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Ann Thorac Surg 1999;67:484-488
© 1999 The Society of Thoracic Surgeons

Original Articles

Should the pericardium be closed routinely after heart operations?

Vivek Rao, MD, PhDa, Masashi Komeda, MD, PhDa, Richard D. Weisel, MDa, Gideon Cohen, MDa, Michael A. Borger, MDa, Tirone E. David, MDa

a Division of Cardiovascular Surgery and Centre for Cardiovascular Research, The Toronto Hospital and the University of Toronto, Toronto, Ontario, Canada

Accepted for publication July 12, 1998.

Address reprint requests to Dr Weisel, The Toronto Hospital, EN 14-215, 200 Elizabeth St, Toronto, Ontario, M5G 2C4 Canada


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Repeat coronary artery bypass grafting is more difficult if the right ventricle is firmly attached to the inner table of the sternum. Closure of the pericardium at the time of the initial procedure may prevent attachment of the right ventricle to the sternum. This study attempts to identify the geometric effects of pericardial closure early after isolated coronary artery bypass grafting.

Methods. Forty-two patients undergoing elective, isolated coronary artery bypass grafting were randomized into two groups: 20 patients underwent closure of the pericardium (Closure group) and the pericardium was left open in 22 patients (Open group). Radiopaque markers were attached to the anterior aspect of the right ventricular epicardium in both groups.

Results. Postoperative chest roentgenograms revealed that the distance between the epicardial surface and the posterior table of the sternum was larger in the Closure group compared to the Open group at 1 week and 3 months postoperatively (p < 0.001). Cardiac index and stroke work index in the early postoperative period was lower in the Closure group compared to the Open group (p < 0.001) despite similar filling pressures.

Conclusions. Pericardial closure may reduce the risk of myocardial injury during sternotomy for repeat coronary artery bypass grafting by preventing right ventricular adhesions. However, adverse hemodynamic effects in the early postoperative period may preclude pericardial closure in patients with impaired ventricular function.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
An increasing proportion of patients are presenting for repeat coronary bypass and valvular procedures [1]. Resternotomy may result in myocardial injury if the right ventricle is firmly attached to the posterior table of the sternum [2, 3]. Closure of the pericardium at the time of the initial operation may decrease adhesions and reduce the risks of resternotomy [4–8]. However, pericardial closure may increase the risk of postoperative cardiac tamponade and result in adverse hemodynamic consequences [7, 9–13]. This prospective randomized study attempts to assess the geometric effects of pericardial closure by measuring the retrosternal space after operation.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 Acknowledgments
 References
 
Forty-five patients undergoing elective, isolated coronary artery bypass grafting agreed to participate in this study and signed a consent form approved by the Hospital Ethics Committee. Closure of the pericardium was possible in 42 of these patients who were then randomized to have their pericardium closed (Closure group, n = 20 patients) or left open (Open group, n = 22 patients). Excessive tension was produced when pericardial closure was attempted in 3 patients who were excluded from randomization.

Two radiopaque markers were applied to the epicardial surface of the right ventricle in the midline (Fig 1 ). The midline was estimated by temporary reapproximation of the sternum. In patients randomized to the Closure group, the pericardium was closed in a manner that attempted to reconstruct the original shape of the pericardial sac on both the midline and anterior diaphragmatic surface using interrupted 2-0 Vicryl sutures. Intraoperative and postoperative care was uniform in all patients with serial hemodynamic measurements being performed at 1, 4, and 8 hours after operation.



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  		Fig 1. A radiopaque marker was applied to the epicardial surface (A) in the midline (B).

 
All patients underwent posteroanterior and lateral chest roentgenograms at 1 week and 3 months postoperatively. The radiographic technique was identical in all patients with standard magnification. To estimate the retrosternal space, the distance between the epicardial markers and the posterior table of the sternum was measured (Fig 2 ). The shortest distance between the epicardial markers and the sternum was identified as the retrosternal distance.



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  		Fig 2. Measurement of the distance between the epicardial markers and the posterior table of the sternum (D), the cardiothoracic ratio (a/b), and the thickness ratio (c/b).

 
To account for differences in body habitus, the transverse diameter of the heart in the posteroanterior projection (a) and of the thorax (b) and the thickness of the thorax in the lateral projection (c) was also measured. The cardiothoracic ratio () and the ratio of thoracic thickness () was calculated as illustrated in Figure 2. The thickness ratio may be increased in patients with chronic obstructive pulmonary disease and may affect the postoperative retrosternal distance. All measurements were performed by a single observer who was blinded to the patient group.

Statistical analysis was performed using the SAS program (Statistical Analysis Systems Institute, Cary, NC). Categorical data were analyzed by {chi}-square or Fisher’s exact test where appropriate. Continuous data are expressed as the mean ± standard error of the mean. A two-way analysis of variance was used to simultaneously evaluate the effect of group and time on postoperative retrosternal distances. Similarly, analysis of covariance was used to evaluate the effect of group, time, and preload on postoperative cardiac index and stroke work index. When the F statistic of the analysis of variance was statistically significant (p < 0.05), differences were specified by Duncan’s multiple range test. Correlations were evaluated by calculating Spearman correlation coefficients.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 Acknowledgments
 References
 
The clinical profile of each group is summarized in Table 1. There were no operative deaths and no major complications in either group. Table 2 presents the retrosternal distance measured as the distance between the epicardial markers and the posterior table of the sternum. Patients in the Closure group had a significantly greater retrosternal distance than the Open group (groups different by analysis of variance, p = 0.0001) at both 1 week (p = 0.0003) and 3 months (p = 0.0001) postoperatively. In both groups, the retrosternal distance decreased between 1 week and 3 months postoperatively (times different by analysis of variance, p = 0.0001).


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  		Table 1. Patient Profile

 

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  		Table 2. Retrosternal Space as Measured by the Distance (in mm) Between the Epicardial Markers and the Posterior Table of the Sternum

 

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  		Table 3. Change in the Cardiothoracic Ratio With Time

 
Figure 3 illustrates a representative patient from each group. There was poor correlation between the retrosternal distance and the thickness ratio at 1 week (r = 0.26, p = 0.10) or at 3 months (r = 0.30, p = 0.05). Similarly, there was poor correlation between the retrosternal distance and the cardiothoracic ratio at 1 week (r = -0.23, p = 0.14) or at 3 month (r = -0.16, p = 0.05). The cardiothoracic ratio (Table 3) decreased (times different by analysis of variance, p = 0.0001) between 1 week and 3 months after operation in both the Open group (0.56 ± 0.07 versus 0.51 ± 0.05, p = 0.0008) and the Closure group (0.54 ± 0.03, 0.48 ± 0.04, p = 0.0001). There were no differences in the cardiothoracic ratio between groups.



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  		Fig 3. Representative cases from each group. Note that the closure group (upper) has a longer retrosternal distance than the open group (lower).

 

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  		Table 4. Postoperative Hemodynamic Measurements

 
Table 4 displays the postoperative hemodynamic data in each group. Cardiac index was significantly greater in the Open group despite similar filling pressures (F = 10.42, p = 0.002 by analysis of covariance). Differences were specified at 1 hour after operation (3.1 ± 0.8 versus 2.3 ± 0.6 L · min-1 · m-2, p = 0.003), with no significant difference observed at either 4 or 8 hours after operation. Similarly, left ventricular stroke work index was higher in the Open group (F = 15.92, p < 0.001 by analysis of covariance) with differences specified at 1 and 4 hours after operation. Figure 4 compares postoperative cardiac index and left ventricular stroke work index between groups as a function of the pulmonary capillary wedge pressure.



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  		Fig 4. A comparison of cardiac index (L · min-1 · m-2) and left ventricular stroke work index (LVSWI: g · m · m-2) at 1, 4, and 8 hours after operation. (PCWP = pulmonary capillary wedge pressure.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
Acknowledgments
 References
 
Hippocrates described the pericardium as "a smooth mantle surrounding the heart and containing a small amount of fluid resembling urine." Most studies concerning the pericardium have focused on its ability to minimize adhesions between the heart and the sternum [4–6] or on the adverse hemodynamic consequences of pericardial closure [7–12]. There have been several reports describing both the advantages and disadvantages of pericardial closure after cardiac operations [13–23].

Maintaining the native geometry of the heart is now recognized as an important factor in preserving left ventricular function after cardiac operations. Preservation of the papillary muscles after mitral valve grafting [24], restoring the conical shape of the heart following left ventricular aneurysm resection [25], and direct cava to cava anastomosis during cardiac transplantation [26] are all modifications designed to improve ventricular function postoperatively. The pericardium has been reported to enhance right ventricular function and improve the interaction between ventricles [20, 21]. Janicki and Weber [20] found that the pericardium served to enhance the distensibility of the ventricles and improved ventricular interaction during diastole. In addition, they found that the intact pericardium improved the systolic function of the right ventricle, but had a variable effect on the performance of the left ventricle. Bailey and colleagues [21] reported that the adhesions between the sternum and the anterior surface of the right ventricle significantly impaired right ventricular function. The researchers postulate that the use of bovine pericardium may reduce right ventricular adhesions and thereby improve right ventricular function.

Restoring the continuity of the pericardium has been associated with decreased left ventricular diastolic filling [7, 11, 12] and may predispose patients to cardiac tamponade should they bleed postoperatively. Cunningham and colleagues [13] described perioperative contraction of the pericardium as a potential cause of the reduced ventricular filling. Daughters and colleagues [7] measured cardiac output and stroke work index in patients immediately after operation and found that removal of the pericardial suture immediately improved left ventricular hemodynamics. This finding raises concerns about pericardial closure in patients with marginal preoperative left ventricular function or in those patients with postoperative ventricular dysfunction who require high preloads to maintain cardiac output.

In our series, we attempted to keep the pericardium under considerable tension during the operation. Often the pericardial stay sutures were tacked to the periosteum of the sternum instead of the retractor or drape. Stretching the pericardium during operation may have facilitated pericardial closure after the operation. Stretching may also prevent pericardial contraction, especially when the pericardium is found to be tight at pericardiotomy. We had 3 patients whose pericardium could not be closed due to excessive tension and they were excluded from this study. We did not observe any episodes of tamponade in our small series. The use of postoperative inotropes was not significantly different between groups. However, cardiac index was depressed in the Closure group in the early postoperative period despite no differences in filling pressures.

Several investigators have reported on the use of pericardial substitutes such as polytetrafluoroethylene [14–16] and autologous fascia lata [17]. When autogenous pericardium is used for intracardiac repair, these substitutes may prove useful in reconstructing the pericardial sac. A different approach to protection of the right ventricle can involve modifying the pericardial incision [22] or the addition of antiadhesive agents such as hyaluronic acid [23].

This study describes the early, geometric effects of pericardial closure after coronary artery bypass grafting. The patients involved in this study were low-risk, elective patients with preserved preoperative left ventricular function. We believe that pericardial closure is a safe, simple method to facilitate resternotomy during subsequent reoperative procedures in this low-risk population. However, cardiac surgeons should be aware of the transient deterioration in hemodynamics associated with pericardial closure. Pericardial closure does result in a greater retrosternal distance at both 1 week and 3 months after operation, which may facilitate sternal reentry. As reoperative procedures become increasingly frequent, techniques to reduce the morbidity of resternotomy will become increasingly important.

We believe that this study provides rationale for pericardial closure in young patients with preserved ventricular function who are at increased risk of requiring reoperation. However, the observed depression in left ventricular function provides evidence against routine closure in patients at risk for postoperative tamponade or in patients with preoperative ventricular dysfunction.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
References
 
We gratefully acknowledge Molly K. Mohabeer and Laura C. Tumiati for their contributions to the completion of this manuscript.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 

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  13. Cunningham J.N., Jr, Spencer F.C., Zeff R., Williams C.D., Cukingnan R., Mullin M. Influence of primary closure of the pericardium after open-heart surgery on the frequency of tamponade, postcardiotomy syndrome, and pulmonary complications. J Thorac Cardiovasc Surg 1975;70:119-125.[Abstract]
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  15. Harada Y., Imai Y., Kurosawa H., Hoshino S., Nakano K. Long-term results of the clinical use of an expanded polytetrafluoroethylene surgical membrane as a pericardial substitute. J Thorac Cardiovasc Surg 1988;96:811-815.[Abstract]
  16. Amato J.J., Cotronneo J.V., Galdieri R.J., Alboliras E., Antillon J., Vogel R.L. Experience with the polytetrafluoroethylene surgical membrane for pericardial closure in operations for congenital cardiac defects. J Thorac Cardiovasc Surg 1989;97:929-934.[Abstract]
  17. Kohanna F.H., Adams P.X., Cunningham J.N., Spencer F.C. Use of autologous fascia lata as a pericardial substitute following open-heart surgery. J Thorac Cardiovasc Surg 1977;74:14-19.[Abstract]
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  23. Mitchell J.D., Lee R., Hodakowski G.T., et al. Prevention of postoperative pericardial adhesions with a hyaluronic acid coating solution. Experimental safety and efficacy studies. J Thorac Cardiovasc Surg 1994;107:1481-1488.[Abstract/Free Full Text]
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