Introduction

Constrictive pericarditis is a rare cause of heart failure resulting from chronic fibrous thickening and at times calcific adhesions of the pericardium. The inelastic condition of the pericardium impedes ventricular filling particularly during late diastole and ultimately reduces cardiac output.¹ Constrictive pericarditis is often difficult to diagnose and differentiate from other conditions such as restrictive cardiomyopathy, but modalities such as echocardiography, magnetic resonance imaging and cardiac catheterization can be very helpful in making the diagnosis.² Patients initially present with fatigue, decreased exercise tolerance and shortness of breath secondary to heart failure. Progressive heart failure can eventually result in severe end-organ damage such as hepatic and/or renal failure.

Surgical pericardiectomy is the most effective treatment for constrictive pericarditis and is traditionally performed via median sternotomy on the arrested heart or occasionally via lateral thoracotomy.³ Both options are invasive with large incisions, significant postoperative pain and relatively long post-operative recovery. More importantly, traditional surgical management of constrictive pericarditis confers a mortality rate of up to 20% in some institutions.⁴

Minimally invasive cardiac surgery has become increasingly popular as a way to avoid morbidity associated with median sternotomy.⁵ Minithoracotomy has been performed with the aim of minimizing the mortality and morbidity associated with the sternotomy approach; however, this technique is still fairly invasive and sometimes confers limited exposure resulting in less effective resections. Thoracoscopy has also been reported as a modality for pericardiectomy but is extremely limited in the extent of dissection it allows and usually results in only partial excision of the paricardium. Partial pericardiectomy has been shown to be useful to treat pericardial effusion and in limited pericardiectomies but has not been shown to be successful for complete pericardiectomy.^6-9 Limitations of the thoracoscopic approach are likely due to lack of adequate instrument mobility/ dexterity and lack of complete visualization due to 2D vision and the inability to manipulate the heart.

We leveraged our experience in robotic beating heart totally endoscopic coronary artery bypass grafting (TECAB) from a left lateral approach with the aid of the EndoWrist Stabilizer (Intuitive Surgical, Sunnyvale, CA) to develop a similar robotic endoscopic approach for pericardiectomy.

New Technique

We have developed a novel approach to the surgical management of constrictive pericarditis using a totally endoscopic, robotic- assisted off pump technique.¹⁰ We have observed that the robotic approach affords improved visualization, which allows a more complete pericardial resection on the beating heart without the use of cardiopulmonary bypass. This has resulted in less postoperative pain, a shorter hospital stay, and earlier overall recovery for this procedure as well as for other robotic endoscopic procedures such as TECAB.^10,15 Most importantly (despite the relatively small numbers thus far) we have observed a lower than predicted early and midterm mortality rate. This can be explained by the fact that avoiding sternotomy/large incisions and cardiopulmonary bypass in these fairly sick patients (who have multiple comorbidities as a result of their constriction) can only be beneficial.

All operations are performed totally endoscopically on the beating heart using the da Vinci Si surgical system (Intuitive Surgical, Inc., Sunnyvale, CA). A left bronchial blocker is placed for single lung ventilation and carbon dioxide insufflation is used to expand the left chest at 8-10 cm H20 pressure and further facilitate visualization. Ports are placed in the second, fourth and sixth interspaces in the anterior axillary line (Figure 1). The middle port is used as a camera port and the other two are used as ports for the robotic arms. A fourth port is placed in the left subcostal area and is used as an assistant port for the EndoWrist Stabilizer. This instrument facilitates exposure of the various regions of the pericardium.

Figure 1: Robotic Pericardiectomy Port Placement. Ports from left to right are assistant port/stablizer port, robotic arm, camera port, second robotic arm.

First, the left phrenic nerve is identified. The pericardium posterior to it is incised using low electrocautery and then dissected to create a plane between the thickened pericardium and the epicardium. This is performed using a combination of blunt dissection and electrocautery (Figure 2). Dissection of the pericardium off the left ventricle (LV) continues posteriorly until the inferior vena cava (IVC) is reached. The posterior pericardium along the diaphragm is then removed as well. The EndoWrist Stabilizer is particularly useful to help lift the heart for better visualization during this portion of the operation. The dissection is then carried out anteriorly and pericardium is removed starting from the left phrenic and working towards the right phrenic releasing the anterolateral aspect of the LV up to the base of the heart. Once the left heart is fully released the dissection is carried over towards the right ventricle (RV) and pericardium is fully resected up towards and including the right atrium. The right phrenic nerve is visualized using the 30 degree 'down' scope after the right pleural space is entered. Extreme care is taken during the dissection in the vicinity of the left and right atrial appendages. Blunt dissection is facilitated by the Intuitive Irrigation tool (Intuitive Surgical, Inc., Sunnyvale, CA).

Figure 2: Pericardium is being removed posteriorly to the phrenic nerve.

The procedure is completed without heparinization therefore allowing for better hemostasis of the raw epicardial surface. Pericardial remnants are then removed via an Endo Catch Bag (Covidien, Minneapolis, MN) and a flexible chest drainage tubes are placed in each pleural space. The operative times for these procedures ranged from 4-5 hours.

The postoperative management is fairly straightforward. A minority of patients will require postoperative inotropic support and longer ICU stays if the constriction has been longstanding. We believe this is due to significant myocardial edema that results from releasing the constriction in these patients.

Discussion

Constrictive pericarditis can be a rapidly progressive and serious disease if not diagnosed early within its course. Surgery is the mainstay of treatment, although medical therapy can be attempted in early stages of disease.¹¹ Post-surgical mortality rates can be high and are quoted as being anywhere from 5 to 20% in the literature.^3,12 Patients particularly vulnerable to serious outcomes are those with radiation induced constrictive pericarditis while those with pericarditis from idiopathic cause have lower postsurgical mortality rates.

The traditional approach to pericardiectomy is via sternotomy on the arrested heart using cardiopulmonary bypass. This approach facilitates 'total pericardiectomy' which is usually defined as excision of the pericardium 'from phrenic to phrenic.' Total pericardiectomy has been shown to be more effective than anterior pericardiectomy alone in relieving symptoms, preventing progression of constrictive pericarditis as well as in long-term survival.^13,14

During the sternotomy approach however and despite arresting the heart, exposure of the posterior pericardium is not always easy. Therefore, parts of it are left behind in some cases with the justification that removal of the majority of the pericardium (i.e., the anterior part) will suffice in releasing the left and right ventricles enough to eliminate the patient's symptoms.

Another difficulty during the traditional surgical approach is the occasional inability to identify the correct plane of dissection to remove the actual constrictive layer. When this happens the constriction is not released and this may be an explanation of why some patients do not benefit from the procedure.

In our experience, the robotic assisted approach offers the benefit of increased dexterity and excellent visualization of the tissues. The magnified high definition 3D scope (which can be brought very close to the target area) allows a particularly excellent view of the pericardial-epicardial junction. This is essential in facilitating both a smooth and bloodless dissection to find the correct plane to provide adequate release of the constriction. As mentioned, this plane may be hard to identify with the naked eye during the traditional arrested heart open approach. We believe that performing the procedure on the full beating heart can improve the definition of this plane as the distinction between the epicardium (which moves with every heartbeat) and the constrictive layer of pericardium is made easier.

Additionally, the approach from the left pleural space affords an excellent view of the posterior pericardium (with gentle retraction of the heart upwards), which is unique from other surgical approaches. This allows for the removal of this part of the pericardium without having to arrest the heart, thus avoiding the complications of cardiopulmonary bypass.

Because of this we feel that the robotic approach facilitates not only 'total pericardiectomy' but in fact a more 'complete pericardiectomy' in that it removes more than the traditionally described 'phrenic to phrenic' pericardium.

In addition, the left sided approach allows for the left ventricle to be released first, which is a well-known surgical dictum during pericardiectomy and provides obvious hemodynamic advantages. Other benefits of our approach include the potential for decreased post-operative pain by avoiding sternotomy. Additionally, none of our patients required cardiopulmonary bypass, which is often a concern in patients who may have end organ damage such as renal failure, liver congestion and cirrhosis--conditions which may render the patient 'too high risk' to undergo corrective surgery.

In our series of 20 patients, including two high-risk patients, totally endoscopic robotic pericardiectomy was performed successfully with excellent results, zero mortality and no serious morbidity. All patients reported resolution of symptoms and improved quality of life.

One patient in our series bears mentioning, as the indication for pericardiectomy in her case was not constrictive. This young patient in her early 30s suffered for two years from idiopathic acute relapsing pericarditis with severe pain non-responsive to medical management including multiple pain medications as well as aggressive anti-inflammatory regimens. The surgical procedure in her situation was very simple (as the pericardium was not thickened or constrictive) yet the relief of symptoms was surprising and remarkable. She went from being practically bed ridden from pain (and pain medications) to resuming all activities within a matter of months postoperatively. We are getting more requests for surgery for this indication but continue to be cognizant of the paucity of data to support a surgical procedure in this extremely rare condition. It would seem that the least invasive option would be the most appropriate for this difficult group of patients.

Finally, a word of caution is warranted. Although we have found the robotic approach to pericardiectomy very effective in our hands and extremely beneficial to our patients, the one significant limitation is the need for a dedicated and experienced robotic cardiac surgical team to achieve the desired outcomes. This is a demanding and time-consuming procedure. Given that pericardiectomy itself is not a commonly performed operation, the team needs to be facile with the robotic approach in other procedures including coronary and valve surgeries.

In summary, we have found the robotic assisted off pump totally endoscopic approach to pericardiectomy to be very effective in releasing the constriction with less morbidity and mortality than the traditional approach.

References

1. Lin Y, Zhou M, Xiao J, Wang B, Wang Z. Treating constrictive pericarditis in a Chinese single-center study: a five-year experience. Ann Thorac Surg 2012;94:1235-40.
2. Kusunose K, Dahiya A, Popovic ZB, et al. Biventricular mechanics in constrictive pericarditis comparison with restrictive cardiomyopathy and impact of pericardiectomy. Circ Cardiovasc Imaging 2013;6:399-406.
3. Sengupta PP, Eleid MF, Kandheria BK. Constrictive pericarditis. Circ J 2008;72:1555-62.
4. Cohn LH, Edmunds LH. Cardiac Surgery in the Adult. New York: McGraw-Hill Medical, 2008.
5. Mack MJ. Minimally invasive and robotic surgery. JAMA 2001;285:568-72.
6. Bakos E, Bakos M, Dubaj M, Poliacik P. Miniinvasive treatmenet of pericardial effusions. Bratisl Lek Listy 2007;108:324-6.
7. Nakamoto H, Suzuki T, Sugahara S, Okada H, Kaneko K, Suzuki H. Successful use of thoracoscopic pericardiectomy in elderly patients with massive pericardial effusion caused by uremic pericarditis. Am J Kidney Dis 2001;37:1294-8.
8. Liem NT, Tuan T, Dung le A. Thoracoscopic pericardiectomy for purulent pericarditis: experience with 21 cases. J Laparoendosc Adv Surg Tech A 2006;16:518-21.
9. Luison F, Boyd WD. Three-dimensional video-assisted thoracoscopic pericardiectomy. Ann Thorac Surg 2000;70:2137-8.
10. Maciolek K, Asfaw ZE, Krienbring DJ, Arnsdorf SE, Balkhy HH. Robotic endoscopic off-pump total pericardiectomy in constrictive pericarditis. Innovations 2016;11:134-7.
11. Cho YH, Schaff HV. Surgery for pericardial disease. Heart Fail Rev 2013;18:375-87.
12. Syed FF, Schaff HV, Oh JK. Constrictive pericarditis--a curable diastolic heart failure. Nat Rev Cardiol 2014;11:530-44.
13. Chowdhury UK, Subramaniam GK, Kumar AS, et al. Pericardiectomy for constrictive pericarditis: a clinical, echocardiographic, and hemodynamic evaluation of two surgical techniques. Ann Thorac Surg 2006;81:522-9.
14. Avgerinos D, Rabitnokov Y, Worku B, Neragi-Miandoab S, Girardi LN. Fifteen-year experience and outcomes of pericardiectomy for constrictive pericarditis. J Card Surg 2014;29:434-8.
15. Balkhy HH, Wann LS, Krienbring D, Arnsdorf SE. Integrating coronary anastomotic connectors and robotics toward a totally endoscopic beating heart approach: review of 120 cases. Ann Thorac Surg 2011;92:821-7.

Keywords: Atrial Appendage, Carbon Dioxide, Cardiac Catheterization, Cardiac Output, Cardiac Surgical Procedures, Cardiomyopathy, Restrictive, Cardiopulmonary Bypass, Comorbidity, Constriction, Coronary Artery Bypass, Diaphragm, Diastole, Drainage, Dyspnea, Echocardiography, Edema, Electrocoagulation, Exercise Tolerance, Heart Failure, Heart Ventricles, Hemodynamics, Hemostasis, Heparin, Insufflation, Intensive Care Units, Length of Stay, Liver Cirrhosis, Magnetic Resonance Imaging, One-Lung Ventilation, Operative Time, Pain, Pain, Postoperative, Pericardial Effusion, Pericardiectomy, Pericarditis, Pericarditis, Constrictive, Pericardium, Phrenic Nerve, Quality of Life, Renal Insufficiency, Sternotomy, Thoracoscopy, Thoracotomy, Ursidae, Vena Cava, Inferior, Robotics

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