In the present study, we found that the pericardial incision can immediately induce the obvious change of LV morphology and contractile pattern. LV morphology changed from an ellipsoid to a sphere, and the relative wall thickness increased immediately after pericardial incision. Additionally, LV deformation parameters markedly changed with a reduced LV global longitudinal and circumferential strain and twist, and an increased global radial strain; however, LV volumes and ejection fraction remained unchanged.
The pericardium maintains the anatomic position of the heart and limits its displacement through ligaments; besides, the relatively inelastic parietal pericardium retracts when it is cut, indicating that it exerts pressure on the underlying myocardial chambers [12-14]. Therefore, pericardial incision may alter the geometry or function of heart during cardiac surgery. Currently, in addition to the patients with CABG, the pericardium is also not sutured after the surgery in the patients with pericardiectomy and inadequate pericardial tissue for suturing, such as adopting autologous pericardial patches in aortic dissection, possible cardiac enlargement due to myocardial edema in complex congenital heart disease or severe valvular heart disease, and so on. Several previous studies have reported a change of RV geometry or reduction of RV systolic function after pericardial incision without suture [7, 15-17], which was similar with our study. Interestingly, the study by Zanobini M, et al. [18] also reported the presence of decreased RV systolic function after pericardial incision even with reclosing the pericardium with a continuous suture in different surgical approach and cardioplegia type. The possible mechanisms of decreased RV function after cardiac surgery may be related to the cardiopulmonary bypass use, pericardial adhesions, modality of cardioplegia delivery and pericardial incision, and so on [18], and its clear-cut mechanisms were warranted to be further addressed in the future study.
To date, the existing researches has mainly focused on the influences of pericardial incision on RV. However, only a few studies have researched the effect of the pericardium on LV morphology and systolic function. Tanaka et al. [19] reported that congenital pericardial defects caused depressed apical and basal rotation, and consequently, LV twist was reduced. A canine experiment also showed that twist was reduced after pericardial opening and restored after suturing the pericardium, which suggests the importance of the pericardium in sustaining LV twist [20]. It is still unclear whether pericardial incision could affect LV morphology and systolic function during CABG.
Our study revealed the change of LV morphology from an ellipsoid to sphere after pericardial incision in the patients with CABG, as well as the reduced LV global longitudinal and circumferential strain, reduced twist and increased global radial strain. In the normal heart, pericardial incision may lead to the change of LV preload, filling pressure, and blood pressure [21]. However, these responses may not be so evident in the heart with severe myocardial damage caused by the stenosis or occlusion of coronary artery. Although our results showed the subtle changes between before and after pericardial incision in CVP, SBP, DBP, MAP, and HR with invasive methods, as well as LV filling pressure by noninvasive echocardiography in the patients with CABG, there were no significant differences for all of them. Therefore, we infered that the mechanisms underlying the change of LV morphology from an ellipsoid to a sphere and LV contractile pattern might be mainly attributed to the physical release of pericardial constraint. Maybe, the change of pressure was another pathophysiological mechanism; however, these speculations should be further verified in the future study.
The LV myocardium is made up by the three-dimensional arrangement of the myocardial cells, which are supported loosely within a continuous matrix of fibrous tissue. Groups of myocytes are surrounded by condensations of the endomysial weave, thus forming the perimysium, which aggregates a meshwork of myocytes into the so-called myofibers [22, 23]. For describing the global arrangement, most studies have depicted LV myocardium as a transmural continuum which changes continuously from a right-handed helical subendocardium to a left-handed helical subepicardium with the mid-myocardium has a circumferential orientation [24, 25]. The unique structure of myofibers results in complicated myocardial motion during systole, and speckle tracking-derived strain could be used to evaluate ventricular systolic function by detecting myocardial deformation in longitudinal, circumferential, radial direction and wringing from base to apex [26].
Deformation parameters change in different directions during the progression of myocardial disease, however, its instantaneous change in this investigation could not be attributed to this. The paradoxical phenomenon in our study that decreased longitudinal and circumferential shortening with preserved ejection fraction is commonly seen in patients with hypertension [27-29]. As the afterload increased, longitudinal and circumferential shortening decreased while the wall thickened as a compensation allowing a preserved ejection fraction. However, there was no significant hemodynamic change immediately after pericardial incision in our study, hence we speculated that the change in myocardial contractile pattern may mainly result from the physical release of pericardial constraint.
Left ventricular ejection fraction is determined by both myocardial strain and wall thickness, which can increase with the increased strain and wall thickness, and even if the strain decreases, it could keep constant because of increased wall thickness [30-32]. Wall thickness is determined by end-diastolic wall thickness and radial thickening (ie radial strain), it has a substantial influence on ejection fraction: a 1 centimeter increase in thickness increased ejection fraction by approximately 13 percentage points [31, 32]. Sheet dynamic and sheet geometry between adjacent myocytes and matrix coupling are crucial for LV wall thickening and dynamics, regional ventricular wall thickening also reflects changes in cardiac fiber and sheet structure during contraction [33, 34].
We could not provide a definite mechanism for the change in contraction pattern in our study, we speculated that the variations in sheet dynamic and geometry caused by the changes in the arrangement of myocytes due to lack of pericardial constraints may play a potential role. Although we did not find significant correlation between wall thickness and ejection fraction, we found the decreased circumferential strain was corelated with the increased radial strain. Therefore, we speculated that the increased radial strain may offset the reduction in longitudinal and circumferential shortening and twisting, allowing for an unchanged ejection fraction.
LV global longitudinal strain as a valuable parameter of LV systolic function has been used in clinical application with a better reproducibility, and it could be a predictor of prognosis and therapeutic effect in patients after CABG [1-4, 35, 36]. It is recommended to detect LV dysfunction early in chemotherapy patients with a percentage reduction of >15% from baseline [11]. In this study, a significant reduction of global longitudinal strain was found in 17 patients immediately after pericardial incision, and it could be independently predicted by the SYNTAX score. The SYNTAX score of these 17 patients was significantly lower than that of the other 10 patients, probably because patients with a lower SYNTAX score may have few coronary lesions and more surviving myocardia with better movement; therefore, they may be more susceptible to pericardial incision than patients with a higher SYNTAX score.
Transesophageal 2D STE was used to evaluate LV systolic function during CABG in our study, which showed a high degree of intra-observer and inter-observer agreement. Intraoperative TEE is one of the cornerstones for evaluating immediate changes in myocardial function and helps provide critical information during cardiac surgery. Myocardial strain imaging derived from speckle tracking using TEE is a feasible, reproducible method for assessing LV deformation, which has good agreement with transthoracic strain imaging [37-40].
Study limitations
This study has several limitations. First, the correlation between the lower SYNTAX score and the reduction of GLS >15% was analyzed based on the limited sample size in the present study. Therefore, a further study with adequate samples from multicenter should be designed to verify these findings. Second, the invasive LV filling pressure and pulmonary capillary wedge pressure were unable to be obtained during the off-pump beating heart CABG, which may provide the pathophysiological basis for LV modification. However, we provided the LV diastolic indices by noninvasive echocardiography, such as mitral E, mitral A, E/A, septal e’, lateral e’ and average E/e’, and tricuspid regurgitation velocity, which can indirectly reflect the LV filling pressure. Third, LV morphology and systolic function were investigated only immediately after pericardial incision, and a long-term follow-up was not performed to assess whether any aspect of recovery of contractile patterns would occur because we could not eliminate the interference of myocardial revascularization after CABG. However, the depressed RV systolic function after pericardial incision did not recover within 1 month after CABG in patients without interference of the right coronary artery, [7] suggesting that the effect of pericardial incision on RV systolic function may have persisted. Gozdzik A et al. in their study, observed that global longitudinal strain was still reduced two years after CABG [41]. Thus, we speculate that the altered LV morphology and contractile pattern may also persist after CABG, and a well-designed animal experiment should be performed in the future.