J Vet Intern Med 2002;16:541–546

Percutaneous Balloon Pericardiotomy as a Treatment for Recurrent Pericardial Effusion in 6 Dogs J.A. Sidley, C.E. Atkins, B.W. Keene, and T.C. DeFrancesco Percutaneous balloon pericardiotomy (PBP) has been performed in people and in a small number of dogs as a treatment for recurrent pericardial effusion with tamponade (PET). We performed this technique on 6 dogs with recurrent PET (5 with heart base tumors and 1 with no identifiable mass). Under general anesthesia and fluoroscopic guidance, a balloon-dilating catheter (diameters 14–20 mm) was introduced percutaneously at the 5th intercostal space through a sheath-introducing catheter, positioned across the parietal pericardium, and inflated 3 times. No dog experienced serious complications. The procedure was considered successful in 4 of 6 dogs. One dog is still alive without recurrence of PET 1 year after the procedure. Three dogs died of unrelated disease without recurrence of PET 5, 19, and 32 months after the procedure. The procedure was not beneficial in 1 dog that was euthanized 9 weeks later because of recurrence of pleural and abdominal effusion thought to be secondary to PET. One dog may have temporarily benefited but developed symptomatic PET 6 months after PBP. PBP appears to be a safe, economical, and potentially effective palliative treatment for recurrent PET and is a reasonable, less invasive alternative to surgery for dogs with recurrent PET, especially effusions caused by heart base tumors and possibly idiopathic pericardial effusion. Premature closure of the stoma is a potential cause for long-term failure and was thought to have been responsible for the recurrence of clinical signs in 2 dogs. Key words: Cardiac tamponade; Chemodectoma; Heart base tumor; Hemangiosarcoma; Idiopathic pericardial effusion.

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ericardial effusion with tamponade (PET) is the most commonly encountered pericardial disease in the dog and cat.1,2 The 2 most common causes of PET in the dog are neoplasia (57%) and idiopathic effusion (17%),2 with 1 retrospective study reporting a similar percentage for both of these causes (38%).3 Other potential causes are infection, left atrial rupture, pericardial cyst, uremia, foreign body, right heart failure, trauma, and pericardial peritoneal diaphragmatic hernia.1,2 Excessive fluid accumulation within the pericardial sac causes a rise in intrapericardial pressure, with a resultant increase in diastolic intracardiac pressure and a subsequent decrease in diastolic filling, stroke volume, arterial pressure, and venous return. Severe hemodynamic consequences may result, including right heart failure and cardiogenic shock. Pericardiocentesis usually is necessary to alleviate clinical signs and can be lifesaving.4 Unfortunately, reaccumulation of pericardial effusion is common. In the past, treatment options have included either periodic pericardiocentesis or thoracotomy and pericardiectomy, with potential tumor resection.4,5 Recently, thoracoscopic partial pericardiectomy has been described as a treatment.6 Percutaneous balloon pericardiotomy (PBP) is a novel technique gaining acceptance in human medicine for the management of patients with malignant PET.7–9 With a percutaneous approach, a balloon-dilating catheter is used to create a hole in the pericardial sac and allow pericardial fluid drainage into the pleural space, where it is more readily absorbed. Excellent results have been obtained with this technique in humans, with success rates as high as 92% and From the Department of Clinical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC. Abstract was presented at The American College of Veterinary Internal Medicine Conference, Chicago, IL, June 10–13, 1999. Reprint requests: Clarke Atkins, DVM, College of Veterinary Medicine, North Carolina State University, 4700 Hillsborough Street, Raleigh, NC 27606; e-mail: clarke㛮[email protected]. Submitted March 23, 2000; Revised November 1, 2001; Accepted February 27, 2002. Copyright 䉷 2002 by the American College of Veterinary Internal Medicine 0891-6640/02/1605-0007/$3.00/0

minimal complications.8 Advantages include avoiding the morbidity and mortality of thoracotomy, minimal postprocedural recovery and hospitalization, and decreased cost. Cobb et al10 1st reported the application of this technique in 2 dogs with intrapericardial neoplasia and recurrent PET. Survivals of 4 and 14 weeks were reported in these dogs, with no recurrence of clinically relevant pericardial effusion noted, but 1 dog was not reexamined before being euthanized for acute onset of dyspnea at 1 month. This report presents our experience with 6 dogs treated by PBP for recurrent PET. Five of the dogs had echocardiographic evidence of a tumor located at the heart base. One dog had no identified cause for the effusion and was presumed to have had idiopathic pericardial effusion. The procedure we used was similar to that described by Cobb et al10 with some modifications.

Materials and Methods PBP was performed on 6 dogs with recurrent symptomatic PET. Five of the 6 dogs in the study had a mass at the heart base identified by echocardiography (2 were confirmed as chemodectomas at postmortem examination). One dog (dog 6) had no identifiable mass and was presumed to have had idiopathic pericardial effusion. All dogs had multiple episodes of pericardial effusion treated by pericardiocentesis before the procedure was performed, with the number of occurrences ranging from 2 to 4. Three of the patients in the study had concurrent diseases, which potentially limited their long-term survival. Dog 1 had appendicular osteosarcoma, dog 2 had a solitary nodule on the spleen diagnosed as lymphoma, and dog 3 had severe mitral and tricuspid regurgitation. The dogs ranged in age from 7 to 13 years, and their weights ranged from 7.8 to 44 kg. There were 2 Labrador Retrievers (dogs 2 and 4), 1 Golden Retriever (dog 6), 1 Lhasa Apso (dog 3), and 2 mixed-breed dogs (dogs 1 and 5).

PBP Procedure PBP was performed under general anesthesia, with fluoroscopic guidance and ECG monitoring. In the 1st dog, the procedure initially was attempted under oxymorphonea sedation (0.05 mg/kg IM) and local anesthesia, but sedation was inadequate, so general inhalational anesthesia then was administered. The dogs were placed in left lateral recumbency with a foam wedge positioned under the spine to angle them slightly sternally. After surgical preparation of the site, a stab incision was made at the right 5th intercostal space at the point of

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Fig 1. Percutaneous balloon pericardiotomy (PBP) procedure. (A) Catheter is inserted percutaneously into the pericardial sac. (B) With a guide wire, the catheter is replaced with a sheath-introducing catheter. (C) Balloon-dilating catheter is inserted into the pericardial sac through the sheath-introducing catheter. (D) The sheath-introducing catheter is removed from the pericardial sac, and the balloon-dilating catheter is positioned across the parietal pericardium and inflated.

costochondral junction. A 16-g (3.25 in.) over-the-needle catheterb was inserted percutaneously into the pericardial sac (Fig 1A). Up to 25 mL (0.25–0.5 mL/kg) of iodinated contrast materialc was injected into the pericardial space to outline it and confirm the catheter location. By means of the short 0.035-in.-diameter guide wire supplied with the introducing catheter (Fig 1B), the catheter was replaced with an 8.5French (Fr) (dogs 1–3) or a 10-Fr (dogs 4–6) percutaneous sheath– introducing catheter.d The short guide wire then was replaced with a 260-cm-long (0.035 in.-diameter) exchange guide wire with a soft flex-

ible tip,e and the guide wire was positioned across the pericardial sac with about 10–15 cm of the wire within the pericardium to maintain the position there. A 14-mm (dogs 1–3) or 18-mm (dogs 4–6), 4-cm balloon-dilating catheterf then was inserted over the guide wire into the pericardial sac (Fig 1C), and the sheath-introducing catheter was partially removed, so it was no longer across the body wall. In the last 2 dogs, the foam wedge was removed at this time to allow the dogs to lie in left lateral recumbency, so that the heart and pericardium would fall slightly away from the body wall, facilitating balloon po-

→ Fig 2. Percutaneous balloon pericardiotomy (PBP) procedure. (A) Balloon-dilating catheter positioned across the parietal pericardium and partially inflated. Note guide wire and waist caused by pericardial constriction. Iodinated contrast material can be seen outlining the pericardial space. (B) Fully inflated balloon-dilating catheter.

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sition. The balloon then was positioned across the parietal pericardium, taking care to make sure the balloon was advanced fully into the thorax. Partial balloon inflation with a 50 : 50 contrast saline mixture helped confirm placement (Fig 1D). When a waist was evident fluoroscopically (Fig 2A), the balloon was fully inflated until the waist disappeared 3 times each for 3 minutes (Fig 2B). Resistance to inflation was detected, but the actual pressure was not measured. The balloon-dilating catheter then was deflated and removed with gentle traction. In the 2nd dog, this procedure was followed by a 2nd dilatation with a 20-mm, 4-cm balloon-dilating catheter placed (without the sheath introducer) over the guide wire. In each dog, after the procedure was performed, only a minimal amount of pericardial fluid remained within the pericardial sac. This was easily assessed fluoroscopically because of the previously injected dye within the pericardial sac. The skin was closed with a single ligature by 2-0 nylon.g Intraoperative antibioticsh were given to all dogs at anesthetic induction and 2 hours later. In dogs 2 and 3, transdermal fentanyl patchesi were applied 16 and 5 hours before the procedure, respectively. In all dogs, oxymorphone was given postoperatively and then as needed for pain. Dog 1 (assessed to be dysphoric with oxymorphone) was given butorphanolj for partial oxymorphone reversal. The dogs were discharged either on the day of or 1 day after the procedure. The 1st 2 dogs were monitored overnight in the intensive care unit. The last 4 were monitored closely for 2–3 hours after the procedure in the intermediate care area and were discharged the same day. The cost of the procedure was approximately one-third to one-half that of a thoracotomy and pericardiectomy at our institution.

Results The procedure was performed without complication in all 6 dogs, and all were discharged within 24 hours. The owner of dog 2 reported signs of anxiety and difficulty getting comfortable for 48 hours after the procedure, which she attributed to pain. A fentanyl patch had been placed before the procedure, and carprofenk also was given as needed after the procedure. Survivals of 32, 19, 8.5, 5, and 2 months were obtained, with 1 dog (dog 6) still alive 1 year after the procedure. Three of the dogs died of unrelated illness without recurrence of pericardial effusion. Dog 1 was euthanized after 5 months with advanced metastatic osteosarcoma. Dog 3 was euthanized with congestive heart failure because of atrioventricular valvular endocardiosis after 19 months. The longest survivor, dog 2, died 32 months after the procedure with nonspecific clinical signs of weakness and lethargy. The cause of death was unknown. Thoracic radiographs at the time of death showed a large heart base mass pushing the trachea to the right. The heart size was relatively normal with normal contours and no radiographic evidence of pericardial effusion. No echocardiogram was performed at that time. The shortest survivor (dog 4) developed recurrent abdominal and pleural effusion 9 weeks after the procedure and was euthanized by the referring veterinarian. No diagnostic tests or postmortem examinations were performed to determine the cause of the effusion. Dog 5 developed a small amount of pericardial effusion without tamponade 2.5 months after the procedure but was asymptomatic. Six months after the procedure, the dog developed exercise intolerance and ascites, and the amount of pericardial effusion had increased substantially. A pericardiocentesis then was performed. Six weeks later, the dog again had recurrence of pericardial effusion, and a 2nd PBP was performed. The dog was euthanized 1 month later, but it is unclear whether

or not signs of pericardial effusion had recurred at the time of euthanasia. Reportedly, the dog was eating well and did not have ascites when euthanized. Two of the dogs that died of unrelated illnesses, neither of which had recurrence of pericardial effusion, were examined postmortem. In dog 1, postmortem examination confirmed a chemodectoma at the heart base that was locally extensive and metastatic to the lungs. Multifocal metastases of osteosarcoma also were identified in the lung and liver. The parietal pericardium was diffusely thickened and multifocally adherent to the visceral pericardium. Microscopic evaluation revealed diffuse chronic lymphocytic pericarditis with marked fibrosis. No patent stoma connecting the pericardial space to the pleural space was observed, but a 1-cm-diameter tunnel attached the pericardium to the parietal pleura at the location of the pericardiotomy site. In dog 3, postmortem examination identified 3 chemodectoma masses: 1 located in the mediastinum, 1 that enveloped the carotid artery and compressed the vena cava, and a 3rd that was attached to the pericardium adjacent to the left atrium. The pericardium was adherent to the heart at the site of the procedure, with fibrous tissue radiating from this point approximately 1–2 cm. There was no patent stoma at the pericardiotomy site. Multifocal metastatic nodules were observed in both the right and left ventricles extending from the epicardium into the endocardium. Mitral and tricuspid valve endocardiosis was confirmed, as well as pulmonary edema, pleural effusion, and ascites. In neither dog was pericardial effusion identified.

Discussion Pericardiectomy with or without mass resection has been considered the definitive treatment for recurrent PET. Thoracotomy, however, is associated with marked morbidity and mortality,11 often requires prolonged hospitalization,12 is expensive, and often is only palliative, as many of the tumors have either metastasized (hemangiosarcoma) or are too expansive (chemodectoma and mesothelioma) to be resected.4,13 In a review of 22 dogs that underwent pericardiectomy, the median survival time for dogs with neoplastic disease was 52 days (range, 0–814 days). Of 9 dogs with neoplasia, 3 (2 with chemodectoma and 1 with lymphoblastic lymphoma) died in the immediate postoperative period.11 In another study, 3 of 25 dogs with idiopathic pericardial effusion undergoing pericardiectomy died postoperatively.14 Recently, thoracoscopic partial pericardiectomy has been described in the dog.6 This procedure has the advantage of avoiding many of the risks inherent to thoracotomy while still allowing biopsy of the pericardial sac, but it involves highly specialized equipment and expertise. PBP is a technique being used in human medicine for the treatment of malignant PET. The majority of people with pericardial effusion have metastatic neoplasia, and life expectancy often is quite short.9 The desire to avoid anesthesia and surgery in these critically ill patients with limited life expectancy makes PBP a desirable alternative. Success rates (defined as no recurrence of pericardial effusion and no clinical complications) of 92% have been reported.8 Although this technique primarily has been used in the treatment of patients with malignant pericardial effusion, there

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have also been reports of its use in the treatment of nonneoplastic effusion. Thanopoulos et al15 reported a 90% success rate with the use of PBP for the treatment of 10 children with large, nonmalignant pericardial effusions and a mean follow-up of 14.9 months (range, 3–29 months). One potential disadvantage of PBP with presumed idiopathic effusion is that it does not allow visualization of the heart and pericardium and does not allow biopsy of the pericardium to rule out neoplasia, unlike other potential treatment options. The only published use of PBP in the dog reported shorter survivals (4 and 14 weeks) in 2 dogs with malignant PET than those reported here.10 This difference may reflect the severity and prognosis of the underlying tumors in that study, which included a right auricular appendage mass (presumed hemangiosarcoma) and a large heart base mass that was thought to have caused obstruction of the caudal vena cava. Five of the 6 dogs in our study had tumors located at the heart base, suggestive of chemodectoma (2 were confirmed at postmortem examination), which carries a better prognosis than other common cardiac tumors, especially hemangiosarcoma.16 The 6th dog did not have a discrete mass identified and was presumed to have had idiopathic pericardial effusion. No dogs in this study were known to have hemangiosarcoma or mesothelioma, and the benefit of PBP in these diseases is unknown. The procedure may not be as beneficial in patients with hemangiosarcoma because of the risk of exsanguination through the pericardial rent.17 In all 6 patients, the procedure was performed without clinically relevant complications. The owner of 1 dog reported signs of anxiety and perceived discomfort for the 1st 2 days after the procedure, despite a fentanyl patch and carprofen administration. In this dog, we had repeated the procedure with a larger balloon, which was introduced through the chest wall without the sheath-introducing catheter. This approach may have caused more trauma to the chest wall and resultant discomfort. The human pericardium is reported to be richly innervated with sensory fibers,18 and thus the torn pericardium also is a potential source of discomfort. Reported complications of this procedure in people include symptomatic pleural effusion, fever, pericardial bleeding requiring surgery, and a small resolving pneumothorax.7,8 None of these complications were encountered in the 6 dogs of this study. The technique that we used was similar to that previously described in dogs10 with some modifications. In humans, this procedure usually is performed with local anesthesia and mild sedation. In the previous report by Cobb et al,10 local lidocaine infiltration and heavy sedation were adequate restraint for 1 patient, but general anesthesia was needed for the other. In the 1st patient of our study, sedation with oxymorphone and local anesthesia was inadequate, and general anesthesia was employed to complete the procedure. We chose to anesthetize the subsequent 5 patients to ensure adequate restraint. Depending on patient cooperation and hemodynamic stability, PBP potentially could be performed under sedation and local lidocaine infiltration. Another modification to those previously described was the instillation of contrast material in the pericardial sac to outline the pericardium and ensure proper catheter placement. This modification also allowed us to easily assess the remaining pericardial effusion after the procedure was per-

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formed. As a 3rd alteration, multiple inflations were done to ensure maximal dilatation of the pericardial window. In 4 of the 6 dogs, larger balloon-dilating catheters also were used. Cobb et al10 used 12-mm-diameter balloons in the 2 patients reported. We used balloons ranging from 14 to 20 mm in diameter. The largest balloon-dilating catheter used (a 20-mm, 4-cm-diameter balloon) would not fit through the sheath-introducing catheter and was introduced over the guide wire without the sheath-introducing catheter. Larger sheath-introducing catheters are available but are more expensive. The dog in which we used the larger (20-mm diameter) balloon was the longest survivor; however, we do not have enough experience with this procedure to determine whether balloon size has an effect on survival. Most studies in humans have been performed with a 20-mm-diameter balloon.7–9 As a 5th alteration, a wedge was used to position the dogs slightly sternally to facilitate pericardial entry. In latter procedures, the wedge was removed before balloon dilation to allow the heart and pericardium to fall away from the body wall, facilitating balloon placement across the parietal pericardium and fully within the thorax. Sufficient pericardial effusion is necessary for PBP so that the pericardial sac can be accessed without producing pneumothorax or penetrating the heart. However, severe tamponade and hemodynamic compromise may increase the risk of anesthesia. For dogs with severe pericardial effusion and cardiac tamponade, pericardiocentesis with PBP at a later date may be preferable. Minimizing anesthesia time by surgical preparation before induction may be useful in minimizing anesthetic risk. Not performing PBP on the 1st occurrence allows for analysis of the pericardial fluid before the procedure to rule out infection and occasionally to obtain a definitive diagnosis. This approach also confirms that the effusion is recurrent, thus warranting more aggressive treatment. The precise mechanism whereby balloon pericardiotomy prevents recurrent PET is unclear. Initially, the hole created allows pericardial effusion to drain into the pleural space, where it can be absorbed more readily. The duration of stoma patency is unknown. Sugimoto et al19 studied 28 patients who underwent a surgically created subxiphoid pericardial window. From examining patients by both autopsy (4 patients) and echocardiography (28 patients), they hypothesized that the long-term efficacy of the pericardial window did not correlate with the persistence of a pericardial opening, but rather, with adhesions between the parietal and visceral pericardium secondary to reactive pericarditis. In the 2 dogs in this study that had postmortem examinations, no patent stoma was observed at the time of death. Both dogs had portions of the parietal pericardium adherent to the visceral pericardium, presumably causing some reduction in the pericardial space. The histopathology in 1 dog disclosed lymphocytic pericarditis with marked fibrosis. On the basis of this hypothesis, a long-term concern may be the development of constrictive pericarditis. This complication, however, does not seem to be common in human patients and was not observed in the 6 dogs in this study. Longer term studies may be needed to better evaluate the long-term efficacy and complication rate of this procedure in animals with relatively long life expectancy. The procedure was successful in preventing recurrent PET in 4 of the 6 dogs in this study, was partially beneficial

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in 1 dog, and was without substantial benefit in 1 dog. Three dogs died of concurrent illness 5, 19, and 32 months after the procedure, with no recurrence of pericardial effusion. The dog with presumed idiopathic pericardial effusion is still alive and asymptomatic 1 year after the procedure, with no recurrence of pericardial effusion. In 1 dog, the procedure prevented clinical signs of recurrent pericardial effusion for 6 months, whereas before the procedure, the dog had recurrence after 1 month. This observation suggests that this procedure may have delayed recurrence, but this benefit is uncertain. One dog was not helped greatly by the procedure and developed recurrent abdominal and pleural effusion 9 weeks afterward. It is likely that recurrent PET caused signs of right heart failure in this dog, but other possibilities include tumor expansion, causing compression of the caudal vena cava, or tumor metastasis, causing malignant effusion. These results are comparable to those reported for surgical pericardiectomy. In the Kerstetter et al11 study of 22 dogs that underwent pericardiectomy, 2 of the 4 dogs with chemodectoma died of postoperative complications, and 2 survived—1 for 7 and 1 for 27 months.11 The median survival time in that study for dogs with benign PET was 26 months. On the basis of our experience, PBP is a safe, economical, and potentially effective method for palliative treatment of recurrent PET for dogs with heart base tumors and is less invasive than surgery. This procedure also may have palliative benefits with other causes of pericardial effusion, such as idiopathic pericardial effusion, but further evaluation is necessary. A disadvantage of this procedure is that it requires fluoroscopic guidance and, for presumed idiopathic effusion, allows neither direct visualization nor the potential for biopsy of a mass or the pericardium. Premature closure of the pericardiotomy site with lack of adherence between the parietal and visceral pericardium is a potential cause for long-term failure of the procedure and is thought to have caused recurrence of clinical signs in 2 of the 6 dogs of this study.

Footnotes Numorphan, Dupont, Wilmington, DE Angiocath, Becton Dickinson, Sandy, UT c Iothalamate Na 66.8%, Conray 400, Mallinckrodt, St Louis, MO d Arrow, Arrow International, Reading, PA e TFE-coated Amplatz stiff guide catheter exchange, Cook, Bloomington, IN f Accent, Cook, Bloomington, IN g Ethilon, Ethicon, Somerville, NJ h Cefazolin sodium, Ancef, SmithKline, Beecham, Philadelphia, PA i Duragesic, Janssen, Palo Alto, CA j Turbugesic, Fort Dodge Animal Health, Fort Dodge, IA k Rimadyl, Pfizer, Exton, PA a

b

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