Pericardial Free Patch Grafting as a Rescue Technique in Surgical Management of Right Atrial HSA

Introduction

Pericardial effusion is the abnormal accumulation of fluid in the pericardial space. With increasing volume and intrapericardial pressure, clinical signs of cardiac tamponade develop. These include: lethargy; pale mucous membranes; tachycardia; weak pulses; and muffled heart sounds. The most common causes of pericardial effusion in dogs are cardiac neoplasia and idiopathic pericarditis.^1–4 The most common neoplasia causing pericardial effusion is right atrial hemangiosarcoma (HSA).^1–3 Survival times in dogs with documented right atrial HSA have been reported from 2 days to 8 mo from the time of diagnosis, even with palliative surgical intervention.^1,2,5–9 Surgical treatment for dogs with atrial HSA is palliative subtotal pericardectomy (either with or without atrial mass removal) via thoracotomy or thoracoscopy.¹⁰ This report outlines the successful use of a pericardial patch graft to repair an atrial tear following the rupture of the right wall of the atria after excision of an atrial HSA.

Case Report

A 7 yr old, neutered female vizsla was referred for an exploratory thoracotomy for recurrent hemorrhagic pericardial effusion and a right auricular mass. The patient originally presented to the referring veterinarian for an acute onset of lethargy and anorexia. On physical examination (performed by the referring veterinarian), the dog was obtunded. Her mucous membranes were pale pink with a capillary refill time of 3–5 sec. She was found to be tachycardic with a heart rate of 160 beats/min. Her pulses were weak and thready, but synchronous. Her respiratory rate was 40 breaths/min. Thoracic radiographs showed a rounded cardiac silhouette. Abdominal ultrasound showed evidence of hepatic hypertension and mild abdominal effusion. The abdominal fluid was consistent with a transudate. A limited thoracic ultrasound showed pericardial effusion and a right auricular mass. Pericardiocentesis was performed and 60 mL of hemorrhagic fluid was removed. The dog required therapeutic pericardiocentesis twice more over the following 10 days. She was referred for exploratory thoracotomy.

On initial examination at the time of referral, the dog was alert and in good body condition. The mucous membranes were pink and the capillary refill time was <2 sec. Thoracic auscultation revealed slightly muffled heart sounds with normal, synchronous pulses. Her lungs ausculted within normal limits and the remainder of her physical examination was unremarkable.

Due to the repeated need for therapeutic pericardiocentesis, exploratory thoracotomy and excisional biopsy of the mass was recommended to allow for histologic characterization of the tumor and, simultaneously, palliative treatment by subtotal pericardectomy. Proposed preoperative diagnostics included hematologic and serum biochemical analysis, coagulation profile, blood type, and thoracic radiographs. Results of a complete blood count (CBC) were unremarkable. The serum biochemical analysis showed mild hyperglycemia (131 mg/dL; reference range, 75–130 mg/dL), hypercholesterolemia (375 mg/dL; reference range, 130–300 mg/dL), elevated alkaline phosphatase (357 IU/L, reference range, 20–142 IU/L), elevated alanine aminotransferase (177 IU/L; reference range, 10–110 IU/L), and elevated aspartate aminotransferase (54 IU/L; reference range, 16–50 IU/L). A coagulation profile showed the prothrombin and partial thromboplastin times were within normal limits. Fibrin degradation products were elevated and were ≥20 μg/mL (reference range, <5 μg/mL). Blood typing showed type A (DEA 1.1) positive. Thoracic radiographs showed no evidence of metastatic neoplasia, pericardial effusion, or cardiac enlargement.

A right, fourth intercostal thoracotomy was performed. There was a moderate amount of pericardial effusion, although the pericardium was not thickened. The pericardium was grasped with forceps and opened with Metzenbaum scissors. The subtotal pericardectomy was continued with electrocautery circumferentially, below the level of the phrenic nerve, with a temporary rotation of the heart through the thoracotomy. A large, red, pedunculated 2 cm × 1 cm mass was seen associated with the distal tip of the right auricle (Figures 1 and 2). The mass was removed with a thoracoabdominal stapler using vascular staples^a. Upon removal of the stapler, the residual atrial tissue had torn between and underneath the staples. Allis and Babcock forceps were used to oppose the torn pieces of the atrium. A tangential vascular clamp was used to replace the previous tissue forceps. A combination of horizontal mattress sutures with medium and large pledgets^b were used in an attempt to close the atrial defect, but the atrium continued to tear. The tangential vascular clamp was replaced to close the atria and part of the adjacent vena cava. A residual portion of the left lateral side of the pericardium was harvested and the fatty tissue was removed from the pericardial graft. A double-armed 5–0 polypropylene^c suture line was used to suture the patch over the defect. A continuous suture pattern was placed in a counterclockwise direction, starting with the right ventricle, continuing across the vena cava and right atrium. While the tangential vascular clamp was left in place, the other half of the patch was sutured with another preplaced simple continuous pattern with double-armed 5–0 polypropylene suture. The suture went from the right ventricle and over the coronary groove and the right atrium. After the tangential vascular clamp was removed, the suture was tightened. The suture lines were tied where the opposite arms of suture met (Figure 3). No further bleeding from the right atrium was noted. The thorax was lavaged with warm saline and a 16 French chest tube was placed. The thoracic cavity was closed routinely. The mass and pericardium were submitted for histopathology and was consistent with HSA of the right auricle and secondary pericarditis.

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The patient lost approximately 500 mL of blood perioperatively, necessitating two packed red blood cell transfusion and one unit of fresh-frozen plasma. Postoperative complications included transient arrhythmias with no clinical significance. The patient was discharged from the hospital 48 hr after surgery on the following medications: tramadol (75 mg per os [PO] q 8 hr); carprofen (50 mg PO q 12 hr); and a 100 μg fentanyl patch. Two weeks after discharge from the hospital, treatment with intravenous carboplatin (270 mg/m² q 21 d for four doses) was initiated. Chemotherapy was tolerated well.

At the time of the fourth chemotherapy treatment, the patient was restaged. Restaging tests included a CBC, serum chemistry analysis, thoracic radiographs, and thoracic and abdominal ultrasound examinations. The CBC and chemistry were unremarkable, except for a mild elevation in alkaline phosphatase 317 mg/dL. Thoracic radiographs, thoracic ultrasound, and the abdominal ultrasound were within normal limits. Approximately 7 mo postoperatively, the patient re-presented to the referring veterinarian for exercise-associated coughing. Examination revealed decreased lung sounds. A cardiac mass and pleural effusion were evident on thoracic radiographs. An echocardiogram was performed, which showed a 5–6 cm mass believed to be arising from the right atrium. These findings were most consistent with recurrent HSA. At that time, the patient began palliative radiation therapy. An isocentric radiation treatment was performed using parallel opposed beams on a 6 megavoltage linear accelerator to deliver a dose of 6 Gy in a 12 cm × 12 cm field centered over the right atrium. The second dose of radiation was postponed due to inappetance. The patient was started on prednisone (10 mg PO q 12 hr). At presentation for her delayed radiation therapy, a recheck echocardiogram revealed progressive disease, as the mass had grown to measure 9 cm × 9 cm. The owner elected to discontinue radiation therapy and take the patient home. The dog's clinical condition worsened and she died at home 260 days post diagnosis. A necropsy was not performed.

Discussion

Pericardectomy as a treatment of atrial HSA prevents recurring cardiac tamponade, which is a life threatening condition. Dunning et al. (1998) report a median survival time of 16 days in dogs with HSA following pericardectomy and right atrial mass resection.² Right atrial mass resection is not associated with an increase in survival.² Atrial mass resection has been described as a treatment of cardiac HSA; however, it has not been shown to improve survival compared with either pericardectomy alone or dogs receiving no surgical treatment.^4–9

In one study of 23 dogs, median survival times were 43 days following right atrial mass resection and 118 days following right atrial appendage mass resection. Survival times were statistically improved at a median of 175 days when adjuvant chemotherapy was used.⁸ This median survival time of 175 days compares similarly to visceral splenic HSA treated with splenectomy and adjuvant chemotherapy.¹¹ There are not any studies evaluating the risks of pericardectomy without resection of an actively bleeding mass, as it is assumed one would not leave a bleeding mass unaddressed in the thorax. Pericardectomy is routinely recommended for heart base masses. Pericardectomy results in improved patient survival, even in the absence of pericardial effusion at the time of resection.^12,13 In the paper by Weisse et al. (2005), pericardectomy was performed in 91% (21) dogs receiving cardiac HSA resection. Pericardial closure was done in only two of these dogs.⁸ As a group, the dogs receiving a combination of pericardectomy, tumor resection, and adjuvant chemotherapy had statistically significant improved survival, noting that the true benefit of pericardectomy for cardiac HSA is not fully determined, as the two dogs with pericardial closure did not receive adjuvant chemotherapy in this paper.⁸

Brisson and Holmberg (2001) described autologous patch grafting for reconstruction of an atrial defect in a dog with atrial free wall HSA undergoing mass resection.⁹ The dog in that report died of metastatic disease 4 mo postoperatively. The clinical use of a pericardial patch graft has previously been implicated for the correction of pulmonic stenosis and tetrology of Fallot in dogs.^14–18 Pericardial patch grafting has also been reported for correction of myriad cardiac diseases in humans.^19–23

A pericardial patch was successfully applied to the right atrial wall of the dog described in this report following the rupture of the right wall after removal of an HSA. The technique previously described by Brisson and Holmberg (2001) used an inflow occlusion of the right heart prior to placement of the pericardial graft.⁹ In the case described herein, the patch was used as a rescue procedure when other techniques failed to repair a defect. Inflow and outflow occlusion were not necessary for a successful clinical outcome because a tangential vascular clamp was placed at the base of the right atrial appendage.

The dog in this report had an overall survival time of 9 mo postdiagnosis with adjunctive chemotherapy. Unfortunately, a necropsy was not performed and postmortem examination of the pericardial graft was therefore not obtained. Based on the relatively long-term survival of the patient postoperatively and evidence of disease progression, it is assumed that the patient died of metastatic disease and not failure of the pericardial graft.

It is not clear why the atrial tissue experienced tearing following placement of the stapling device, as it was applied without tension on the atrial tissue. Histopathologically, tumor cells appeared demarcated on the ex vivo specimen, making it less likely microscopic disseminated disease was present within the remaining atrium resulting in compromised tissue integrity. It is acknowledged that the atrium is susceptible to tearing regardless of handling technique or whether a manually sutured resection or stapled resection was performed.²⁴ Furthermore, as the residual atrial tissue proximal to where the stapler was applied was found to be extremely friable as rescue buttressed sutures were placed, it is not believed that preplacement of buttressed mattresses would have altered the outcome in this patient.

There are strong opinions and personal experiences regarding the success of atrial stapling versus manual resection, but there are only limited published studies in dogs to date. In a left atrial appendage exclusion device study evaluating such a device in mongrel dogs, right atrial stapling, not suturing, was used as the control treatment.²⁵ Also, in a nonrandomized study reviewing left atrial appendage occlusion in human patients, the use of a stapler resulted in better complete occlusion than in the manual sutured group with tearing occurring during routine manipulation prior to any intervention as well as in both the staple and suture groups.²⁴

Conclusion

An autologous pericardial patch graft can be used as a rescue technique without inflow and outflow occlusion during atrial mass resection. It may also be used to cover an unresectable right atrial mass to prevent cardiac tamponade with subsequent bleeding. This procedure may provide a more favorable outcome than previously reported in dogs with atrial HSA when combined with adjunctive therapy.