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Right arrow Electrophysiology - arrhythmias

Ann Thorac Surg 2007;83:532-537
© 2007 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Do Cardiac Neuropeptides Play a Role in the Occurrence of Atrial Fibrillation After Coronary Bypass Surgery?

Niyazi Guler, MDa,*, Cenap Ozkara, MDb, Haluk Dulger, MDa, Veysel Kutay, MDa, Musa Sahin, MDa, Enver Erbilen, MDb, Hasan Ali Gumrukcuoglu, MDa

a Departments of Cardiology, Cardiovascular Surgery, and Biochemistry, Yuzuncu Yil University, Van
b Department of Cardiovascular Surgery, Corlu Sifa Hospital, Tekirdag, Turkey

Accepted for publication August 22, 2006.

* Address correspondence to Dr Guler, Yuzuncu Yil University, Arastirma Hastanesi, Van/Turkey (Email: niyaziguler{at}hotmail.com).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: One of the potential mechanisms to explain the occurrence of postoperative atrial fibrillation (AF) is imbalance of autonomic nervous system tone. The myocardium is innervated not only by cholinergic and adrenergic nerves but also by peptidergic nerves that synthesize and secrete neuropeptides. To investigate the possible role of cardiac neuropeptides in the development of AF after coronary artery bypass grafting (CABG), we analyzed the plasma levels of substance P (SubP), neuropeptide Y (NPY), and angiotensin II (Ang II) in patients who underwent elective on-pump CABG.

METHODS: This prospective study group included 83 consecutive patients scheduled for elective, on-pump CABG. Depressed left ventricular (LV) function (ejection fraction [EF] less than 0.30), concomitant cardiac procedures, history of atrial fibrillation, second or third degree atrioventricular block, implanted pacemaker, postoperative myocardial infarction, use of class I or III antiarrhythmic drug, and hemodynamic deterioration were exclusion criteria. Preoperative and postoperative serum levels of SubP, NPY, and AngII were measured by radioimmunoassay technique.

RESULTS: Postoperative AF occurred in 27 patients (32.5%). Using multivariate logistic regression analyses, only a decrease in SubP level (odds ratio [OR] = 1.87, 95% confidence interval [CI] = 0.767 to 0.99, p = 0.031) and an increase in AngII level (OR = 2.61, 95% CI = 1.002 to 1.021, p = 0.023) after CABG were found to be independently associated with AF. Increased age (p = 0.02), diabetes mellitus (p = 0.023), preoperative use of beta blocker (p = 0.024), proximal right coronary artery involvement (p = 0.024), low preoperative sodium levels (p = 0.023), low LVEF (p = 0.013), and increased mitral E wave deceleration time (p = 0.044) were also associated with AF.

CONCLUSIONS: These results indicate that the increase in AngII and the decrease in SubP after CABG may play a role in the occurrence of postoperative AF. Further studies are needed to define the physiologic and pathologic relevance of these substances at the occurrence of AF in patients who undergo CABG.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
The incidence of atrial fibrillation (AF) in patients undergoing coronary artery bypass graft operation (CABG) varies between 17% and 65%, depending on the definitions and diagnostic methods [1, 2]. The occurrence of postoperative AF has been associated with prolonged hospital stay, intensive care unit readmission, persistent congestive heart failure, increased stroke risk, increased overall costs, and increased mortality [1–5]. Various risk factors for the occurrence of postoperative AF have been identified. History of AF, advanced age, valvular heart disease, heart failure, vascular disease, chronic obstructive pulmonary disease, stroke, MI, electrolyte abnormalities, right coronary artery (RCA) involvement, pulmonary vein venting, bicaval venous cannulation, prolonged cross-clamp time, postoperative atrial pacing, and nonuse of beta-blockers are all preoperative characteristics that have been shown in statistical analyses to increase the risk of postoperative AF [2, 6–10].

The autonomic nervous system (ANS) modulates dispersion of atrial refractory periods and intraatrial conduction, and therefore influences the occurrence of AF. The innervation of the heart is regulated directly by parasympathetic tone through the vagus nerve and indirectly by sympathetic tone. The myocardium is innervated not only by cholinergic and adrenergic nerves but also by peptidergic nerves that synthesize and secrete neuromodulatory peptides, such as substance P (SubP), angiotensin II (AngII), neuropeptide Y (NPY), and atrial natriuretic peptides [11–13]. Neuropeptides can act as neurotransmitters or neuromodulators interfering with the sympathetic and parasympathetic systems to modulate heart rate. Furthermore, it has been demonstrated the injection of various peptides such as AngII, SubP, VIP, and bradykinin adjacent to spontaneously active in situ right atrial neurons resulted in cardiac arrhythmias [14]. Hardwick and colleagues [15] showed that local application of SubP depolarizes parasympathetic postganglionic neurons. The NPY is largely distributed in the sympathetic system and among the other sites the peptide is co-localized with norepinephrine in synaptic terminals of postganglionic neurons innervating the cardiovascular system [13]. Important concentrations of NPY are found in the nodal tissue, the atria, and the coronary vessels [16, 17]. It is co-released with catecholamines into the circulation during intense activation of the sympathoadrenomedullary system. Recently, modulators of atherosclerosis such as AngII have been identified as possibly playing a role in the development of nonsurgical AF [18, 19].

To investigate the possible role of cardiac neuromediators in the occurrence of AF after CABG we measured plasma concentrations of SubP, AngII, and NPY just before and two days after operation. We also investigated the clinical, echocardiographic, and laboratory risk factors for the occurrence of postoperative AF.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patient Selection
The study group included 83 consecutive patients scheduled for elective, nonemergent on-pump CABG. After approval of the local ethics committee and written, informed consent was obtained, the study was performed in a prospective manner. Clinical, echocardiographic and angiographic data were acquired preoperatively. The patient’s usual cardiac medication, including beta blockers and calcium channel blockers, was continued until the morning of surgery and reinstituted on the day after the operation depending on the patient’s clinical status. No patient received cardiac inotropes within 24 hours of the second set of biochemical measurements. Routine postoperative monitoring was initiated for the first three days in the intensive care unit, and continued with clinical and 12-lead electrocardiographic follow-up to detect all episodes of AF. The primary end point of this study was the new onset of sustained (>30 seconds). Atrial fibrillation was defined by the absence of consistent P waves before each QRS complex and with an irregular cardiac rhythm other than sinus within seven days after surgery and detected by 12-lead electrocardiograms.

Depressed left ventricular (LV) function (ejection fraction [EF] less than 0.30), concomitant cardiac procedures such as valve repair or replacement, history of atrial fibrillation or other supraventricular arrhythmias (including paroxysmal supraventricular arrhythmias or atrial flutter), second or third degree atrioventricular block, implanted pacemaker, postoperative myocardial infarction, use of class I or III antiarrhythmic drug, and hemodynamic deterioration requiring postoperative cardiopulmonary support or left ventricular assist device were exclusion criteria. No patient received drugs as prophylactic therapy for AF. However, same dose magnesium was routinely administered to all patients preoperatively.

Echocardiographic Evaluation
Transthoracic echocardiography was performed the day before operation. Patients were imaged in the left lateral decubitus position with a commercially available system (Vingmed Vivid 3, General Electric-Vingmed, Milwaukee, WI). Images were obtained by a 3.5 MHz transducer at a depth of 16 cm in the parasternal and apical views. Left atrial and left ventricle dimensions and LVEF were derived from the parasternal long axis view using M-mode echocardiography. Mitral and aortic flow characteristics were analyzed as assessed using pulsed Doppler echocardiography. Peak velocity during early filling (E), late filling from the atrial contraction (A), the ratio of E/A, the deceleration time from peak early filling extrapolated to the baseline, and isovolumetric relaxation time from the distance between mitral and aortic flow were measured.

Anesthetic Management and Surgical Procedures
The anesthetic and surgical procedures were similar for all patients. The same medical staff performed all operations and anesthetic management throughout the study period. All patients received premedication with oral diazepam and an intramuscular injection of atropine and midazolam before entering the operation room. Anesthesia was induced with intravenous fentanyl, propofol, and a muscle relaxant (pancuronium) and maintained with additional doses of these drugs or with inhaled sevoflurane.

Ascending aortic and right atrial double-staged cannulation with moderate systemic hypothermia (30°C) was implemented for patients in whom cardiopulmonary bypass was used. Cardiac arrest was obtained and maintained by intermittent antegrade hyperkalemic blood cardioplegia. Additional infusion of cardioplegic solution was performed manually into each harvested graft after completion of the corresponding distal anastomosis. The average cardiopulmonary bypass duration was 119 ± 27.9 minutes.

Samples for Measurement of Neuropeptides
A total of 10 mL of venous blood was drawn from each subject the day of operation just after premedication. Postoperative blood samples for neuropeptides were received at the second day of CABG. Blood samples were then centrifuged at 2,000 rpm for 10 minutes in a refrigerated centrifuge to separate serum samples from the cells. Serum samples were stored at –20°C in plastic tubes until the analysis. Serum levels of SubP, NPY, and AngII were measured by radioimmunoassay (RIA) technique (Phoenix Pharmaceuticals, Inc, Belmont, CA) in the Isocomp I gamma counter, according to the manufacturer [20].

Statistical Analysis
All analyses were done between patients in whom AF developed and those in whom it did not. Data were analyzed in the following stepwise manner, and all comparisons, regardless of the statistical significance, are reported to allow assessment of the potential for finding significant association due to chance.

We first ran the stepwise logistic regression analysis for variables selection to construct the best logistic regression model for AF. Before independent variables were entered into the logistic regression model, the –2 log likelihood for the model with only the intercept constant was given. This intercept-only –2 log likelihood is designated (denoted as L0 by Hosmer and Lemeshow) to indicate that none (zero) of the independent variables were included in the equation. Then multivariable logistic regression model was used to estimate parameters. In logistic regression model the following independent variables were included: age, diabetes mellitus, preoperative beta blocker use, proximal RCA involvement, preoperative Na, K, and Mg levels, left ventricular ejection fraction, deceleration time of mitral E velocity, pre- and postoperative Ang II levels, pre- and postoperative SubP levels, and pre- and postoperative NPY levels. In addition, the differences (postoperative minus preoperative values) of neuropeptides were analyzed.

Baseline comparisons between the groups and all other statistical analyses were performed using the Student unpaired t test for continuous data and {chi}2 statistic or Fisher exact tests where appropriate for categorical data. All statistical tests were two sided, and significance was accepted at the 0.05 level. Data are presented as mean standard error.

All analyses were performed using SAS STAT (Version 9.13; SAS, Cary, NC).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Postoperative AF occurred in 27 patients (32.5%). Clinical and echocardiographic characteristics and surgical data of patients who did (n = 27) or did not (n = 56) develop AF are presented in Tables 1 and 2. Go In patients with AF, age was higher, proximal RCA involvement at angiography was more frequent, and plasma Na level was lower. Also, decreased LVEF and increased mitral E velocity deceleration time at the echocardiography were statistically significant in patients with AF.


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  		Table 1. Baseline Clinical, Laboratory, and Angiographic Characteristics
 

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  		Table 2. Preoperative Echocardiographic Parameters
 
Using multivariate logistic regression analyses, only increased age, diabetes mellitus, use of preoperative beta blocker, proximal RCA involvement, low preoperative Na levels, low LVEF, and increased mitral E wave deceleration time were found to be independently associated with AF (Table 3). It was also found that the decrease in the substance P level (odds ratio [OR] = 1.87, 95% confidence interval [CI] = 0.767 to 0.99, p = 0.031) and increase in the AngII level (OR = 2.61, 95% CI = 1.002 to 1.021, p = 0.023), after CABG were statistically significant. Figures 1 and 2 Go demonstrate the changes of SubP and AngII levels by CABG in patients with AF and those without AF; increase of NPY level (OR = 1.134, 95% CI = 0.99 to 1.3, p = 0.07) was not reached to statistical significance.


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  		Table 3. Multivariable Logistic Regression Analysis
 

Figure 1
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  		Fig 1. The changes of substance P levels by coronary artery bypass surgery. (Grey bars = baseline; black bars = postoperative second day; AF = atrial fibrillation.)

 

Figure 2
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  		Fig 2. The changes of angiotensin II levels by coronary artery bypass surgery. (Grey bars = baseline; black bars = postoperative second day; AF = atrial fibrillation.)

 
Operation time, aortic pump duration, and aortic clamp duration were not different between groups. In addition, there was no correlation between aortic fat pat destruction and the occurrence of postoperative AF. Also, the number of bypass grafts, previous myocardial infarction, and previous coronary intervention were not found to have a significant association with postoperative AF. Although, as already mentioned, lower preoperative Na+ level was associated with AF, there was no such association between preoperative magnesium and potassium levels and the development of AF. However, magnesium was administered preoperatively to all patients who underwent CABG in our study.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
These results indicate that the increase of AngII and the decrease of SubP after CABG may play a role in the occurrence of postoperative AF. The mechanism responsible for postoperative AF in patients with the necessary atrial electrical substrate is not entirely clear and is multifactorial. Electrophysiologic effects in the atrium leading to AF can also be caused or triggered by physiologic processes such as adrenergic or vagal stimulation, electrolyte disturbances, or by certain drugs or agents [21, 22]. Alterations of ANS activity can be seen after CABG. An imbalance in ANS may increase the heterogeneity of atrial refractoriness, thus increasing susceptibility to AF [23]. A diminished heart rate variability (HRV) was described after CABG, and mainly attributed to a reduced parasympathetic activity [24]. Dimmer and colleagues [25] reported that a shift in the autonomic balance with a loss of vagal tone and a moderate increase in sympathetic tone are observed before the onset of AF compared with those in controls. Frost and colleagues [26] demonstrated that attenuated preoperative cardiac vagal modulations are independent risk factors for the development of atrial fibrillation or flutter after CABG. Myocardial ischemia involves both local changes in myocyte function and reflex alterations in the cardiac nervous system that regulates the myocardium. These multimodal sensory afferent neurons respond to ischemia-induced changes in the chemical-mechanical milieu of the heart. The SubP is detected in sinoatrial and atrioventricular nodes of most mammals and around blood vessels in the human atria [27, 28]. Our study showed that the decrease of SubP levels, reflecting the parasympathetic activity, was significant in patients developing postoperative AF. Similarly, Paroli and colleagues [29] found that SubP levels were significantly decreased 48 hours after the end of the coronary artery stent implanting. In light of these studies, our results may support that reduced parasympathetic activity may be important in the occurrence of postoperative AF.

The other important finding of our study is that the increase of AngII levels after CABG was statistically significant in patients developing AF. The renin-angiotensin system may play a role in the pathophysiology of AF. An increased activity of the atrial tissue angiotensin-converting enzyme (ACE) concentration was found in patients with AF [30, 31]. Atrial fibrillation is associated with electrical remodeling in the atria and AngII is involved in the process of atrial electrical remodeling [32]. Angiotensin II has been identified as possibly playing a role in the development of AF in nonsurgical patients. Recent meta-analysis showed that use of ACE inhibitors or angiotensin receptor blockers prevent the development of new-onset AF in individuals at risk and prevent recurrence of AF after cardioversion [33]. Furthermore, Wachtell and colleagues [18] showed that new-onset AF was significantly reduced by losartan compared with atenolol-based antihypertensive treatment, despite equivalent blood pressure reduction. That losartan reduced the rate of new-onset AF by 33% compared with atenolol with similar blood reduction is surprising, as many regard beta blockers a first choice therapy to prevent AF and for rate control in established AF. The mechanism by which ACE inhibition exerts its protective effect against occurrence of AF is not completely understood. It has been shown that angiotensin facilitates the release of norepinephrine from atrial sympathetic fibers through activation of prejunctional angiotensin receptors [34]. An increase in sympathetic tone is considered as an important factor in initiating AF [35]. Angiotensin II, by increasing afterload and LV systolic stress, may cause increased chamber diameter and high intracavitary pressures that are associated with dispersion of refractoriness, reduced action potential duration, and induction of early and delayed depolarization. In light of these trials and our study, it might be hypothesized that AngII may play a role in the pathogenesis of the development of AF after CABG.

Although the increase was not reached to statistical significance (p = 0.07), NPY levels were increased in patients developing AF after CABG in our study. Because the localization and release of NPY are closely related to sympathetic nerve activity, its plasma concentrations often parallel the changes of plasma norepinephrine. Authors [27] have shown the presence of a dense sympathetic innervation of the sinoatrial node, most of the neurons being immunoreactive for NPY [27]. It has been reported that NPY, released by sympathetic neuron terminals after intense stimulation, also provokes a long inhibition of vagal tone [13]. These results also may suggest that vagal withdrawal and moderate increase in sympathetic tone may trigger postoperative AF.

In our study, we observed that the occurrence of AF after CABG was more frequent in patients with advanced age. In addition, logistic regression analysis revealed that postoperative AF developed more frequently in patients with proximal RCA involvement, preoperative low plasma sodium level, and diabetes mellitus. Also, AF after CABG was seen more commonly in patients with low LVEF and increased mitral E wave deceleration time. Advanced age, increased deceleration time, and low EF have been found to be risk factors for postoperative AF in previous studies [8–10, 36]. Right coronary stenosis and diabetes mellitus were additional risk factors for AF in some studies [6, 7, 37]. Although it is well known that a preoperative low level of potassium and magnesium is an important risk factor for the occurrence of AF, our study showed a preoperative low sodium level could play a role in the development of postoperative AF [38, 39].

Our study investigated only AF that occurred during the in-hospital period. As a result, we may have underestimated the incidence of AF that may have occurred in the late postoperative and out-of-hospital period. Keeping patients hospitalized for up to one week after operation may allow us to determine late episodes of AF. However, prolonging the hospitalization for those without early postoperative complications would likely be financially prohibitive. Second, our measurements of neuropeptides were static, albeit conducted serially, without varying conditions. However, comparison of the prebypass versus postbypass measurements provided information on the impact to occurrence of postoperative AF. Finally, we did not measure other parasympathetic and sympathetic parameters, such as norepinephrine, which may have provided additional information on changes in ANS tone.

In conclusion, this study shows that SubP levels significantly decrease while AngII levels significantly increase in patients who develop AF after CABG. Although it does not reach statistical significance, NPY levels also increased in patients with AF. The increase in AngII and NPY levels and the decrease in SubP levels after CABG led to the conclusion that postoperative AF may be triggered by a loss of vagal tone and an increase in sympathetic tone. These results may contribute to the understanding of the complex relation between the occurrence of postoperative AF and neuropeptides. Current therapies that can alter neurohormonal activation in the setting of atherosclerosis and surgical trauma, such as blockade of the renin angiotensin system by ACE inhibition or angiotensin receptor blockade or HMG-CoA reductase inhibition, should be evaluated to prevent AF after open heart surgery. Further studies are needed to define the physiologic and pathologic relevance of these substances at the occurrence of AF in patients who undergo CABG.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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A. Sezai, M. Hata, T. Niino, Y. Kasamaki, T. Nakai, A. Hirayama, and K. Minami
Study of the factors related to atrial fibrillation after coronary artery bypass grafting: A search for a marker to predict the occurrence of atrial fibrillation before surgical intervention
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