Chylothorax Associated With a Congenital Peritoneopericardial Diaphragmatic Hernia in a Dog

Introduction

Chylothorax develops when chyle leaks from the intrathoracic lymphatic duct system into the pleural space. The most common known causes of chylothorax include trauma, thoracic mass, heartworm infestation, heart disease, pericardial disease, infection, lung lobe torsion, iatrogenic damage to the thoracic duct, congenital abnormalities, venous thrombi, and neoplasia.^1–3 Frequently, the etiology of chylothorax is unknown. The purposes of this report are to describe a case of chylothorax secondary to a peritoneopericardial diaphragmatic hernia (PPDH) and discuss potential pathophysiological mechanisms of chylothorax in this case. To the authors’ knowledge, this is the first reported case of chylothorax secondary to a presumably congenital PPDH in a dog.

Case Report

A 2-year-old, neutered male, West Highland white terrier was presented with a 3-month history of increasing respiratory effort and rate, inappetence, and lethargy. On physical examination, the dog was normothermic, tachycardic (150 beats per minute), and panting. The heart and lung sounds were muffled bilaterally during thoracic auscultation. No other physical abnormalities were detected.

Hematological abnormalities included mild hypoproteinemia (total protein 5.8 g/dL; normal range 6 to 7.5 g/dL) and mild leukopenia (5.91 cells × 10³/μL; normal range 6 to 17 cells × 10³/μL). Results of biochemical analysis were within normal limits. Thoracic radiographs were obtained and revealed moderate bilateral pleural effusion obscuring the cardiac silhouette. The mediastinum was symmetrically widened with soft-tissue opacity.

An echocardiogram was performed. A 5 × 6-cm, solid mass of soft-tissue echogenicity was noted in the left thorax. The mass was thought to be extrapericardial at the time of examination. The remainder of the cardiac examination was normal. Thoracocentesis was performed, and 120 mL of opaque, white fluid was aspirated from the pleural space.

Cytological and biochemical evaluations of the fluid were characteristic of a chylous effusion. The total nucleated cell count was 3.03 × 10³ cells/μL and composed of lymphocytes (39%), activated macrophages (37%), nondegenerate and often vacuolated neutrophils (22%), and reactive mesothelial cells. Fluid cholesterol was less than serum cholesterol, and fluid triglycerides were markedly greater than serum triglycerides (fluid cholesterol 96 mg/dL, serum cholesterol 149 mg/dL; fluid triglycerides 995 mg/dL, serum triglycerides 31 mg/dL). The fluid was cultured and found to be negative for aerobic bacterial growth. A smear of the fluid was evaluated for acid-fast bacilli (i.e., Mycobacterium) and was negative, and a polymerase chain reaction test for Mycobacterium was also negative.

A thoracic computed tomography scan was performed under general anesthesia. Findings included marked bilateral pleural effusion and a noncontrast-enhancing, fat-attenuating mass within the pericardium. The mass was caudal and ventral to the heart and continuous with falciform fat in the cranial abdomen [Figure 1]. The lesion was consistent with a PPDH with herniation of falciform or omental fat.

The dog was anesthetized, a midline celiotomy was performed, and the abdomen was explored. A small amount of omentum was observed coursing to the midventral diaphragm just dorsal from the sternum and through a diaphragmatic hernia approximately 2.5 cm in diameter. A caudoventral midline sternotomy was performed, extending the surgical approach cranially into the thorax. A moderate amount of chylous effusion was removed from the thorax. The pericardium appeared mildly thickened and was expanded by a large intrapericardial mass. Within the pericardial sac, a large (8 × 5.5 × 2.5 cm), nonadherent, pseudoencapsulated mass of fat compressing the heart was appreciated [Figure 2]. The mass was continuous with the omentum at the level of the diaphragm. The omentum was ligated and divided caudal to the diaphragm, and the mass was removed. A subtotal pericardectomy was performed to the level of the phrenic nerves. The sternotomy was closed routinely after placement of a thoracic tube. The small ventral hernia ring in the diaphragm was closed. The mass, pericardium, and a pleural biopsy sample were submitted for histopathological analysis.

A cisterna chyli ablation (CCA) was then performed. To delineate abdominal lymphatics and identify the cisterna chyli, methylene blue dye was injected into an ileocolic lymph node to effect (approximately 0.5 mL). The cisterna chyli was then ablated with sharp excision of its walls. The abdominal incision was closed routinely, and the dog recovered uneventfully. Postoperative analgesia was maintained with a continuous-rate infusion of morphine, lidocaine, and ketamine. A 25-μg transdermal fentanyl patch^a was applied, and oral carprofen^b (2 mg/kg per os q 12 hours) was initiated for 2 weeks.

The cumulative amount of chylous fluid drained from the pleural space over the initial two postoperative days was 121 mL. By the third postoperative day, the chylous effusion was negligible. Analysis of the thoracic fluid 3 days postsurgery was still consistent with chylous effusion (cholesterol 65 mg/dL; triglycerides 701 mg/dL). However, because the dog was doing well clinically, the chest tube was removed, and the dog was discharged the following day.

Grossly, the mass within the pericardium was composed of loosely packed, white, soft lobules that disintegrated easily with handling. Sections of the mass obtained for histopathological evaluation revealed loosely packed lobules containing well-differentiated adipocytes with occasional, randomly scattered blood vessels. Often, lobules were encapsulated by thin bands of connective tissue on one side lined by simple squamous epithelium (i.e., mesothelium). The mass was diagnosed as herniated abdominal fat.

Biopsy specimens from the pericardium revealed one surface lined by irregular, papilliferous extensions lined by mesothelium. The extensions were multifocally infiltrated by mild numbers of leukocytes (i.e., neutrophils, plasma cells, lymphocytes, and fewer macrophages). Subjacent to the mesothelial surface was loosely packed, well-differentiated, edematous adipose tissue that was subjacent to the opposite surface. The opposite surface was composed of a thick, dense, eosinophilic band of connective tissue that was diffusely congested with multifocal areas of hemorrhage. The pericardium was diagnosed as mild, proliferative, hemorrhagic pericarditis.

The section of pleura consisted of a surface lining of densely packed mesothelium overlying connective tissue bundles harboring random, cohesive clusters of leukocytes (i.e., neutrophils, plasma cells, lymphocytes, and fewer macrophages) multifocally. The histopathological diagnosis was mild hemorrhagic pleuritis.

According to the owner, after discharge from the hospital, the dog exhibited a permanent and complete resolution of the cough and dyspnea. The dog’s appetite and energy level also normalized. The dog was rechecked on days 13 and 76 postoperatively. At these times, physical examination was normal, and thoracic radiographs demonstrated resolution of pleural fluid.

Discussion

Peritoneopericardial diaphragmatic hernia is a relatively common congenital diaphragmatic abnormality, and it is often asymptomatic.⁴ As seen in this case, ventral defects are a result of improper transverse septum development secondary to prenatal injury, a teratogen, or a genetic defect.⁴

Many of the known etiologies of chylothorax cause a physical or functional obstruction to the flow of chyle within the thoracic duct. Increased thoracic duct outflow pressure will reduce lymph flow rates in the thoracic duct in an animal model, and this may predispose the animal to formation of chylothorax. Constrictive pericarditis has been previously associated with chylothorax.^3,5 Recently, pericardectomy has been suggested as a means of decreasing right atrial pressures and perhaps relieving a subtle functional obstruction of the thoracic duct for dogs and cats with idiopathic chylothorax.⁶

While the central venous and right atrial pressures in this dog were not measured, based on the surgical findings, right atrial pressure was likely increased secondary to extracardiac intrapericardial compression from the PPDH. After surgical resolution of the PPDH and the accompanying compression, the chylothorax resolved rapidly and permanently; therefore, PPDH seems the most likely cause of the chylothorax. Other causes of chronic intrapericardial distension, such as chronic pericardial effusions, frequently do not result in significantly increased intrapericardial pressures because of pericardial hypertrophy and a resultant increase in compliance.⁷ The same is likely true for most cases of PPDH. However, in this dog, the ventral aspect of the mass was in contact with the sternum [Figure 1], suggesting direct compression of the mass between the sternum and heart. Because of this physical juxtaposition of the sternum, mass, and heart, any amount of pericardial hypertrophy may not have maintained low intrapericardial pressures. The reason the presumably congenital PPDH took 2 years to cause chylothorax is unknown; however, cellular growth or swelling secondary to venous strangulation may have increased the size of the mass and resulted in increased cardiac compression. Based on gross examination during surgery, the herniated mass was abdominal fat (most likely omental fat), although falciform fat could not be ruled out. The origin of the herniated fat could not be determined histologically.

Three surgical procedures (i.e., removal of the mass, pericardectomy, and CCA) were performed in an attempt to maximize clinical success with a single surgical and anesthetic episode. Which procedure had the most effect is unknown; perhaps all three procedures were needed simultaneously. Likely, removal of the hernia contents compressing the heart had a significant effect in resolution of the chylothorax. Pericardectomy was performed because the pericardium appeared thick and was greatly distended; pericardectomy has resulted in resolution of chylothorax in some cases.⁶ Cisterna chyli ablation was performed to encourage formation of abdominal lymphaticovenous anastomoses.⁸ In normal research dogs, when CCA was combined with thoracic duct ligation, the frequent result was extrathoracic redirection of chyle.⁸ Cisterna chyli ablation and thoracic duct ligation have also been described for treatment of a small number of clinical cases of canine idiopathic chylothorax.⁸

Theoretically, in addition to creating abdominal lymphaticovenous anastomoses, CCA may also result in reduced lymphatic hypertension in the abdominal and caudal thoracic lymphatic system after thoracic duct ligation.^8,9 This effect may decrease the drive for collateral lymphatic development after thoracic duct ligation.⁸ In this case, CCA was not used in combination with thoracic duct ligation; the effect or efficacy of CCA in this circumstance is unknown. However, the clinical signs in this dog resolved very rapidly and prior to the probable time it would take to form lymphaticovenous anastomoses, suggesting the CCA was likely not responsible for the rapid resolution of the chylothorax.

Conclusion

Chylothorax often occurs as a complication secondary to another underlying condition. The primary condition may result in physical or functional obstruction of the thoracic duct, causing increased thoracic duct lymph pressures and leakage. In cases of presumed idiopathic chylothorax, efforts should be made to rule out potential primary pathology, including PPDH.

Acknowledgments

The authors acknowledge the assistance and advice of Howard Steinberg, VMD, PhD, Diplomate ACVP, in the interpretation of histopathological samples.