphrenic pericardiectomy (Figs. 9A and 9B ), usually performed together with ligation of the thoracic duct, in order to promote lymph flow in the cranial vena cava._²⁵ Pericardiectomy is also a rational choice in cases of pericardial thickening/constriction;_¹²

• ablation of the cisterna chyli (also associated with mesenteric lymphangiography for better visualisation – Figs. 10A and 10B). Up to now this has been considered a “salvage” procedure to be used after failure of the preceding techniques;_^28,44,4
• ligation of the duct and pericardiectomy can also be performed via thoracoscopy_^2,43 (Fig. 11) ;

•  omentalisation of the pleural space (by the transdiaphragmatic route – Fig. 12 - or transcostal approach, in this latter case after passing through appropriately created subcutaneous tunnels). This is not currently recommended as a first-line treatment;_^11,14,35,53 furthermore, it should be appreciated that in any case the omental lymphatic vessels empty into the thoracic duct;

• if appropriate, single consolidated lung lobes can be removed (Fig. 13);
• the surgical approach can be via a double lateral thoracotomy (5_^th intercostal space for the pericardium and 9_^th-10_^th for the thoracic duct, on the right in the dog and on the left for the cat), a paracostal access (for the thoracic duct and cisterna chyli_⁴⁸), or via sternotomy_¹⁴;
• before completing the surgery, a thoracostomy tube should be placed to monitor the change in the pathology (Fig. 14); the tube is usually removed within a maximum of 7-10 days.

• in some cases, a chylous effusion may resolve rapidly (within one or a few days); in other cases the effusion may remain for a variable period or continue in the form of a non-chylous sero-haemorrhagic collection, which also persists for a variable period;
• the rate of resolution of chylothorax after selective ligation (post- lymphangiography) of the thoracic duct (with or without ablation of the cisterna chyli) varies between 20% and 80%);_{^{2,6,8,21,25,26,32,46,50}}
• selective ligation of the thoracic duct associated with pericardiectomy resolves the effusion in 80-100%  of dogs and 75-80% of cats;_^2,13,25
• en bloc ligation (not selective, i.e. not preceded by lymphangiography to shorten the operating time) resolves idiopathic chylothorax in 50% of cases._^6,38,52 If this technique is combined with subphrenic pericardiectomy, the long-term cure rate is 80% in the dog and 75% in the cat;_¹¹
• contemporaneous pleural omentalisation does not currently seem to improve the success rate;_^11,49
• if the procedures listed above fail, ablation of the cisterna chyli_¹¹ and/or omentalisation can be proposed;
• recent studies indicate duct ligation and contemporaneous ablation of the cisterna chyli as a treatment of first choice

References

1. Adler, R.H., Levinsky, L., 1978. Persistent chylothorax: Treatment by talc pleurodesis. The Journal of Thoracic and Cardiovascular Surgery 76, 859-864, 1978
2. Allman, D.A., Radlinsky, M.G., Ralph, A.G., Rawlings, C.A., 2010. Thoracoscopic Thoracic Duct Ligation and Thoracoscopic Pericardectomy for Treatment of Chylothorax in Dogs. Veterinary Surgery 39, 21-27.
3. Birchard, S.J., Cantwell, H.D., Bright, R.M., 1982. Lymphangiography and ligation of the canine thoracic duct: a study in normal dogs and three dogs with chylothorax. Journal of the American Animal Hospital Association 18,769–777.
4. Birchard, S.J., Smeak, D.D., Fossum, T.W., 1988. Results of thoracic duct ligation in dogs with chylothorax. Journal of the American Veterinary Medical Association  163, 68-71.
5. Birchard S.J., Bilbrey S.A., 1990. Chylothorax associated with dirofilariasis in a cat Journal of the American Veterinary Medical Association 197(4):507-9
6. Birchard, S.J., McLoughlin, M.A., Smeak, D.D., 1995. Chylothorax in the dog and cat: a review. Lymphology28:64-72, 1995
7. Birchard, S.J., Smeak, D.D., McLoughlin, M.A. 1998 Treatment of idiopathic chylothorax in dogs and cats. Journal of the American Veterinary Medical Association 212, 652-657.
8. Bilbery, S.A., Birchard, S.J., 1994. Pulmonary lymphatics in dogs with experimentally induced chylothorax. Journal of the American Animal Hospital Association 30, 86–91.
9. Boston, S.E., Moes, N.M., Martin, D.M., 2006. Idiopathic primary chylopericardium in a dog. Journal of the American Veterinary Medical Association 229, 1930-1933
10. Bracha S, Caron I, Holmberg DL, O'Grady MR, O'Sullivan LM, Brisson BA, Stalker MJ., 2009. Ectopic thyroid carcinoma causing right ventricular outflow tract obstruction in a dog. J Am Anim Hosp Assoc.45(3):138-41.
11. Bussadori R., Provera A., Martano M., Morello E., Gonzalo-Orden J.M., Giuseppe La Rosa, Nicoli S., Repetto S.M., Zabarino S., Buracco P. Pleural omentalisation with en bloc ligation of the thoracic duct and pericardiectomy for idiopathic chylothorax in nine dogs and four cats. The Veterinary Journal 188(2):234-6, 2011.
12. Campbell, S.L., Forrester, S.D., Johnston, S.A., Jacobson, J:D., Moon, M.L., 1995: Chylothorax associatedwith constrictive pericarditis in a dog. Journal of the American Veterinary Medical Association 206, 1561-1564
13. Carobbi B, White RA, RomanelliG., 2008. Treatment of idiopathic chylothorax in 14 dogs by ligation of the thoracic duct and partial pericardiectomy. Vet Rec.2008 163(25):743-5.
14. da Silva CA, Monnet E., 2011. Long-term outcome of dogs treated surgically for idiopathic chylothorax: 11 cases (1995-2009). J Am Vet Med Assoc.239(1):107-13.
15. Diana  A., Guglielmini C., Acocella F., Cipone M., 2009. Chylothoraxassociated with tricuspid dysplasia and atrial septal defect in a bullmastiff. J Am Anim Hosp Assoc.45(2):78-83.
16. Doiguchi, O., Doiguchi, M., 2004. Effects of OK-432 treatment on the idiopathic chylothorax of a dog. Journal of the Japan Veterinary Medical Association 57, 381-385.
17. Donahoe JM, Kneller SK, Thompson PE. Chylothoraxsubsequent to infection of cats with Dirofilaria immitis.J Am Vet Med Assoc. 1974 Jun 1;164(11):1107-10.
18. Enwiller, T.M., Radlinsky, M.G., Mason, D.E., Roush J.K., 2003. Popliteal and mesenteric lymph node injection with methylene blue for coloration of the thoracic duct in dogs. Veterinary Surgery 32, 359-364.
19. Esterline, M.L., Radlinsky, M.G., Biller, D.S., Mason, D.E., Roush, J.K., Cash, W.C., 2005.  Comparison of radiographic and computed tomography lymphangiography for identification of the canine thoracic duct. Veterinary Radiology & Ultrasound46, 391-5.
20. Fossum, T.W., Birchard, S.J., 1986. Lymphangiographic evaluation of experimentally induced chylothorax after ligation of the cranial vena cava in dogs. American Journal of Veterinary Research47, 967-971.
21. Fossum, T.W., Birchard, S.J., Jacobs, R.M., 1986a. Chylothorax in 34 dogs. Journal of American Veterinary Medical Association 188, 1315-1318.
22. Fossum, T.W., Forrester, S.D., Swenson, C.L., Miller, M.W., Cohen, N.D., Boothe, H.W., Birchard, S.J., 1991. Chylothorax in cats: 37 cases (1969-1989). Journal of the American Veterinary Medical Association 198, 672-678.
23. Fossum, T.W., Evering, W.N., Miller, M.W., Forrester, S.D., Palmer, D.R., Hodges, C.C., 1992.Severe bilateral fibrosing pleuritis associated with chronic chylothorax in five cats and two dogs. Journal of the American Veterinary Medical Association 201, 317-324.
24. Fossum, T.W., Miller, M.W., Rogers, K.S., Bonagura, J.D., Meurs, K.M., 1994. Chylothorax associated with right-sided heart failure in five cats. Journal of the American Veterinary Medical Association204, 84-89.
25. Fossum, T.W., Mertens, M.M., Miller, M.W., Peacock, J.T., Saunders, A., Gordon, S., Pahl, G., Makarski, L.A., Bahr, A., Hobson, P.H., 2004. Thoracic duct ligation and pericardectomy for treatment of idiopathic chylothorax. Journal of Veterinary Internal Medicine 18, 307-310.
26. Fossum, T.W., 2009. Chylothorax: When surgery is indicated? In: Proceedings of the 18^th Annual Scientific Meeting of the European College of Veterinary Surgeons, Nantes,France, pp 473-477
27. Gould, L., 2004. The medical management of idiopathic chylothorax in a domestic long-haired cat. The Canadian Veterinary Journal 45, 51-4.
28. Hayashi, K., Sicard, G., Gellasch, K., Frank, J.D., Hardie, R.J., McAnulty, J.F., 2005. Cisterna chili ablation with thoracic duct ligation for chylothorax: results in eight dogs. Veterinary Surgery 34, 519-523.
29. Hodges CC, Fossum TW, Evering WL, 1993. Evaluation of thoracic duct healing after experimental laceration and transection. Veterinary Surgery 22:431, 1993.
30. Jerram, R.M., Fossum, T.W., Berridge, B.R., 1999. The efficacy of mechanical abrasion and talc slurry as methods of pleurodesis in normal dogs. Veterinary Surgery 28, 322-332.
31. Johnson, E.G., Wisner, E.R., Kyles, A., Koehler, C., Marks, S.L., 2009. Computed tomographic lymphography of the thoracic duct by mesenteric lymph node injection. Veterinary Surgery 38, 361-367.
32. Kagan, K.G., Breznock, E.M., 1979. Variations in the canine thoracic duct system and the effects of surgical occlusion demonstrated by rapid aqueous lymphography, using an intestinal lymphatic trunk. American Journal of Veterinary Research 40, 948–958.
33. Kerpsack, S.J., McLoughlin, M.A., Birchard S.J., Smeak, D.D., Biller, D.S., 1994. Evaluation of mesenteric lymphangiography and thoracic duct ligation in cats with chylothorax: 19 cases (1987-1992). Journal of Veterinary Internal Medicine 205: 711-715.
34. Kopko, S.H., 2005. The use of rutin in a cat with idiopathic chylothorax. The Canadian Veterinary Journal 46, 729-731.
35. Lafond, E., Weirich, W.E., Salisbury, S.K., 2002. Omentalization of the thorax for treatment of idiopathic chylothorax with constrictive pleuritis in a cat. Journal of the American Animal Hospital Association 38, 74-78.
36. Laing, E.J., Norris, A.M., 1986. Pleurodesis as a treatment for pleural effusion in the dog. Journal of the American Animal Hospital Association 22, 193–196, 1986.
37. McAnulty JF., 2011. Prospective comparison of cisterna chyli ablation to pericardectomy for treatment of spontaneously occurring idiopathic chylothorax in the dog. Vet Surg.40(8):926-34.
38. Monnet, E., 2003. Pleura and pleural space. In: Slatter, D. (Ed.), Textbook of Small Animal Surgery(third edition), Vol. 1. Saunders, PhiladelphiaPA, USA, pp. 387-405
39. Mulz JM, Kraus MS, Thompson M, Flanders JA., 2010. Cranial vena caval syndrome secondary to central venous obstruction associated with a pacemaker lead in a dog. J Vet Cardiol.12(3):217-23.
40. Naganobu, K., Ohigashi, Y., Akiyoshi, T., Hagio, M., Miyamoto, T., Yamaguchi, R., 2006. Lymphography of the thoracic duct by percutaneous injection of iohexol into the popliteal lymph node of dogs: experimental study and clinical application. Veterinary Surgery 35, 377-381.
41. Pardo, A.D., Bright, R.M., Walker, M.A., Patton, C.S., 1989. Transcatheter thoracic duct embolization in the dog. An experimental study. Veterinary Surgery 18, 279-285
42. Peterson, S.L., Pion, P.D., Breznock, E.M., 1989. Passive pleuroperitoneal drainage for management of chylothorax in two cats. Journal of the American Animal Hospital Association 25, 569–572
43. Radlinsky, M.G., Mason, D.E., Biller, D.S., Olsen, D., 2002. Thoracoscopic visualization and ligation of the thoracic duct in dogs. Veterinary Surgery 31, 138-146.
44. SchmiedtCW, Washabaugh KF, Rao DB, Stepien RL., 2009. Chylothorax associated with a congenital peritoneopericardial diaphragmatic hernia in a dog.Journal of the American Animal Hospital Association 45(3):134-7.
45. Smeak, D.D., Birchard, S.J., McLoughlin, M.A., Lindsey, M.M., Holt, D.E., Caywood, D.D., Downs, M.O., 2001. Treatment of chronic pleural effusion with pleuroperitoneal shunts in dogs: 14 cases (1985-1999). Journal of Veterinary Internal Medicine 219: 1590-1597, 2001.
46. Sicard, G.K., Waller, K.R., Mcanulty, J.F., 2005. The effect of cisterna chyli ablation combined with thoracic duct ligation on abdominal lymphatic drainage. Veterinary Surgery 34, 64-70
47. Singh A, Brisson BA., 2010. Chylothorax associated with thrombosis of the cranial vena cava. Can Vet J.51(8):847-52.
48. Staiger BA, Stanley BJ, McAnulty JF., 2011. Single paracostal approach to thoracic duct and cisterna chyli: experimental study and case series. Vet Surg.40(7):786-94.
49. Stewart K, Padgett S., 2010. Chylothorax treated via thoracic duct ligation and omentalization. J Am Anim Hosp Assoc.46(5):312-7.
50. Suter, P.F., 1984. Thoracic Radiography. In: Suter, P.F. (Ed.), A Text Atlas of Thoracic Diseases of the Dogs and Cats. Suter P.F.,Wettswill, Switzerland, p 723
51. Thompson, M.S., Cohn, L.S., Jordan, R.C., 1999. Use of rutin for medical management of idiopathic chylothorax in four cats. Journal of American Veterinary Medical Association 215, 345–348.
52. Viehoff,  F.W., Stokhof, A. A., 2003. En bloc ligatie van de ductus thoracicus bij twaalf honden met idiopatische chylothorax. Tijdschr Diergeneeskd128, 278-283.
53. Williams, J.M., Niles, J.D., 1999. Use of omentum as a physiologic drain for treatment of chylothorax in a dog. Veterinary Surgery 28, 61-65.