Omentalization of the Thorax for Treatment of Idiopathic Chylothorax With Constrictive Pleuritis in a Cat

Introduction

Chylothorax is an infrequently encountered condition in cats and dogs in which chyle accumulates within the thoracic cavity. The condition can pose a therapeutic challenge, as the pathophysiology of chylothorax in cats and dogs is poorly understood. Early reports of the disease suggested that chylothorax most commonly resulted from a defect in the thoracic duct, usually secondary to trauma.^1–5 Recent research has challenged this conjecture,^6–8 and for the majority of cases of chylothorax, an underlying disease process is never identified, and the condition is considered idiopathic.⁹ Studies of clinical and experimental chylothorax have revealed lymphangiectasia of mediastinal and pleural lymphatics.⁷⁸ The authors of these studies postulated that partial obstruction of the thoracic duct at the lymphaticovenous angle may cause diffuse lymphangiectasia, with subsequent seepage of chyle into the pleural space.

The mainstay of surgical treatment for idiopathic chylothorax has been the identification and ligation of the thoracic duct in the caudal aspect of the thoracic cavity. Thoracic duct ligation has a reported success rate of no more than 59% in dogs and substantially less in cats.^9–11 This less-than-ideal success rate with thoracic duct ligation has prompted the development of numerous additional surgical techniques for the treatment of refractory chylothorax in both dogs and cats.^12–16 No long-term studies, however, compare the success rates for any of these techniques with that of thoracic duct ligation. In a recent case report of idiopathic chylothorax in a dog, the authors used an omentalization technique to treat chylothorax that was refractory to medical management and in which thoracic duct ligation could not be performed.¹⁷ The success of omentalization in the dog of that report suggests that the omentalization technique may hold promise for successful management of refractory chylothorax.

The case reported herein describes the use of an omental advancement technique to successfully treat a cat with idiopathic chylothorax and concurrent, severe, constrictive pleuritis. To the authors’ knowledge, this is the first report of omentalization of the thorax used for a cat with idiopathic chylothorax.

Case Report

A 6-year-old, 2.9-kg, spayed female Himalayan cat was referred to the Purdue University Veterinary Teaching Hospital (PU-VTH) with a 2-month history of persistent pleural effusion, tachypnea, weight loss, and progressive anorexia. There was no history of prior illness or trauma. Diagnostic tests performed by the referring veterinarian included hematology, serum biochemical analysis, enzyme-linked immunosorbent assay test for feline leukemia virus, immunofluorescent antibody test for feline immunodeficiency virus, serum thyroxine concentrations (T₃ and T₄), thoracic radiography, and cardiac and thoracic ultrasonography. All tests were unremarkable with the exception of lymphopenia (616 lymphocytes/μL; reference range, 1.2 to 8.0 × 10³ lymphocytes/μL), low serum alkaline phosphatase (7 IU/L; reference range, 10 to 100 IU/L), low serum triglyceride concentration (23 mg/dL; reference range, 25 to 81 mg/dL), and the identification of pleural effusion on radiography. Previous therapy included intermittent thoracocentesis and a low-fat diet.^a

At presentation to the PU-VTH, the cat was tachypneic (respiratory rate, 66 breaths per minute [bpm]), underweight (body condition score, 2.5 out of 5; normal, 3¹⁸), and had harsh lung sounds bilaterally. Rectal temperature was 39.1°C. All other aspects of the physical examination were unremarkable. Thoracic radiographs revealed bilateral pleural effusion, which was worse in the left hemithorax. Thoracocentesis revealed a milky, opaque fluid, with a triglyceride concentration of 469 mg/dL (serum triglyceride concentration, 46 mg/dL) and a cholesterol concentration of 45 mg/dL (serum cholesterol concentration, 98 mg/dL). Cytopathology of the pleural fluid revealed small lymphocytes as the predominant cell type. There was no growth upon aerobic and anaerobic bacterial culture of a sample of the pleural fluid. Hematology was characterized by lymphopenia (640 lymphocytes/μL; reference range, 1.0 to 7.0 × 10³ lymphocytes/μL), with reactive lymphocytes noted. Heartworm antibody test was negative. Repeat cardiac and thoracic ultrasound examinations showed no evidence of underlying disease processes. A diagnosis of idiopathic chylothorax was made based on the characteristics of the pleural fluid and the inability to identify an underlying cause for the chylous effusion. The owner elected to treat the cat medically, and the cat was discharged from the hospital. The owner was instructed to feed the cat a low-fat diet^a and administer rutin^b (150 mg per os [PO], bid). Thoracocentesis was to be performed by the referring veterinarian as needed.

The cat responded poorly to medical management; she refused to eat the low-fat diet and was difficult to medicate. She presented again to the PU-VTH after 14 days of medical management. She was still tachypneic (respiratory rate, 60 bpm) and had required thoracocentesis by the referring veterinarian; between 25 and 45 mL of fluid was drained from the pleural cavity approximately every 4 days to alleviate signs of respiratory distress. The owner elected surgical therapy at this time.

Two hours prior to anesthesia, 2 mL/kg body weight of heavy cream was fed PO to aid in the delineation of the lymphatic vessels. An exploratory thoracotomy was performed at the left ninth intercostal space. The entire hemithorax was filled with chylous fluid, including flecks of inspissated, chylous-appearing material. The volume of fluid was not measured but was estimated to be approximately 25 mL. The left lung lobes were not visible but were entrapped medially to a thick, fibrous membrane that was parallel to and lateral to the mediastinum (i.e., constrictive pleuritis). Decortication of the membrane was performed by carefully removing the thickened membrane from the underlying pulmonary parenchyma. The membrane was closely adhered to the parenchyma and did not separate easily. Because of the difficulty separating the membrane from the parenchyma, only about 25% of the visible membrane was removed, allowing an estimated 50% increase in pulmonary expansion [Figure 1]. Intraoperatively, no air leakage was detected. Attempts were made to identify and ligate the thoracic duct in the caudodorsal mediastinum; however, it was not visualized. The decision was made to perform a transdiaphragmatic omental advancement as previously described in a dog.¹⁷ A left paracostal celiotomy was performed, and the omentum was identified. The omentum was advanced into the thoracic cavity through a 1-cm defect created in the diaphragm, approximately 2 cm medial and ventral to the left crus. No attempt was made to divide the dorsal and ventral leaves of the omentum or to create a pedicle, because the omentum easily extended to the cranial aspect of the thoracic cavity. The omentum was advanced cranial to the heart and was sutured to the mediastinum dorsally and ventrally with simple interrupted sutures of 4-0 polydioxanone^c to ensure that the omentum would remain in contact with as much of the pleural surface as possible. The thoracic and abdominal incisions were closed routinely after placement of a 12-French thoracostomy tube. Antibiotic therapy (cefazolin,^d 22 mg/kg body weight, intravenously [IV]) was instituted intraoperatively and was continued tid during the postoperative period.

Postoperatively, a large amount of air was evacuated from the thorax via the thoracostomy tube, necessitating continuous thoracic drainage.^e During the first postoperative day, a total of approximately 40 mL of chylous fluid was evacuated from the thoracic cavity. The pleural fluid that was evacuated decreased steadily in volume over the following 3 days and became serosanguineous in character; however, fluid triglyceride and cholesterol concentrations were not measured. Less than 1 mL of fluid was aspirated on the fifth postoperative day. Pneumothorax resolved within 72 hours postoperatively, and the chest tube was removed on the fifth postoperative day. Because intermittent pyrexia began on the fourth postoperative day (peak rectal temperature, 39.8°C), the tip of the thoracostomy tube was submitted for microbiological testing after removal. Bacterial culture yielded no growth on enriched medium. The cat was released from the hospital 8 days after surgery, with no dietary restrictions and no medications other than cefadroxil^f (22 mg/kg body weight, PO tid for 1 week). The respiratory rate at rest at the time of discharge from the hospital was 44 to 56 bpm, and the rectal temperature was 39.3°C. Based on the cat’s clinical status and because of the difficulty administering oral medication to the cat, long-term recommendations for rutin therapy were not made.

Twenty-two days postoperatively, reexamination revealed persistent tachypnea (respiratory rate, 60 bpm), although the owner reported lower respiratory rates (36 to 54 bpm) at home. The cat was still underweight but was reportedly eating a feline maintenance diet^g well. Hematology and serum biochemical analysis revealed neutropenia (neutrophils, 2.67/μL; reference range, 3.0 to 12.0 × 10³/μL) and lymphopenia (lymphocytes, 710/μL). All other parameters were within reference ranges. Fifty days postoperatively, the owner reported that the cat had near normal respiratory rates (24 to 36 bpm) at home, normal activity, and a normal appetite. Upon reexamination, neutrophil and lymphocyte counts had returned to the low end of the reference ranges. Thoracic radiographs revealed rounded lung lobe margins and signs of pleural thickening, predominantly in the left hemithorax, consistent with constrictive pleuritis with or without pleural effusion. Despite the persistence of these radiographic abnormalities, lung expansion in the left hemithorax was improved, as shown by the increase in volume of aerated lung apparent on the radiographic projections. Thirteen months postoperatively, the cat had a normal activity level and appetite, and no abnormalities were detected on physical examination. The cat weighed 3.2 kg, and body condition score was considered normal (3 out of 5). Thoracic radiographs were unchanged from the previous examination, substantiating probable persistence of constrictive pleuritis. Repeat hematology revealed recurrence of lymphopenia and neutropenia. Because of financial constraints, evaluating the cause of this was not pursued. As the cat was clinically normal, no dietary restrictions were necessary.

Discussion

The accumulation of chyle within the thoracic cavity causes respiratory compromise, which can be life-threatening. First-line treatment for animals with respiratory compromise secondary to chylothorax is thoracocentesis to alleviate respiratory distress. Once the patient is stabilized, the focus is on verifying the chylous nature of the thoracic fluid and identifying an underlying cause.

The most reliable method for definitive diagnosis of chylothorax is comparison of pleural fluid and serum triglyceride and cholesterol concentrations.¹⁹ In chyle, the pleural fluid triglyceride concentration is often 10× that in the serum, and the fluid cholesterol concentration is lower than that in the serum. Chyle usually appears distinctively opaque and milky-white, although it can also be clear, pinkish, or yellowish in color. Cytopathological examination can reveal a predominant cell type of either lymphocytes or neutrophils. It is important to distinguish chylothorax from other forms of pleural effusion, because treatments differ. The cat of this report was confirmed to have chylothorax based on a thoracic fluid triglyceride concentration of 469 mg/dL and a serum triglyceride concentration of 46 mg/dL. In addition, the thoracic fluid cholesterol concentration was 45 mg/dL, while the serum cholesterol concentration was 98 mg/dL.

Because chylothorax has been reported to occur in association with such diseases as heartworm disease,²⁰²¹ fungal granulomas,²² diaphragmatic hernia,³²³ cardiac disease,²⁴²⁵ and neoplastic disease,²⁶²⁷ the diagnostic workup should focus on identifying an underlying cause. In one retrospective study of 37 cats with chylothorax, no underlying disease process could be identified in 27 (73%) of the cases.⁹ In the case reported here, no underlying disease process causing the chylothorax could be identified.

Medical management of chylothorax consists of periodic thoracocentesis to restore pulmonary expansion, and treatment is directed at changing the character of the chyle so that it is more readily absorbed into the systemic circulation. A low-fat diet is prescribed in an attempt to decrease the volume of chylous fluid produced. However, the efficacy of this practice in dogs has been questioned,²⁸ and in cats it is unknown. Dietary therapy probably does not change the volume of chylous fluid produced, but the fluid produced may have lower lipid content, which may allow it to be more readily absorbed through the pleura. This speculation has not been substantiated clinically or experimentally.

Recently, the use of rutin, a benzopyrone compound, has been investigated for medical management of chylothorax in small animals.^28–30 Benzopyrones have been used in humans for the treatment of lymphedema.³¹ They act by stimulating macrophages to break down protein in lymph, thereby rendering the lymph more accessible to reabsorption. There are a few reports of successful management of chylothorax in cats and dogs using rutin, but no long-term studies have been performed to compare it with other methods of treatment. Although rutin was prescribed in the case reported here, the dose and frequency were not as high as has recently been recommended for treatment of chylothorax in small animals (50 to 100 mg/kg body weight, tid).²⁸ Furthermore, because of the difficulty of administering medication to the cat of this report, it was not possible to evaluate whether a higher dose of rutin would have been more effective.

Thoracic duct ligation is considered the surgical treatment of choice for chylothorax.¹⁷²⁸³⁰ The goal of thoracic duct ligation is to promote the formation of alternate lymphaticovenous drainage routes for lymph by ligating all pathways into the thoracic duct.⁷ The thoracic duct is most accessible in the caudal thorax and is usually more prominent in the right hemithorax in dogs and in the left hemithorax in cats. Intraoperative identification of multiple branches of the thoracic duct using mesenteric lymphangiography is considered important to verify complete ligation, and postoperative lymphangiography is suggested to verify that all branches have been ligated.²⁸ However, persistent chylous or nonchylous effusion has been observed following verified complete thoracic duct ligation.²⁸ In the case reported here, the thoracic duct could not be identified and ligated. Intraoperative lymphangiography was not performed, but it may have been useful for identification of the thoracic duct.

The omentum has many properties that render it useful in a variety of veterinary surgical procedures, including prostatic abscessation, the treatment of large and chronic nonhealing wounds, vascular surgery, and gastrointestinal surgery.^32–37 The omentum contains aggregates of lymphoid tissue (i.e., milk spots) that have direct contact with the peritoneal cavity³² and provide efficient lymphatic drainage. These lymphatics eventually drain to the subpyloric and splenic lymph nodes and into the thoracic duct to reach the systemic circulation. Williams and Niles postulated that the omentum served as a physiological drain in the treatment of chylothorax.¹⁷ However, the chyle that is resorbed by the omentum eventually drains back into the thoracic duct and hence into the thoracic cavity. An alternative explanation for the role of the omentum in resolving chylothorax is that the angiogenic and adhesion-forming properties of the omentum stimulate healing of the source of chyle seepage, thereby enhancing the formation of alternate lymphaticovenous drainage. However, the true function of the omentum in chylothorax remains unknown.

Constrictive pleuritis is considered a severe complication of chylothorax and is associated with a very poor outcome in both dogs and cats.^38–40 With constrictive pleuritis, the visceral pleura becomes severely thickened and entraps the pulmonary parenchyma, preventing normal lung expansion and thereby compromising ventilation. The cause of constrictive pleuritis is not known, though it may be associated with the irritation of long-standing chyle within the thoracic cavity, the irritation of repeated thoracocentesis, or the long-term presence of a thoracic drain.^40–42 Chronic inflammatory exudates (such as chyle and pus) may induce changes in mesothelial cell morphological features, resulting in increased permeability, mesothelial cell desquamation, and the triggering of both internal and external pathways of the coagulation cascade.³⁸ The only effective treatment for constrictive pleuritis is decortication, but there is a substantial risk of disruption of pulmonary parenchyma and subsequent pneumothorax or hemorrhage. Considering the degree to which the left hemithorax of the cat of this report was affected, the authors felt that the potential benefits of decortication outweighed these risks. However, complete decortication was not performed because of the concern of causing irreparable pulmonary parenchymal damage. The cat did develop a transient pneumothorax that resolved with conservative management, but the authors estimated that pulmonary expansion in the left hemithorax was improved by about 50% using this technique. The authors theorized that the omentum may have aided in sealing the damaged area of the pulmonary parenchyma responsible for air leakage.

Follow-up radiographs of the cat of this report made 50 days postoperatively showed initial improvement consistent with resolution of pleural fluid. Thoracic radiographs made 13 months postoperatively, however, were not changed compared to those made 50 days postoperatively. The rounded lung-lobe edges and thickened pleura were most likely a result of persistent constrictive pleuritis, and further radiographic improvement of the thorax is therefore unlikely.

Conclusion

The success of omentalization of the thoracic cavity for management of chylothorax and constrictive pleuritis in this cat suggests an alternative treatment method for cases of chylothorax in which other treatments fail. Although omentalization without thoracic duct ligation may carry a risk of development or progression of constrictive pleuritis, omentalization of the thoracic cavity warrants further investigation to determine its effects and the long-term prognosis of patients with chylothorax treated with this technique.