© 2000 by European Society of Cardiology
Copyright © 2000, European Society of Cardiology
Neurally mediated depressor hemodynamic response induced by intracoronary catheter balloon inflation in pigs
Servicio de Cardiologìa, Hospital General Universitari Vall d’Hebron, 08035 Barcelona, Spain
* Corresponding author. Tel.: +34-93-489-4031; fax: +34-93-274-6063 jcinca{at}hg.vhebron.es
Received 1 November 1999; accepted 28 December 1999
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Abstract |
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 Top Abstract 1 Introduction2 Methods3 Results4 DiscussionReferences |
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Objectives: To assess whether intracoronary catheter balloon inflation triggers a neurally mediated hemodynamic response that interacts with the ischemia-induced myocardial dysfunction. Methods: Forty-eight chloralose anesthetized pigs underwent a 60 s intraluminal catheter balloon inflation of the proximal left anterior descending (LAD) coronary artery before and after one of these treatments: disruption of LAD pericoronary nerves with phenol (n=6), bilateral stellectomy (n=8), bilateral cervical vagotomy (n=6), atropine (n=5), and ganglionic blockade with hexamethonium (n=10). In 13 other pigs, we assessed the reproducibility of two balloon inflations spaced 15 min (n=6) or 60 min (n=7). The ECG, left ventricular (LV) pressure, and LV dP/dt were recorded during each intervention. Right ventricular (RV) pressure, RV dP/dt, and aortic blood flow were also measured in a subset of pigs. Results: Balloon inflation induced an early (10 s) and reproducible (ANOVA, P<0.001) drop in systolic pressure and peak dP/dt; a decrease in aortic blood flow; a rise in end-diastolic pressure; and elevation of the ST segment. Pericoronary denervation, stellectomy and ganglionic blockade attenuated (P<0.001) the drop in LV parameters during coronary inflation, but atropine and vagotomy did not. Conclusions: A depressor hemodynamic response subserved by pericoronary nerves worsens the LV dysfunction induced by brief coronary catheter balloon inflation in anesthetized pigs. Cholinergic fibers do not appear to play a major role.
KEYWORDS Angioplasty; Autonomic nervous system; Hemodynamics; Ischemia
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1 Introduction |
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TopAbstract1 Introduction2 Methods3 Results4 DiscussionReferences |
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Myocardial ischemia secondary to acute interruption of coronary blood flow is mainly responsible for the depression of systolic and diastolic ventricular function in patients undergoing percutaneous transluminal coronary angioplasty. As promptly as 15–20 s after balloon inflation, LV diastolic function is markedly depressed [1,2], the LV end-diastolic volume increases [1], and abnormalities in LV wall thickness and motion become evident [1,3]. Shortly thereafter, the LV systolic function deteriorates giving rise to a reduction of the ejection fraction and to an increase of end-diastolic volume [1,2,4]. Reperfusion after 40–60 s of coronary balloon inflation is accompanied by an immediate and complete recovery of myocardial function, even when several occlusions are performed in the same individual [1].
Although interruption of myocardial perfusion is a major determinant of the LV dysfunction elicited by intracoronary catheter balloon inflation, other hemodynamic effects linked, for example, to stimulation of coronary receptors as the coronary balloon is distended or to stimulation of myocardial receptors by the acute ischemic process need to be considered. Indeed, excitation of coronary mechanoreceptors by increases in coronary perfusion pressure are known to induce a rapid neurally mediated depressor hemodynamic response in cats [5] and dogs [6]. On the other hand, it has been recognized that myocardial mechano- and chemoreceptors excited by the derangements generated in the ischemic myocardium may trigger additional reflex responses [7–10].
It is therefore possible that during coronary catheter balloon angioplasty, an hemodynamic response subserved by pericoronary nerve fibers interacts with the hemodynamic alterations induced by interruption of coronary blood flow. To test this hypothesis we compared the LV derived hemodynamic parameters before and after experimental procedures that alter the cardiac autonomic nervous activity in a model of intraluminal coronary catheter balloon inflation in anesthetized pigs.
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2 Methods |
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TopAbstract1 Introduction2 Methods3 Results4 DiscussionReferences |
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2.1 Experimental preparation
Forty-eight pigs of either sex weighing 30–40 kg underwent general anesthesia with sodium metomidate (4 mg/kg IV) followed by alpha-chloralose (100 mg/kg IV). Respiration was artificially maintained with a pressure respirator Transpac (Pneupac, UK). Conventional ECG was recorded with a six channel recorder 710 Mingograf. The LV pressure was measured with a precalibrated pressure transducer Millar SPC-300 (Millar Instruments, USA) and the LV dP/dt was derived from the LV pressure signal with a derivative filter Nihon Khoden ED-601G (Nihon Kohden Corporation, Tokyo, Japan). To better delineate the hemodynamic changes elicited by coronary balloon inflation we also recorded the right ventricular (RV) pressure with a 7F Swan-Ganz catheter in a subset of 13 pigs and the aortic blood flow at the aortic root with a transonic flowmeter system (Transonic Systems Inc, USA, mod T206; Transonic flowprobe 16A199 for vessels with diameters between 12 to 16 mm) in 5 pigs. Analogic signals were recorded in a thermal array Nihon Khoden RTA 1200 polygraph and were digitized at 1 kHz and stored in a hard disk using a software developed in our laboratory. Arterial blood gases were measured at regular intervals and were kept within normal limits by adjustment of the respirator characteristics. Intravenous 0.9% NaCl solution was administered to compensate blood volume losses (less than 100 ml). This investigation conforms with the Guide for the Care and Use of Laboratory Animals published by the US National Institutes of Health (NIH Publication No. 85-23, revised 1996). This study was approved by the Ethics Committee of our institution.
2.2 Coronary catheter balloon inflation
After intraarterial administration of 10,000 IU of sodium heparin, a 7F Amplatz right -1 (Cook Cardiology, USA) guiding catheter was introduced into the right femoral artery and was advanced near to the ostium of the left coronary under fluoroscopic control (Arco Si, serial 02, ATS Pedrengo, Italy). A 0.014'' wire guide was then introduced into the LAD and its position was verified by selective coronary angiography using Hexabrix-320 contrast medium. A 3.5F shaft angioplasty catheter with a balloon of 3.5 mm diameter, 20 mm length (Schneider Europe) was advanced through the wire guide until the deflated balloon entered into the proximal LAD. Two separate coronary balloon inflations of 60 s duration at 10 atm were performed in each animal.
2.3 Autonomic neural interventions
2.3.1 Pericoronary nerve disruption
The proximal segment of the LAD was approached through a midsternotomy and was dissected for about a length of 20 mm. The pericoronary nerves along this arterial segment were disrupted by topical adventitial application of a 5-mm2 piece of gauze soaked in an aqueous solution of phenol (88% carbolic acid). We have previously shown [11] that this procedure disrupts the pericoronary nerves leading to sympathetic and parasympathetic denervation of the myocardium supplied by the phenol treated coronary artery in pigs. Others have demonstrated that afferent sympathetic nerve fibers are also interrupted by direct application of phenol in dogs [12].
2.3.2 Bilateral stellectomy
Using the midsternotomy approach, the left and right stellate ganglia were dissected and were isolated with a thin silk thread. Previously to sectioning, both ganglia were identified by direct electrical stimulation (square pulses of 14 V amplitude, 1 ms duration, 10 Hz). During 60 s of neural stimulation increases in heart rate and/or in LV systolic pressure and peak LV dP/dt should be observed. In this model, the hemodynamic response to right stellate stimulation was greater than that evoked by left ganglion stimulation. Histological verification was also performed.
2.3.3 Bilateral vagotomy
The two vagal trunks were dissected for about 20 mm through two cervical incisions at the borders of the thrachea. Prior to sectioning they were identified by electrical stimulation. Square pulses of 14 V amplitude, 1 ms duration, and 10 Hz frequency induced slowing of heart rate and AV conduction disturbances. Thoracotomy was not performed in this group of pigs.
2.3.4 Autonomic neural receptor blockade
Muscarinic receptors were blocked by intravenous administration of atropine sulphate (0.08 mg/kg) whereas ganglionic neural transmission was blocked by intravenous injection of hexamethonium bromide (Sigma Chemical, USA, 10 mg/kg). Only one drug was used in each animal and was administered 10 min after recovery from the first balloon inflation. The thorax was not opened in these cases. The dose of atropine chosen here is enough to induce complete block of the effects of methacholine on porcine coronary arteries [11]. The dose of hexamethonium was similar to that previously used to block nicotinic receptors in dogs [13] and in pigs [14].
2.4 Protocol and study population
All pigs were submitted to two separate coronary catheter balloon inflations of 60 s duration. Heart rate, ST segment potential in lead V1, LV systolic pressure (LVSP), RV systolic pressure (RVSP), LV end-diastolic pressure (LVEDP), RV end-diastolic pressure (RVEDP), peak of LV and RV (+) and (–) dP/dt, and aortic blood flow were recorded continuously from 2 min before to 10 min after each coronary balloon inflation. Measurements were performed automatically every 5 s during the first 2 min of balloon inflation and every 10 s thereafter using a customized software.
The 48 pigs entering this study were allocated into the following series:
Group I (n=13): These open chest pigs underwent two coronary balloon inflations spaced 15 min (n=6) or 60 min (n=7) apart to assess the reproducibility of the hemodynamic response. These time intervals mimic the time elapsed between the two balloon inflations in the different experimental series in this study.
Group II (n=6): In this group, we assessed whether chemical disruption of pericoronary nerves along the balloon treated LAD influenced the hemodynamic changes induced by coronary balloon inflation. The test inflation was carried out 60 min after pericoronary phenol application.
Group III (n=8): In this series, we analyzed the effects of bilateral stellectomy on the hemodynamic response to coronary balloon inflation. The test coronary inflation was performed 5 min after stellectomy.
Group IV (n=6): These pigs were used to assess the effects of bilateral cervical vagotomy on the hemodynamic response to coronary balloon inflation performed 5 min after vagal transsection.
Group V (n=5): In this group, we evaluated the effects of muscarinic receptor blockade with atropine on the LV hemodynamic changes induced by a test coronary balloon inflation performed 5 min after drug administration.
Group VI (n=10): This series was submitted to ganglionic blockade with hexamethonium in order to analyze the effects of this treatment on the LV hemodynamic changes induced by a coronary balloon inflation performed 5 min after drug administration.
2.5 Data analysis
Data were expressed as the mean ± standard deviation. Differences in the magnitude and time course of the changes in the ECG and hemodynamic variables elicited by coronary balloon inflation before and after each treatment were assessed by the ANOVA test for repeated measures. For this analysis we entered the values obtained at baseline and after 15, 30, 45, and 60 s of balloon inflation. Changes in baseline RR interval, hemodynamic variables, and double product (LVSP(mmHg)xheart rate (beats/min)) induced by each treatment were statistically evaluated by the Student's t test for paired samples. A P value <0.05 was considered significant.
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3 Results |
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3.1 Effects of coronary balloon inflation
Fig. 1 illustrates the hemodynamic and electrocardiographic changes induced by a single 60-s catheter balloon occlusion of the LAD in 27 open chest pigs (Groups I to III) and in 21 closed chest animals (Groups IV to VI). Coronary balloon inflation induced in both series of pigs a significant (ANOVA, P<0.01) and prompt (10–15 s) decline in both LVSP and LV dP/dt accompanied by a rise in LVEDP and by upright ST segment deviation. At baseline conditions, pigs undergoing thoracotomy had lower LVSP and lower peak LV dP/dt than closed chest animals (Table 1). However, during coronary balloon inflation these two groups of pigs attained a comparable peak decay in LVSP and LV dP/dt, although slight differences in the time course of the changes in LV dP/dt and LVEDP were seen (Fig. 1). Thoracotomy modifies the spatial relationship between the heart and the exploring electrode and this may account for the lower magnitude of ST segment changes seen in lead V1 in pigs of open chest group. In a subset of 13 open chest pigs submitted to additional measurement of RV pressure and aortic blood flow we observed that LAD coronary balloon inflation also causes a parallel drop (P<0.01) in both RVSP and RV dP/dt and a rise in RVEDP (Figs. 2 and 3
). Aortic blood flow decreases progressively during coronary inflation (mean value: from 3.7±1.2 l/min to 3.0±1.8 l/min, n=5, P<0.001). Deflation of the catheter balloon after 60 s of coronary occlusion gave rise to a complete recovery of the hemodynamic and ST segment alterations (Figs 1–3). Two coronary balloon occlusions spaced 15 or 60 min apart elicited a comparable hemodynamic response (Fig. 4A). There was no correlation between the magnitude of the changes induced by balloon inflation and the preceding values of systolic pressure, dP/dt, and double product (r2<0.4).
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3.2 Pericoronary neural disruption
Adventitial application of phenol at the proximal segment of the LAD was followed by a slight decrease in peak LV (+) dP/dt but this treatment did not cause appreciable changes in LVSP, heart rate nor in double product (Table 2). Disruption of pericoronary nerves with phenol significantly attenuated the drop in LVSP and LV (+) dP/dt elicited by coronary balloon inflation (Fig. 4B). This treatment also tended to attenuate the rise in LVEDP after balloon inflation, although this effect was not statistically significant. Pericoronary denervation did not affect those changes in peak LV (–) dP/dt and ST segment induced by coronary balloon inflation.
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3.3 Surgical neural transsection
Transsection of both stellate ganglia tended to decrease baseline heart rate, LVSP and LV dP/dt (Table 2), leading to a 26% reduction of double product. Bilateral stellectomy significantly attenuated the alterations in peak LV (+) dP/dt induced by coronary balloon inflation (Fig. 5). However, changes in LVSP, peak of LV (–) dP/dt, and ST segment were not significantly altered by stellectomy.
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Bilateral cervical vagotomy was followed by a significant acceleration of sinus node rate and by a tendency towards a rise in LVSP and LV dP/dt leading to a non significant 20% increase of the double product (Table 2). The LV hemodynamic changes induced by coronary balloon inflation were not significantly modified by bilateral vagotomy.
3.4 Autonomic receptor blockade
Atropine tended to increase the baseline heart rate although the double product did not change significantly. This drug did not affect the time course of the alterations in LV parameters and ST segment elicited by balloon inflation.
Administration of hexamethonium slightly decreased baseline sinus node rate and LVSP thus leading to a 39% reduction of double product. The drug also depressed peak LV (+) and (–) dP/dt (Table 2). Hexamethonium attenuated significantly the changes in LVSP, LVEDP, and peak LV (+) dP/dt induced during the first 30–40 s of coronary balloon inflation (Fig. 6). ST segment changes were also attenuated significantly (P<0.01) by the drug.
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4 Discussion |
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TopAbstract1 Introduction2 Methods3 Results4 DiscussionReferences |
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4.1 Neural response to coronary catheter balloon inflation
Intracoronary catheter balloon inflation may trigger two distinct neural responses: one resulting from stimulation of coronary mechanoreceptors as the catheter balloon is inflated, and the other, arising from myocardial mechano- and chemoreceptors excited by ischemia secondary to interruption of coronary blood flow. Whereas a large number of studies have evidenced the ability of coronary occlusion to trigger cardiac reflexes (i.e.: efferent sympathetic inhibition [5,9,10,15,16] or efferent sympathetic hyperactivity [7,17]), studies analyzing the potential of catheter balloon inflation to evoke neurally mediated hemodynamic responses are lacking. Indirect indication that coronary balloon inflation may elicit a neural hemodynamic response is given by studies in anesthetized cats [18] showing that stimulation of coronary mechanoreceptors by brief increases in coronary perfusion pressure induced a reflex decrease of both blood pressure and sympathetic activity in cardiac and renal nerves.
This study reveals that intracoronary catheter balloon inflation elicits a neurally mediated hemodynamic depressor response which acts in concert with the LV dysfunction caused by interruption of coronary blood flow. The existence of a neural component in this model is denoted by the fact that either disruption of LAD pericoronary nerves with phenol, bilateral stellectomy, or ganglionic blockade with hexamethonium attenuated the LV hemodynamic alterations induced by the ensuing coronary balloon inflation. Among these interventions, pericoronary denervation exerted a prominent protective effect thus indicating that a fundamental limb of the neural action induced by coronary balloon inflation is subserved by nerve fibers in or near the dilated coronary artery. Moreover, attenuation of catheter balloon-induced LV dysfunction by systemic administration of hexamethonium suggests involvement of efferent postganglionic nicotinic receptors. Vagal fibers do not play a relevant role since neither vagotomy nor atropine influenced the course of the hemodynamic alterations induced by inflation of the catheter balloon. Bilateral stellectomy attenuated the drop in LV (+) dP/dt during balloon inflation suggesting that efferent sympathetic nerve fibers may participate in this hemodynamic response. Afferent cardiac fibers can also be affected by stellectomy since it has been reported that intrathoracic cardiac afferent neurons with sensory neurites in the heart may interact with efferent postganglionic neurons in the extrinsic cardiac ganglia forming intrathoracic feedback loops [19]. The reason by which stellectomy exerts a less marked attenuation of LV parameters than pericoronary denervation may lie on two circumstances: (a) the fact that stellate ganglia do not subserve the entire sympathetic input to the heart but other mediastinal ganglia and intrinsic cardiac ganglia contribute as well [20], and (b) that a major component of the neural action described here may be processed in the intrinsic cardiac plexus. The nature of the neurally mediated changes induced by balloon inflation, namely the decrease in LVSP and LV dP/dt, suggests that the underlying mechanism is a withdrawal of cardiac sympathetic nerve drive because a vagally-induced negative inotropism was ruled out by the lack of significant effects of vagotomy and atropine. Previous studies have shown that withdrawal of sympathetic activity may involve coronary mechanoreceptors subserved by afferent vagal fibers [6,18], although sympathetic afferents can be implicated as well [21–23]. Reflex inhibition of efferent sympathetic tone caused by augmentation of carotid sinus pressure begins within 2 s [6], whereas sympathetic inhibition induced by coronary occlusion develops 20–30 s later [10]. Thus one may speculate whether the early neural hemodynamic effect induced during coronary balloon inflation in this study is triggered by stimulation of coronary receptors whereas the later alterations arise from ischemia-induced stimulation of myocardial receptors. This study emphasizes the potential role of pericoronary nerves in cardiac pathophysiology and, in this regard, conveys with other studies that have shown, for example, that block of the pericoronary nerve with lidocaine abolishes the reflex withdrawal of the renal sympathetic activity during coronary occlusion in dogs [10] or, that electrical pericoronary nerve stimulation elicits hemodynamic responses in anesthetized cats [24].
Hexamethonium and stellectomy decreased the baseline double product thus one could speculate whether a reduction in myocardial demands by these interventions would favor a better hemodynamic tolerance to balloon inflation without the concurrence of any neurally mediated protective effect. However, in favor of a neural action we have seen that the hemodynamic response to coronary balloon inflation does not correlate with the magnitude of the baseline hemodynamic parameters and, in addition, pericoronary nerve disruption elicits the most pronounced hemodynamic protection despite that this intervention has no major hemodynamic effects.
4.2 Hemodynamic effects of coronary catheter balloon inflation
Changes in LV hemodynamic parameters induced by coronary catheter balloon inflation in this study are comparable to those reported in patients undergoing coronary angioplasty [1]. Moreover, transient catheter occlusion of the LAD induced dysfunction of both ventricles in man [25–27] and in this model in the pig. Dysfunction of the RV is characterized by a reduction in the ejection fraction [25] and by an alteration of the diastolic function [26]. The mechanism of RV dysfunction during balloon dilation of the LAD is not well known but abrupt increases in pulmonary pressures, ischemia of the interventricular septum, or LV dilation leading to pericardial constraint have been alluded. This study confirms that balloon inflation of the LAD increases the filling pressure in both ventricles but, in addition, demonstrates that integrity of the pericardium is not a requisite for the occurrence of RV dysfunction as this alteration is also present in pigs undergoing midsternotomy and pericardial incision.
4.3 Clinical implications
Similarities in pericoronary innervation and in LV dysfunction induced by intracoronary catheter balloon inflation between humans [1] and pigs suggest that present data may have a clinical counterpart. It is conceivable that pericoronary nerves contribute, in addition to ischemia, to the hemodynamic dysfunction seen in patients submitted to angioplasty of the LAD coronary artery. This study suggests that sympathetic, but not vagal nerve fibers, may subserve the hemodynamic depressor response thus, pretreatment with atropine is not expected to exert a protective effect. By contrast, patients undergoing angioplasty under an abnormal sympathetic neural balance, like those treated with beta adrenoreceptor blockers or those suffering acute myocardial ischemia, may depict an unpredictable interaction between the neurally mediated hemodynamic depressor response and the ischemia-induced ventricular dysfunction. Patients with a previous myocardial infarction may also show a different neural response during coronary angioplasty because of the presence of postinfarction autonomic neural dysfunction. Periinfarction denervation has been seen in humans [28] and in various animal species [29] and in the presence of acute ischemia may favor electrophysiologic unstability [30]. Moreover, the neural response to coronary angioplasty may be altered in patients with primary disturbances of the autonomic nervous system. Finally, the magnitude of this neural depressor effect in this model could have been attenuated by anesthesia thus, in the clinical setting a greater neural response might be expected.
Time for primary reviews 24 days.
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Acknowledgements |
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We thank Dr. David Garcìa-Dorado for constructive review of the manuscript. This work was supported by grants from Comisión Interministerial de Ciencia y Tecnologìa (SAF96-1513), Marató TV3, and from our institution (PR-HG 96/1746).
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