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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 2  |  Issue : 1  |  Page : 17-27

Indications, timing and techniques of radical pericardiectomy via modified left anterolateral thoracotomy (ukc's modification) and total pericardiectomy via median sternotomy (holman and willett) without cardiopulmonary bypass


1 Department of Cardiothoracic and Vascular Surgery, All Institute of Medical Sciences, New Delhi, India
2 Department of Cardiology, All Institute of Medical Sciences, New Delhi, India
3 Department of Cardiac Anaesthesia, All Institute of Medical Sciences, New Delhi, India

Date of Web Publication26-May-2016

Correspondence Address:
Ujjwal Kumar Chowdhury
Department of Cardiothoracic and Vascular Surgery, All India Institute of Medical Sciences, New Delhi - 110 029
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/2395-5414.182999

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  Abstract 

Background: Patients with constrictive pericarditis can be treated by pericardiectomy by either left anterolateral thoracotomy or median sternotomy. The terms “radical,” “total,” “extensive,” “complete,” “subtotal,” “adequate,” “near-total,” and partial pericardiectomy have been used often without much clarity. We describe our experience with a radical pericardiectomy technique via modified left anterolateral thoracotomy and compare the same to total pericardiectomy via median sternotomy. Methods: In this study, 67 (54.9%) patients underwent radical pericardiectomy via modified left anterolateral thoracotomy (Group I), and 55 (45.1%) patients underwent total pericardiectomy via median sternotomy (Group II). Results: The operative mortalities were 2.9% and 7.2% for the radical and total pericardiectomy groups, respectively. The time taken for normalization to Class I/II in Groups I and II was 30 ± 11 and 36 ± 14 days, respectively (P = 0.009). Surgical techniques did not affect the outcome of atrial fibrillation (P = 0. 77). Reoperation was not required for any patient. The radical pericardiectomy was also associated with less postoperative low cardiac output state as compared to patients undergoing total pericardiectomy (P < 0.001). There was no difference in mean duration of hospitalization; however, the radical pericardiectomy group achieved the New York Heart Association I and II Status quicker than the total pericardiectomy group (P = 0. 009). Conclusions: We conclude that using several technical modifications of pericardial excision, it is possible to achieve radical pericardiectomy via modified left anterolateral thoracotomy, particularly removing the constricting pericardium over the anterolateral, diaphragmatic surfaces of left ventricle and the anterior and diaphragmatic surfaces of the right ventricle until the right atrioventricular groove without using cardiopulmonary bypass in the great majority of patients undergoing pericardiectomy for chronic constrictive pericarditis. Although the surgical approach for pericardiectomy is based on surgeon's preference, left anterolateral thoracotomy is the preferred and noncontroversial approach in the setting of purulent pericarditis and effusive constrictive pericarditis to prevent sternal infection. We recommend median sternotomy approach with or without cardiopulmonary bypass, in the setting of calcific pericardial patches, pericardial masses, reoperations, and calcific pericardial “cocoon” and for those with predominant right-sided and annular involvement.

Keywords: Anterolateral thoracotomy, pericardiectomy, median sternotomy


How to cite this article:
Chowdhury UK, Narang R, Malhotra P, Choudhury M, Choudhury A, Singh SP. Indications, timing and techniques of radical pericardiectomy via modified left anterolateral thoracotomy (ukc's modification) and total pericardiectomy via median sternotomy (holman and willett) without cardiopulmonary bypass. J Pract Cardiovasc Sci 2016;2:17-27

How to cite this URL:
Chowdhury UK, Narang R, Malhotra P, Choudhury M, Choudhury A, Singh SP. Indications, timing and techniques of radical pericardiectomy via modified left anterolateral thoracotomy (ukc's modification) and total pericardiectomy via median sternotomy (holman and willett) without cardiopulmonary bypass. J Pract Cardiovasc Sci [serial online] 2016 [cited 2018 Dec 18];2:17-27. Available from: http://www.j-pcs.org/text.asp?2016/2/1/17/182999


  Introduction Top


Pericardiectomy is the only accepted treatment for chronic constrictive pericarditis. The idea of resecting pericardium for constrictive pericarditis dates back to 1898 when DeLorme first suggested it. However, the German group Rehn and Sauerbruch in 1913 performed successful pericardial resection for constrictive pericarditis through a left anterolateral thoracotomy approach.[1] The operative approaches used by Churchill and later by Harrington are now of historical interest. Other surgical approaches for pericardiectomy include left anterolateral thoracotomy, median sternotomy, or a U-incision with the base of “U” at the left sternal border (Harrington's approach) and bilateral anterolateral thoracotomy.[2],[3]

Despite the experience spanning over 100 years, there is no foolproof formula in the published literature that can be used in deciding an optimal approach for a given patient. The literature is rife with examples of patients with constrictive pericarditis treated by pericardiectomy by either left anterolateral thoracotomy or median sternotomy. Despite the effectiveness of surgical therapy for the treatment of constrictive pericarditis, there are disparate opinions regarding the role of corticosteroids in the treatment of tuberculous pericarditis, timing of operation, issue of surgical approach, extent of decortication, and requirement of cardiopulmonary bypass.[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19]

The efficacy of pericardiocentesis in preventing chronic constrictive pericarditis in pericardial effusion (serous/or hemorrhagic) has been inadequately investigated. The problems of perioperative diagnostic error also have not been adequately addressed in the surgical literature despite known difficulties in differentiating patients with restrictive cardiomyopathy from those with constriction.[18],[20],[21],[22] In our study, constrictive pericarditis was considered to be hemodynamically significant when there were clinical features of constriction with supportive echocardiographic and hemodynamic criteria as outlined earlier.[23] Echocardiographically, pericardial thickness of more than 3 mm was generally considered significant. A constrictive pattern was defined as 25% or greater increase in mitral E-velocity with expiration as compared with inspiration and an augmented (25%) or more diagnostic flow reversal in the hepatic vein after the onset of expiration compared with inspiration.[23]

Computed tomography with predominant use of an ultrafast scanner and magnetic resonance imaging (MRI) are superior imaging modalities for detection of pericardial calcification as well as the often asymmetric pericardial thickening.[24],[25],[26] In addition, MRI defines the typical cardiac morphological characteristics and the presence of myocardial atrophy/fibrosis.[24],[25],[26]

Reports addressing the issue of surgical approach, extent of pericardiectomy, and postoperative hemodynamics are limited and controversial.[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17] The terms “radical,” “total,” “extensive,” “complete,” “subtotal,” “adequate,” “near-total,” and partial pericardiectomy also have been variably used in the literature to describe the procedure to be performed, often without precise definition of the limits of pericardial resection.[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17]

Published reports attest to the unpredictable and variable pattern of constrictive pericarditis and lend support to radical decortication. In 2005, for uniformity with other studies, total pericardiectomy was defined as wide excision of the pericardium with the phrenic nerves defining the posterior extent, the great vessels including the intrapericardial portion of superior vena cava and superior vena cava-right atrial junction defining the superior extent, and the diaphragmatic surface, including the inferior vena cava-right atrial junction defining the inferior extent of the pericardial resection.[23] Constricting layers of the epicardium were removed whenever possible. The atria and venae cavae were decorticated as a routine in all cases in this study group. Pericardiectomy was considered partial if both ventricles could not be decorticated completely because of dense myopericardial adhesions or calcification.[23] Radical pericardiectomy would be defined as removal of the entire pericardium over the anterolateral, diaphragmatic surfaces of left ventricle, portion of pericardium posterior to the phrenic nerve and the left ventricle, and the anterior and diaphragmatic surfaces of right ventricle until the atrioventricular groove leaving behind intact left and right phrenic pedicles.

Second, the importance of unrecognized constricting epicardial (visceral pericardial) peel was described by Harrington in 1944, and successful pericardiectomy requires decortication of the ventricular epicardium and relief of all constricting layers.[3] In one study, pressure-volume loops were monitored intraoperatively during pericardiectomy for constrictive pericarditis. The intraoperative normalization of the pressure-volume loop was used as an indicator of operative success.[26]

Tuberculosis continues to be the leading cause of chronic constrictive pericarditis in developing countries with a reported incidence of 38–83%. Due to the emergence of drug-resistant strains of tuberculosis in association with AIDS, that number is increasing.[7],[27],[28] The advent of antitubercular chemotherapy brought down the mortality from tubercular pericarditis from 90% to about 40%.[7],[13],[25],[26] In patients with tubercular pericarditis, our policy is to institute antitubercular chemotherapy for a minimum period of 12 months.

Several investigators including ourselves have advocated early pericardiectomy after the clinical symptoms and diagnosis have been confirmed before the occurrence of severe constriction and myocardial atrophy.[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23] In 2005, we attempted to compare two surgical approaches for the treatment of chronic constrictive pericarditis, i.e., median sternotomy and left anterolateral thoracotomy among 395 patients. The surgical approach was primarily based on surgeon preference and remained uniform in our previous study. However, the median sternotomy approach was the preferred option in the following clinical scenario: (1) annular constrictive pericarditis, (2) extracardiac intrapericardial mass, (3) presence of a gradient between the superior and inferior venae cavae and right atrium 2 mmHg or greater, (4) calcific pericardial patch compressing the right atrium and right ventricular outflow tract, (5) constriction after previous open heart surgery, (6) circumferential “cocoon” calcification of the pericardium, and (7) recurrent constrictive pericarditis after partial pericardiectomy.[23]


  Methods Top


We report our surgical experience with 67 patients who underwent radical pericardiectomy via modified left anterolateral thoracotomy (Group I), and 55 patients who underwent total pericardiectomy via median sternotomy (Group II).

In this study, we demonstrated that the maximum benefit for chronic constrictive pericarditis, in particular, is expected from total pericardiectomy, which is best achieved through a median sternotomy and is very difficult if not impossible through a conventional left anterolateral thoracotomy.

We concur with the observations of previous investigators that routine use of cardiopulmonary bypass to achieve total pericardiectomy is unnecessary and should be employed only in special circumstances, namely (1) inadvertent damage to a cardiac chamber, (2) those who have had a previous cardiac operation or a previous partial pericardiectomy, (3) presence of calcific pericardial “cocoon” encompassing all cardiac chambers, (4) patients requiring pericardiectomy following mediastinal irradiation, and (5) presence of a coexistent cardiac lesion that requires correction.[14],[15],[23],[29]

However, a left anterolateral thoracotomy was the preferred approach in cases of purulent pericarditis and effusive-constrictive pericarditis. Thoracotomy was the preferred option in these patients because of the presence of concomitant pyothorax and the concerns of sternal infection. We could achieve total pericardiectomy in these patients because of loculations and poorly formed adhesions which could be easily pealed off.[23],[27],[29]

Patients undergoing creation of a pleuropericardial window for pericardial effusion, pericardial biopsy, and concomitant pericardiectomy with repair of congenital or acquired heart diseases were excluded from this study.

Criteria for decision-making and selection of surgical approach for patients undergoing radical pericardiectomy via left anterolateral thoracotomy without cardiopulmonary bypass

In our previous study, we compared the outcomes after total versus partial pericardiectomy. Our study demonstrated that total pericardiectomy was associated with decreased operative mortality (P = 0.02), less postoperative low-output syndrome (P < 0.001), abbreviated hospitalization (P < 0.001), and better long-term survival than partial pericardiectomy (P = 0.004). Ascites, low ejection fraction (0.40 or less), renal dysfunction, hyperbilirubinemia, higher preoperative right atrial pressure (>24 mmHg), atrial fibrillation, pericardial calcification, tricuspid regurgitation and mitral regurgitation, partial pericardiectomy, thoracotomy approach, and postoperative low-output syndrome were significant negative factors for survival according to univariate and multivariate analyses. The risk of death was 4.5 times higher (95% confidence interval [CI]: 2.05–9.75) in patients undergoing partial pericardiectomy as compared to total pericardiectomy.[23]

Interestingly, despite total pericardiectomy, the operative mortality rate was 7.6% in our series and 6–19% in several large series published after 1985.[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[23] Unlike others, there was no effect of age, tuberculous etiology, and advanced New York Heart Association (NYHA) symptoms on late survival in our series presumably because of our young patient population and timely institution of chemotherapy and surgery.[23] Reoperations for recurrent constrictive pericarditis after partial pericardiectomy are common.[14],[16] Published reports attest to the unpredictable and variable pattern of constrictive pericarditis and lend support to thorough and radical decortication.[15],[16]

Although the median sternotomy approach allowed a more radical clearance of pericardium overlying the right atrium and venae cavae including the cavoatrial junctions, these areas usually are of little hemodynamic significance in the majority of patients. Furthermore, it is impossible to excise the portion of the pericardium posterior to the phrenic nerve using this approach.

As enunciated above, the median sternotomy approach was the preferred option of the author (UKC) in the selected heterogeneous group of patients undergoing pericardiectomy. To decrease the hospital mortality rates of 7.6% and postoperative low-output syndrome, the author proceeded to perform several technical modifications of the conventional left anterolateral thoracotomy approach to achieve further radical excision of the pericardium posterior to the phrenic nerve and diaphragmatic pericardium. Thus, there were seven forces driving our decision-making for improvement of the results of patients undergoing pericardiectomy via modified anterolateral thoracotomy.

  • The desire to obtain improved operative exposure of the right ventricle and right atrium by developing a new dissection plane between the posterior surface of the sternum and anterior surface of the pericardium
  • The desire to dissect the pericardium posterior to the phrenic nerve overlying the left atrium and posterolateral surface of the left ventricle
  • The desire to develop a new cleavage plane between the diaphragmatic pericardium and diaphragm
  • The desire to minimize cardiac manipulation at the time of dissection by dividing the anterior and posterior pericardial flap into two halves, respectively
  • The desire to minimize postoperative autotransfusion by inserting a peritoneal dialysis catheter before surgical incision and placing it on gravity drainage intraoperatively
  • The desire to maintain oxygenation and hemodynamic stability during pericardiectomy via left anterolateral thoracotomy by placing an intercostal chest drain on the opposite side in case of right-sided significant pleural effusion
  • The desire to keep both groins prepared at the time of pericardiectomy via modified left anterolateral thoracotomy in case of inadvertent injury to the cardiac chambers and/or great vessels and urgent requirement of the institution of cardiopulmonary bypass.


Surgical management

Radical pericardiectomy for chronic constrictive pericarditis via left anterolateral thoracotomy (UKC's modification)

The operation

  1. Step I: Positioning of the patient

    • The patient is prepared for left anterolateral thoracotomy with the patient tilted slightly to the right. Both the groins are positioned and draped for emergent exposure of the femoral vessels and institution of cardiopulmonary bypass if required
    • The submammary incision, with entry into the chest via fourth or fifth intercostal space, gives excellent access to the left ventricle, left atrium, and right ventricle. Transfixation and division of left internal thoracic artery are required in most patients. In our experience, we do not transect the sternum to gain exposure to right ventricle and right atrium across midline but employ several maneuvers as described below to facilitate exposure to the right-sided cardiac chambers with certainty and safety. It is important to divide the intercostal muscles posteriorly almost till the angle of the ribs to facilitate opening of the retractor blade without causing any rib fractures
    • A scapular/deep bladed retractor is used to retract the muscles of the lateral thoracic wall to facilitate undercutting of the intercostal muscles [Figure 1]a.
    Figure 1: (a) Intraoperative views of the steps of radical pericardiectomy via left modified anterolateral thoracotomy (UKC's modification). The chest is opened through the 4th intercostal space. (b) A large wet sponge is placed over the left lung and retracted posteriorly to facilitate exposure. The excessive fat overlying the left ventricular apex is removed and the left phrenic neurovascular pedicle is identified. (c and d) A new dissection plane is developed between the sternum and the anterior surface of the pericardium. (e) The new dissection plane is extended beyond the midsternum to the right phrenic pedicle. (f) A new cleavage plane is created between the diaphragmatic pericardium and diaphragm.

    Click here to view


  2. Step II: Removal of the excessive fat overlying the left ventricular apex and left phrenic nerve, subtotal thymectomy

    • A large wet abdominal sponge is placed over the left lung and retracted posteriorly to facilitate exposure. It is important to identify the left phrenic neurovascular pedicle after removing the large amount of fat which usually overlies left ventricular apex in proximity to the left phrenic nerve
    • The thymus is routinely dissected off the pericardium to facilitate exposure of the pericardium over the ascending aorta and pulmonary artery. The thymus is excised subtotally, transfixing the superior pole of the thymic gland [Figure 1]b.


  3. Step III: Development of a new dissection plane between the sternum and the anterior surface of the pericardium

    • It is important to retract the posterior table of the sternum using a right-angled deep blade retractor and a new dissection plane is developed using cautery between the sternum and the anterior surface of the pericardium [Figure 1]c and [Figure 1]c.


  4. Step IV: Extension of the dissection plane beyond the midsternum to the right phrenic pedicle

    • Three tissue forceps or three No. 1 silk sutures are employed over the anterior portion of the pericardium to facilitate traction thereby extending the newly developed dissection plane beyond the midsternum to the right phrenic pedicle [Figure 1]e.


  5. Step V: Development of a new cleavage plane between the diaphragmatic pericardium and diaphragm

    • Using cautery dissection, a new cleavage plane is partially developed between the diaphragmatic pericardium and diaphragm [Figure 1]f.


  6. Step VI: Mobilization and isolation of the left phrenic pedicle

    • After exposing the pericardium, two full-length parallel incisions are made using a cautery with low voltage (around 8–10 mV), 0.5 cm anterior and posterior to the left phrenic neurovascular pedicle and extended until the level of the pulmonary artery superiorly and diaphragm inferiorly. Multiple silk stay sutures are placed on the incised pericardial edges anteriorly and posteriorly to achieve exposure and the left phrenic pedicle was thereafter isolated using two vessel loops [Figure 2]a.
    Figure 2: (a) Two full-length parallel excisions are made using a cautery 0.5 cm anterior and posterior to the left phrenic pedicle and extended up to the pulmonary artery superiorly and diaphragm inferiorly. (b and c) The pericardium posterior to the phrenic nerve is dissected and raised from the posterolateral surface of the left ventricle and left atrial appendage. The midportion of the posterior pericardium is divided at the center into two halves. (d and e) The pericardium anterior the phrenic nerve is subsequently raised from the left ventricle, right ventricle, and pulmonary artery and divided into two halves in between stay sutures to minimize intermittent cardiac compression. The anterior flap is excised 0.5 cm anterior to right phrenic nerve till the pulmonary artery superiorly and the inferior vena cava-right atrial junction inferiorly. (f) Inferiorly, a new cleavage plane is developed between the diaphragm and thickened pericardium and the entire width of the diaphragmatic pericardium is excised in toto.

    Click here to view


  7. Step VII: Dissection of the pericardium posterior to the left phrenic nerve and division of the posterior pericardium in two halves

    • Posteriorly, the pericardium was gently dissected and raised from posterolateral surface of the left ventricle and left atrial appendage. The midportion of the posterior pericardial flap was subsequently divided at the center into two halves to facilitate adequate mobilization until the levels of left-sided pulmonary veins and excised [Figure 2]b and [Figure 2]c.


  8. Step VIII: Dissection of the pericardium anterior to the phrenic nerve and division of the anterior pericardium in two halves

    • Using cautery at 8–10 mV, the anterior pericardial flap (APF) was thereafter raised from the right ventricle and pulmonary artery. Four to five silk stay sutures on the anterior pericardial edge are extremely helpful during the process of dissection
    • APF was subsequently divided into two halves at the center to minimize intermittent cardiac compression and unstable hemodynamics. While raising APF, the surgeon should be more cautious to avoid injury to the dilated and thinned right atrium and inferior cavoatrial junction
    • Anteriorly, the pericardium is dissected until about 0.5 cm anterior to the right phrenic nerve. The anterior flap was thereafter excised till the level of the ascending aorta superiorly and inferior vena cava-right atrial junction inferiorly [Figure 2]d and [Figure 2]e.


  9. Step IX: Development of a new cleavage plane between the diaphragmatic pericardium and diaphragm

    • Inferiorly, a new cleavage plane is made to develop between the diaphragm and thickened pericardium all along its length. Loculated pus may be encountered at this time or subsequent stages in the dissection. Three to four silk stay sutures are placed on the edge of the diaphragmatic pericardium dividing into two halves. Dissection is done between the pericardium and diaphragmatic surface of the right ventricle including the left ventricle. The apex is completely freed from the pericardial adhesions. After the cardiac chambers are freed off the underlying adhesions, the entire width of diaphragmatic pericardium is excised in toto taking special precaution near the inferior cavoatrial junction [Figure 2]f and [Figure 3]a,[Figure 3]b,[Figure 3]c
    • All constricting epicardial layers are peeled off the cardiac chambers and great vessels taking care not to injure the underlying structures including the coronary arteries and veins
    • Calcific plaques, bars, and circumferential patches of calcified pericardium were divided with a rongeur or a thick hemostat and were removed avoiding injury to the phrenic nerves and the underlying vascular structures. Isolated calcific deposits burrowing deeply into the ventricular muscle may be safely left in situ.
Figure 3: (a) Inferiorly, a new cleavage plane is developed between the diaphragm and thickened pericardium and the entire width of the diaphragmatic pericardium is excised in toto. (b and c) Intraoperative pictures of the decorticated heart with an intact phrenic pedicle and the excised pericardium. (d) Intraoperative views of the steps of total pericardium via median sternotomy. The chest is opened through the mid-sternotomy incision. (e) Both pleural spaces are entered to visualize both phrenic nerves and to decompress the pleural effusion. (f) An I-shaped incision is made in the midline over the pericardium up to the level of the pulmonary artery superiorly and diaphragm inferiorly.

Click here to view


Specific useful maneuvers to facilitate radical pericardiectomy via left anterolateral thoracotomy

  • In patients with massive ascites and right or bilateral pleural effusion, it is the author's practice to place an indwelling peritoneal dialysis catheter in the peritoneal cavity before thoracotomy. An intercostal chest drain on the right side of patients with massive right-sided pleural effusion facilitates placement of the patient in left lateral position without compromising with ventilation. An indwelling peritoneal dialysis catheter helps in removal of the third space fluid after completion of the pericardiectomy. This minimizes autotransfusion after the procedure is over, thereby prevents cardiac dilatation and low cardiac output in the perioperative period. The general belief of acute sudden circulatory collapse following sudden decompression of the third space has been unfounded in our experience.


Total pericardiectomy for chronic constrictive pericarditis via median sternotomy

The operation

  • Step I: Subtotal thymectomy, mobilization of the pleural reflection


  • The thymus is subtotally excised to expose the pericardium overlying the aorta and pulmonary artery. Subsequently, the thymus and pleural reflection are mobilized laterally to obtain a wide width of pericardium [Figure 3]d.


  • Step II: Identification of both phrenic pedicles


  • Both pleural spaces are entered to visualize both phrenic nerves and decompress the pleural effusion if present. It is important to remove the large amount of fat which usually overlies the left ventricular apex in proximity to the left phrenic nerve [Figure 3]e.


  • Step III: I-shaped midline incision over the pericardium


  • The pericardium was inspected and palpated to determine a soft and uncalcified area. An I-shaped incision was made in the midline over the pericardium up to the level of the pulmonary artery superiorly and diaphragm inferiorly [Figure 3]f.


  • Step IV: Development of a dissection plane between the pericardium and the heart


  • The dissection of the pericardium of the heart was done using cautery until the fibrous pericardium along with its serous layer. When it is done properly, there is clear visualization of the epicardial fat and the coronary arteries. Inability to visualize the coronaries indicates that the dissection plane is not deep enough, i.e., the epicardial peel of Allison is intact
  • It is important to set the cautery between 8 and 10 mV during the process of dissection to avoid cautery-induced ventricular fibrillation. Multiple silk stay sutures were then placed on the cut edges of the incised pericardium. The pericardium was initially divided at the bottom portion close to the diaphragmatic reflection over the right ventricle, and the lateral pericardial flap was raised superiorly and laterally. If calcified plaques or spicules penetrating the epicardium were present, these were left behind with islands of calcified pericardium, making numerous scores over the patch. Circumferential patches of calcified pericardium were crushed with a thick hemostat and/or bone cutter and were removed avoiding injury to the underlying vascular structures, coronaries, and phrenic nerves. We have not used either cavitational ultrasonic surgical aspiration system for removal of calcium or nerve stimulator for identification of the phrenic nerve on any patient in this study [Figure 4]a
  • Although some surgeons grasp the edges of the incised pericardium with a Kocher or Alice Clamp, we use multiple silk stay sutures for holding the edges for traction. Retraction of the heart can be done with the left hand using a wet sponge on the heart by the operating surgeon or a sponge forceps held by the assistant.
Figure 4: (a) The pericardium overlying the anterior surface of the right ventricle and left ventricular apex is dissected off the heart along with its serous layer with clear visualization of the epicardial fat and coronary arteries. The pericardium is initially divided at the bottom portion closed to the diaphragmatic reflection. (b-d) The anterior pericardial flap is divided into two halves in the middle who facilitate mobilization with minimal intermittent cardiac compression. The left phrenic neurovascular pedicle is identified and a full-length incision is made 0.5 cm anterior to the pedicle which will be the posterior extent of pericardial excision. (e) A plane is developed between the diaphragmatic pericardium and diaphragm in between stay sutures. (f) The pericardium is divided into two halves and dissected off the diaphragm.

Click here to view


  • Step V: Creation of the pericardial flap on the left side and division of the same in two halves


  • Generally, I prefer to start mobilization of the pericardium at the lower end of “I” incision on the left side and proceed upward toward the aorta till the lower border of the brachiocephalic vein creating a flap of about 1 cm width
  • At this point, the flap is divided at the midportion to facilitate mobilization with minimal compression/manipulation of the cardiac chambers/great vessels, thereby minimizing/maintaining hemodynamic stability. Thus, the dissection proceeds laterally. The posterior extent of this dissection line is approximately 1 cm anterior to the left phrenic nerve
  • It is important to remember that the left phrenic pedicle frequently has a more anterior course than expected. Although same centers periodically stimulate the left phrenic nerve with a nerve stimulator, we have not used the same. The left anterior interventricular coronary artery should be well visualized in the operative field [Figure 4]b,[Figure 4]c,[Figure 4]d.


  • Step VI: Mobilization of the diaphragmatic pericardium and release of left ventricular apex


  • Regardless of the diagnosis, a plane is developed between the diaphragmatic pericardium and the diaphragm. Three to four silk stay sutures are placed on the edge of the diaphragmatic pericardium dividing into two halves
  • Dissection is done between the pericardium and posterolateral left ventricular wall and along the inferior walls of the left and right ventricles. Posterolaterally, the pericardium posterior to the left phrenic nerve down to the left-sided pulmonary veins is dissected and excised. Generally, there is a greater hemodynamic compromise while removing the diaphragmatic pericardium [Figure 4]e.


  • Step VII: Excision of the diaphragmatic pericardium


  • Finally, the diaphragmatic pericardium on the right side is dissected off the diaphragm avoiding injury to the dilated and thinned inferior vena cava. The edges of the incised pericardium are treated gently with electrocautery to obtain hemostasis. The pericardial and pleural cavities are irrigated with normal saline [Figure 4]f.


  • Step VIII: Creation of the pericardial flap on the right side and division of the same in two halves


  • Next, the dissection proceeds laterally on the right side in a similar fashion as we did on the left side. Its important to divide the right pericardial flap in the midportion and surgeon should be more cautions to avoid injury to the right atrium or inferior vena cava/inferior cavoatrial junction. Due to the thinness and dilatation, these structures are more vulnerable to injury during dissection. The pericardial reflection overlying the intra- and extra-pericardial junction of superior vena cava is incised as a routine. The posterior extent of the dissection line is approximately 1 cm anterior to right phrenic nerve [Figure 5]a,[Figure 5]b,[Figure 5]c,[Figure 5]d.
Figure 5: (a and b) The right phrenic neurovascular pedicle is identified and a full-length incision is made 0.5 cm anterior to the right phrenic nerve till the superior cavoatrial junction superiorly and inferior cavoatrial junction inferiorly. The right-sided pericardial flap is divided into two halves and excised freeing the superior and inferior cavoatrial junctions. The surgeon should be more cautious on the right side due to the thinness and dilatation of the right atrium. (c and d) Intraoperative pictures of the decorticated heart and the excised pericardium.

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Definitions and acceptable normal values

For uniformity with other studies, total pericardiectomy was defined as wide excision of the pericardium with the phrenic nerves defining the posterior extent, the great vessels including the intrapericardial portion of superior vena cava and superior vena cava-right atrial junction defining the superior extent, and the diaphragmatic surface, including the inferior vena cava-right atrial junction defining the inferior extent of the pericardial resection.[23] Radical pericardiectomy was defined as excision of the pericardium as defined under total pericardiectomy including the removal of the pericardium posterior to the phrenic nerve and the diaphragmatic pericardium. Constricting layers of the epicardium were removed whenever possible. The atria and venae cavae were decorticated as a routine in all cases in this study group. Pericardiectomy was considered partial if both ventricles could not be decorticated completely because of dense myopericardial adhesions or calcification.[23],[29]

Constrictive pericarditis was considered to be hemodynamically significant when there were clinical features of constriction with supportive echocardiographic and hemodynamic criteria as outlined earlier. Perioperative mortality was defined as that occurring within 30 days after surgery. Cardiac-related death was defined as death due to cardiac causes such as progressive congestive heart failure (CHF).[23],[29]

Transthoracic two-dimensional, color-flow Doppler echocardiographic studies were performed on all patients before and after the operation. Mitral, tricuspid, superior vena cava, hepatic vein, and pulmonary flow velocities were measured. Mitral or tricuspid regurgitation was assessed semi-quantitatively as Grade 1 + to 4+. Ejection fraction was calculated using modified Quinones method. A constrictive pattern was defined as 25% or greater increase in mitral E-velocity with expiration as compared with inspiration and an augmented (25% or more) diastolic flow reversal in the hepatic vein after the onset of expiration compared with inspiration.

Low-output syndrome was diagnosed if the patient required inotropic support dopamine (4–10 µg/kg/min), dobutamine (5–10 µg/kg/min), epinephrine (0.01–0.1 µg/kg/min), milrinone (50 µg/kg intravenous bolus followed by 0.375–0.75 µg/kg/min), either isolated or in combination, in the operating room or intensive care unit to maintain stable hemodynamics in the absence of mechanical external compression after correction of all electrolytes or blood gas abnormalities and after adjusting the preload to its optimal value. Low-output syndrome was also diagnosed if there was an increasing requirement of the above-mentioned inotropes along with afterload reduction with sodium nitroprusside. Patients who received < 4 µg/kg/min of dopamine to increase renal perfusion were not considered to have low-output syndrome.

Patients characteristics

The patients were entered in the study protocol after informed consent had been obtained from patients or guardians. All patients in this study population were operated on a single surgeon (UKC) making uniformity in the surgical protocol possible. One hundred and twenty-two consecutive patients undergoing pericardiectomy for chronic constrictive pericarditis from January 2005 and December 2015 were included in this prospective study; in this study, 67 (54.9%) patients underwent radical pericardiectomy via modified left anterolateral thoracotomy (Group I) and 55 (45.1%) patients underwent total pericardiectomy via median sternotomy (Group II). Their demographic and clinical profiles are depicted in [Table 1].
Table 1: Demographic, operative, and postoperative data of the study group

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Patients age at operation ranged from 15 to 58 years (mean ± standard deviation [SD], 31.84 ± 14.62 years). Duration of symptoms ranged from 5 to 60 months (mean ± SD, 17.45 ± 12.9 months). Preoperatively, 82 (67.2%) patients were in NYHA-III and 40 (32.8%) were in NYHA-IV.

All patients had CHF as predominant symptom. Eighty-nine (72.9%) patients started to have chest pain, 3 (2.5%) had evidence of cardiac tamponade, and supraventricular arrhythmias were found in 42 (34.4%) patients. Ninety percent had distended jugular veins, 80% ascites, 86% hepatomegaly, 45% pleural effusion, and 30% had pulsus paradoxus. Five out of 122 patients required tapping and steroid therapy for recurrent pericardial effusion. All patients with tuberculosis (n = 88) received multidrug therapy (isoniazid, rifampicin, ethambutol, and pyrazinamide) for 9 months. Before operation, all patients were on digitalis and diuretics. Two (1.6%) patients were diagnosed to have recurrent chronic constrictive pericarditis 5 years after pericardiectomy via left anterolateral thoracotomy done at another center. The etiology was considered tubercular if the histopathology of the excised pericardium showed granulomas, caseation, giant cells (n = 82; 67.2%) or if the fluid and debris removed at surgery were positive for acid-fast bacilli (n = 6; 4.9%) or if gene expert analysis was positive for tuberculosis. A history of pulmonary tuberculosis and lymph node tuberculosis was present in 68 (55.7%) and 9 (7.4%) patients, respectively. The demographic characteristics of both groups of patients did not reach statistical significance.

Laboratory investigations showed elevated erythrocyte sedimentation rate (range 40–90 mm at 1 h) in 102 (83.6%), renal dysfunction (serum creatinine > 2 mg/dl) in 41 (33.6%), and hyperbilirubinemia in 35 (28.7%) patients. Chest roentgenogram revealed pericardial calcification in 40 (32.8%), pleural effusion in 40 (32.8%), and pulmonary infiltrates in 13 (10.6%) patients. The calcification was distributed over the anterior and inferior surfaces of the heart in 37 (30.3%) and all around the heart like cocoon in 4 (3.3%) patients.

Electrocardiogram demonstrated low voltage QRS complex (n = 86), flattening or T-wave inversion (n = 82), atrial fibrillation (n = 41), and premature ventricular contraction (n = 9). Although these changes were present in the majority of patients, they appeared nonspecific. Echocardiography revealed pericardial thickness (>3 mm, n = 89), inferior vena cava dilatation (n = 97), right atrial enlargement (n = 99), abnormal septal motion (n = 89), >25% increase in mitral inflow velocity with expiration compared with inspiratory phase (n = 97), moderate mitral regurgitation (Grade 2+, n = 21), and moderate tricuspid regurgitation (Grade 2, n = 19).

Preoperative cardiac catheterization was performed in eight patients. The rest did not have catheterization either because of their Class IV symptoms with renal dysfunction or the echocardiographic findings were unequivocal. All demonstrated the findings consistent with constrictive pericarditis because of an elevated right atrial pressure, usually with an M- or W-shaped contour, and abnormally high right ventricular end-diastolic pressure with a characteristic dip-plateau diastolic configuration, equalization of end-diastolic pressure in all cardiac chambers, and a ratio of right ventricular end-diastolic to right ventricular systolic pressure of > 0.30.

Statistical analysis

Data were analyzed with SPSS 10.0 statistical package (SPSS, Chicago, Illinois, USA). Continuous and interval-related data are presented as the mean ± SD whereas categorical variables are presented as frequency distribution and percentages. Qualitative data were analyzed by using the Chi-square test or Student's t-test. Mortality rates were calculated depending on the total number of years of follow-up for each patient. Actuarial estimates were calculated using the Kaplan–Meier technique. The log-rank test was performed to analyze statistically difference of survival between patients undergoing radical versus total pericardiectomy. A probability value of 0.05 or less was considered statistically significant.


  Results Top


The operative mortalities were 2.9% and 7.2% for the radical and total pericardiectomy groups, respectively. The deaths (n = 6, 4%) were due to intractable low cardiac output (Group I, n = 2; Group II, n = 4) in both groups of patients culminating in hepatorenal syndrome and multisystem failure. Two of these patients also had refractory ventricular arrhythmias. Postoperative echocardiography revealed increased biventricular dimensions, abnormal diastolic filling pattern with raised right atrial pressure.

All patients were routinely started on dopamine (4 µg/kg/min) to increase renal perfusion on operation table after completing excision of the thickened pericardium. Patients considered to have low-output syndrome (n = 56) required dopamine (4–10 µg/kg/min), epinephrine (0.01–0.1 µg/kg/min), and milrinone (50 µg/kg intravenous bolus followed by 0.375–0.75 µg/kg/min) either isolated or in combination. Median duration of inotrope requirement was 4 days (range 2–7 days) in these patients. Patients with normal renal function were administered oral angiotensin-converting enzyme (ACE) inhibitors before weaning from inotropic agents.

There was marked reduction of filling pressure within 24 h in both groups of patients undergoing radical and total pericardiectomy (95.5% vs. 85.4%, P = 0.06). The degree of reduction of filling pressure and the prevalence of low-output syndrome were significantly different between the groups (P < 0.001). Mean duration of hospitalization was 6 ± 4 and 7 ± 3 days in Groups I and II, respectively (P = 0.12).

Echocardiographically, diastolic filling characteristics remained abnormal in 38 (31.1%) patients of the study group in the immediate postoperative period including six patients expired after surgery. At closing interval, 12 (10.3%) survivors continued to have abnormal diastolic filling pattern of Doppler echocardiogram. Postoperatively, digoxin, diuretics, and ACE-inhibitors were weaned at varying time intervals. There were no late deaths.

Survivors (n = 116) underwent clinical examination, electrocardiogram, and echocardiogram every 3 months. Follow-up was 100% complete (range, 1–134 months; median 67.5 months) and yielded 687.3 patient-years of data with a mean follow-up time of 67.6 (± standard error 37.4) months. The actuarial survival of the entire study group of patients at a mean follow-up time of 67.6 months was 94% ± 0.02% (95% CI: 88.3 ± 97.2%). At their last follow-up, 111 (95.7%) patients were in NYHA Class I and 5 (4.3%) were in NYHA Class II. The time taken for normalization to Class I/II in Groups I and II was 30 ± 11 and 36 ± 14 days, respectively (P = 0.009). Fourteen (34.1%) of 41 patients who had preoperative atrial fibrillation continued to remain in atrial fibrillation. Surgical techniques did not affect the outcome of atrial fibrillation (P = 0.77). Reoperation was not required for any patient.

In this series, radical pericardiectomy was associated with a further reduction of operative mortality as compared to total pericardiectomy of our previous publication (2.9% vs. 7.6%) and patients undergoing total pericardiectomy of the present study (2.9% vs. 7.2%).[23] The results of the present study compared favorably with the hospital mortality rates of 6% to 19% of several long series published after 1985.[6],[7],[8],[12],[13],[23],[29]

The radical pericardiectomy was also associated with less postoperative low cardiac output state as compared to patients undergoing total pericardiectomy (P < 0.001). Although there was marked reduction of filling pressure in the postoperative period in both groups of patients, the radical pericardiectomy group demonstrated greater degree of postoperative reduction of right atrial filling pressure as compared to total pericardiectomy group. There was no difference in mean duration of hospitalization; however, the radical pericardiectomy group achieved NYHA-I and II status quicker than total pericardiectomy group (P = 0.009). Normalization of cardiac hemodynamics in patients undergoing radical pericardiectomy may be the possible reason for shorter interval to attain NYHA-I and II status.

Study limitations

Since thoracotomy was the preferred option in patients with purulent pericarditis and median sternotomy was the preferred option in the setting of calcific pericarditis, calcific pericardial cocoon, and pericardial masses; inclusion of all patients for study comparison may be an important bias of the study.

Studies are underway to compare the clinical and hemodynamic outcome of patients undergoing radical pericardiectomy via modified left anterolateral thoracotomy and total pericardiectomy via median sternotomy on a larger number of patients with different etiologies.


  Conclusions Top


We conclude that using several technical modifications of pericardial excision as enumerated above, it is possible to achieve radical pericardiectomy via modified left anterolateral thoracotomy, particularly removing the constricting pericardium over the anterolateral, diaphragmatic surfaces of left ventricle and the anterior and diaphragmatic surfaces of the right ventricle until the right atrioventricular groove.

Although the surgical approach for pericardiectomy is based on surgeon preference, left anterolateral thoracotomy is the preferred and noncontroversial approach in the setting of purulent pericarditis and effusive constrictive pericarditis to prevent sternal infection. We would recommend median sternotomy approach with or without cardiopulmonary bypass for total pericardiectomy in the setting of calcific pericardial patches, pericardial masses, reoperations, and calcific pericardial “cocoon” and for those with predominant right-sided and annular involvement.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
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