Case Studies In Small Animal

Cardiovascular Medicine

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Case 31

Caval Syndrome Section from "Small Animal Cardiovascular Medicine" On-Line

Text from "Small Animal Cardiovascular Medicine"

CAVAL SYNDROME

Caval syndrome is an acute manifestation of heartworm disease that occurs in association with a large number of heartworms in the right heart that entwine around and pass through the tricuspid valve apparatus. This syndrome has been reported to occur in up to 20% of heartworm cases although the studies involved were not designed to determine this number and the incidence is almost assuredly much less than this. Caval syndrome most commonly occurs in male dogs that have had no previous clinical signs of heartworm disease. It can occur in dogs infested with a moderate or a large number of worms.

Pathophysiology

Caval syndrome is a life-threatening presentation of heartworm disease. The outstanding features of the syndrome are severe tricuspid regurgitation with poor cardiac output and intravascular red cell lysis with resultant hemoglobinemia and hemoglobinuria. The hemoglobinuria is usually marked resulting in dark brown to black urine color.

The pathophysiology of caval syndrome may be as follows. The initiating event must be a mass of worms falling into the right ventricle (see below under "Etiology"). Once the worms are in the right ventricle they probably can move toward the right atrium by entwining themselves in the tricuspid valve apparatus. The mass of worms in and around the tricuspid valve apparatus produces acute and severe tricuspid regurgitation. Severe pulmonary hypertension may exacerbate the amount of tricuspid regurgitation. The severe regurgitation results in a decrease in forward blood flow through the pulmonary vasculature, back to the left heart. As a result, the left heart becomes volume underloaded (the diastolic size of the left ventricle, and left atrium decrease in size) and the left ventricular forward cardiac output decreases. The decrease in systemic blood flow results in clinical signs of poor perfusion (pale or ashen mucous membranes, decreased femoral pulse pressure). The acute, severe tricuspid regurgitation causes a right apical systolic murmur, right heart failure (jugular vein distension, hepatomegaly, and, potentially, ascites), and hemolysis. The right heart failure is purely secondary to the right atrial and right ventricular volume overload caused by the tricuspid regurgitation and not to occlusion of the tricuspid valve orifice since there is no pressure gradient across the tricuspid valve when this variable is measured. The pathophysiology of the hemolysis is not completely understood since hemolysis does not occur in tricuspid regurgitation due to other causes. However, all of the signs of caval syndrome, including hemolysis, have been reproduced by placing silicone tubes the size of heartworms across the tricuspid valve in experimental dogs. Consequently, there is little doubt that the hemolysis is related to shear stresses on the red cells created by the red cells being forced to flow around the worms at a high velocity (calculated to be around 4 m/sec if the systolic pulmonary artery pressure is 65 mmHg). In addition, there is evidence that the red cells are more fragile in dogs with caval syndrome. Factors that may increase red cell fragility include altered serum free and esterified cholesterol concentrations and lecithin acyltransferase activity.

Etiology

The exact reason or reasons that a large number of heartworms invade the right heart are not completely understood. It has been noted that caval syndrome is most common in dogs with many heartworms. In one study of experimental dogs, one group of dogs with a large worm burden developed caval syndrome while another group with a similar worm burden did not. In this study, the group of dogs that developed caval syndrome had an average mean pulmonary artery pressure of 60 mmHg while the dogs that did not develop caval syndrome had an average mean pulmonary artery pressure of 30 mmHg. Consequently, it appears that a large worm burden and moderate to severe pulmonary hypertension may be precipitating variables. It should be noted, however, that another study has documented caval syndrome in dogs with an average of only 40 worms and as little as 12 worms in one dog (range from 12 to 125 worms). Also, many dogs in this study had a mean pulmonary artery pressure less than 30 mmHg.

Statistical alterations such as these do not give any clues as to the reasons why worms end up in the right heart. There are very few ways for heartworms to get from the pulmonary arteries to the right heart. They cannot start there since there is nothing to trap them in the right ventricle once they enter the circulation. Consequently, they have to start in the pulmonary arteries and somehow descend into the right ventricle and then ascend into the right atrium. Although, heartworms can move (anyone who has watched them crawl out of a jugular vein during removal for caval syndrome can attest to this) they have nothing to grab onto in the pulmonary artery to actively move from the pulmonary artery into the right ventricle. Consequently, they must fall through the pulmonic valve. Heartworms are normally held in place against gravity in the pulmonary arteries by blood flow. Consequently, a marked decrease in blood flow would allow them to fall into the right ventricle. This happens after death and is the reason that heartworms are found in the right ventricle at postmortem examination. One study has documented that administering a large dose of a beta blocker to decrease cardiac output can result in heartworms falling back into the right heart. In this study, heartworms were observed, using echocardiography, in the right ventricle and right atrium (across the tricuspid valve) in five of 6 dogs. A murmur of tricuspid regurgitation was audible in these dogs. In 2 cases the worms remained in this position throughout the experiment while in the other three dogs, the worms were expelled back into the pulmonary arteries. Another manuscript has suggested that pentobarbital administration can do the same thing. This suggests that any hemodynamic event that results in transient or sustained pulmonary artery hypoperfusion can result in heartworms falling back into the right heart. This also suggests that hemodynamic forces may act to push heartworms back into the pulmonary artery, strengthening the argument that blood flow is the determining variable. If the worm mass is great enough, the force may not be great enough to push them back out or if they entwine themselves around the tricuspid valve apparatus they may not be expelled. Once the worms are in place in the tricuspid valve orifice and tricuspid regurgitation is produced, forward blood flow is probably too low to expel the worms from the right heart. Dogs with a large worm burden more commonly have severe heartworm disease and severe heartworm disease is more commonly associated with hemodynamic abnormalities such as moderate to severe pulmonary hypertension and decreased cardiac output. Dogs with severe heartworm disease may also have arrhythmias. All these could contribute to either sustained or transient decreased pulmonary blood flow that could cause heartworms to fall into the right ventricle. The movement of heartworms from the pulmonary arteries to the right heart is commonly labeled "migration." Migration infers an active moving process and so cannot be a correct term for this process. Once the worms are in the right ventricle, however, they probably can migrate to the right atrium by attaching to the tricuspid apparatus and pulling themselves into the right atrium. Once they are in this structure there are no more cardiac structures for them to attach to so their migration should be complete. If large numbers were present, however, the leading worms could be forced into the vena cavae by the trailing worms.

Clinical signs and diagnosis

Dogs that present because of caval syndrome commonly have evidence of circulatory collapse (shock) and so are weak and pale and have a slow capillary refill time. Hemoglobinuria and bilirubinuria are present and are due to intravascular hemolysis. Hemoglobinemia can also usually be identified. Respiratory signs of tachypnea and dyspnea may be present. A murmur secondary to tricuspid regurgitation is ausculted over the right cardiac apex. The jugular veins are often distended and the liver is enlarged. Ascites may be present. Laboratory abnormalities that are commonly present include microfilaremia, moderate regenerative anemia, and increases in serum AST, ALT, alkaline phosphatase, bilirubin, and urea nitrogen concentrations. Urine hemoglobin concentration is increased. The laboratory abnormalities are secondary to hemolysis, acute hepatic congestion, and hypoperfusion. Thoracic radiographs are usually typical of severe heartworm disease. The electrocardiogram will have an S wave present in lead CV6LU in most cases with evidence of right heart enlargement in other leads in fewer cases. Arrhythmias may be present.

The diagnosis of caval syndrome is made based on typical clinical signs combined with identifying a mass of heartworms in the right atrium and right ventricle and involving the tricuspid valve apparatus using echocardiography. Other echocardiographic findings include right ventricular volume overload, left ventricular volume underload with a normal to decreased shortening fraction, and paradoxical septal motion.

The prognosis for caval syndrome is guarded to poor. Even with appropriate therapy the mortality rate is often in the 30-40% range. Organ failure and disseminated intravascular coagulation can develop before or after therapy and can result in death.

Treatment

Treatment of caval syndrome involves supportive care and removing the worms from the right atrium and possibly from the right ventricle as soon as possible. Supportive care generally should include intravenous fluid administration to improve cardiac output, to prevent or help reverse disseminated intravascular coagulation, to prevent hemoglobin nephropathy, and to reverse lactic acidosis due to decreased tissue perfusion. If fluids are administered before worm removal, care must be taken not to exacerbate the right heart failure. Once the worms are removed, right heart failure abates rapidly. Consequently, fluid administration may be more aggressive at this time. Other supportive measures can include administration of corticosteroids, heparin, and possibly antibiotics.

Heartworm removal is accomplished by passing an instrument down the jugular vein, into the right heart, grasping or entwining the worms, and removing them. The procedure may be accomplished with no chemical restraint if the patient is moribund, with sedation if the patient is tractable, or with anesthesia if the patient is intractable. The right lateral neck should be clipped and scrubbed in preparation for surgery. If no chemical restraint or only sedation is used, a local anesthetic should be infiltrated over the jugular vein. The skin should be incised over the jugular vein and the vein isolated using blunt dissection. A ligature should be placed around the proximal end of the vein and tied. Another piece of suture should be placed around the distal end of the vein to control bleeding. A small incision is then made in the jugular vein through which an instrument is passed. A variety of instruments have been described for removing heartworms from dogs with caval syndrome. A long alligator forceps (20-40 cm and of a small diameter) is the most commonly used instrument. It has the advantages of being easy to maneuver and easy to grasp worms. Alligator forceps, however, are rigid instruments that can perforate vessels and cardiac chambers and the jaws can be closed forcefully enough to macerate worms. Consequently, they must be used with extreme care. The Jackson forceps is a forceps made specifically to remove heartworms from the right atrium. It is long and cumbersome in small patients. Its jaws are long and flat. This allows for more gentle worm grasping but at times it does not grasp worms firmly enough to result in worm removal. Endoscopic baskets used for retrieval of gastric foreign bodies, a horsehair type brush (Tayama String brush, Kawasaki Masuda, Irakakogyo, Japan), and a flexible alligator forceps (Ishihara alligator forceps, Fuji Photo Optical LTD, Japan) have all been used with success to remove heartworms. Once the instrument is placed into the jugular vein, it must be advanced carefully. This can be done without any imaging assistance or it can be done with either fluoroscopic or echocardiographic guidance. Fluoroscopic guidance makes it easier to pass the forceps through the thoracic inlet and allows one to visualize where the catheter is in the heart. Echocardiographic guidance allows one to have some feel for the relationship between the forceps and the worms. It also allows one to identify remaining worms. If one is doing the procedure without imaging assistance, the distance between the opening made in the jugular vein and the heart should be estimated by aligning the tip of the forceps with the fourth intercostal space on the outside of the dog and noting where the jugular vein opening sits with respect to the rod portion of the forceps. One should usually not worry if one goes in somewhat deeper than this measurement because the forceps usually slides down the caudal vena cava. The most difficult region to manipulate the forceps through is the thoracic inlet. It is not unusual for the forceps to start going down an axillary vein, into a front leg. If resistance is met in this region, the forceps should be withdrawn and the neck of the dog pulled ventrally so that the tip of the forceps is aimed more dorsally and the forceps gently advanced again. Once the tip of the forceps is in the right atrium, the jaws should be opened, the forceps advanced slightly, the jaws closed, and the forceps removed. Usually 1-4 worms are removed. This should be repeated until 5-6 successive attempts are unsuccessful or until no or only a few worms are seen on the echocardiogram.

In the authors' experience, macerating worms results in massive antigen release that results in pulmonary vasoconstriction or may precipitate disseminated intravascular coagulation. We have watched the right ventricle of one cat on ultrasound become progressively more hypodynamic and progressively distend over several minutes, presumably due to acute severe pulmonary hypertension, following the maceration of one worm during withdrawal. At times, worm maceration is unavoidable since worms may be inexorably entwined around chordae tendineae. This results in worm pieces being removed. If worm maceration has occurred, we recommend parenteral corticosteroid (anti-inflammatory doses) and heparin (100-500 U/kg q8h) administration.

Following the removal of the adult worms, intravenous fluids should be administered. Urine color, BUN, and hematocrit should be monitored. Some dogs require oxygen therapy. The dog may be sent home once it has stabilized. When the dog's appetite, respiratory rate, BUN, and hematocrit are normal again, an adulticide should be administered to kill the remaining worms. Following the removal of the worms, the tricuspid regurgitation disappears, cardiac output increases, and right atrial pressure decreases, as expected. This, however, usually takes several days.

Mark D. Kittleson, D.V.M., Ph.D. All rights reserved.