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The effect of electrical neurostimulation on collateral perfusion during acute coronary occlusion
© de Vries et al; licensee BioMed Central Ltd. 2007
Received: 12 February 2007
Accepted: 27 June 2007
Published: 27 June 2007
Electrical neurostimulation can be used to treat patients with refractory angina, it reduces angina and ischemia. Previous data have suggested that electrical neurostimulation may alleviate myocardial ischaemia through increased collateral perfusion. We investigated the effect of electrical neurostimulation on functional collateral perfusion, assessed by distal coronary pressure measurement during acute coronary occlusion. We sought to study the effect of electrical neurostimulation on collateral perfusion.
Sixty patients with stable angina and significant coronary artery disease planned for elective percutaneous coronary intervention were split in two groups. In all patients two balloon inflations of 60 seconds were performed, the first for balloon dilatation of the lesion (first episode), the second for stent delivery (second episode). The Pw/Pa ratio (wedge pressure/aortic pressure) was measured during both ischaemic episodes. Group 1 received 5 minutes of active neurostimulation before plus 1 minute during the first episode, group 2 received 5 minutes of active neurostimulation before plus 1 minute during the second episode.
In group 1 the Pw/Pa ratio decreased by 10 ± 22% from 0.20 ± 0.09 to 0.19 ± 0.09 (p = 0.004) when electrical neurostimulation was deactivated. In group 2 the Pw/Pa ratio increased by 9 ± 15% from 0.22 ± 0.09 to 0.24 ± 0.10 (p = 0.001) when electrical neurostimulation was activated.
Electrical neurostimulation induces a significant improvement in the Pw/Pa ratio during acute coronary occlusion.
Cardiovascular disease is a leading cause of mortality and morbidity. Percutaneous coronary interventions (PCI) and coronary artery bypass grafting (CABG) are established revascularization modalities, yet for some patients PCI and CABG are not an option, or do not result in complete revascularization. The report of the ESC joint study group for refractory angina define refractory angina as a chronic condition which cannot be controlled by medical therapy nor by revascularization, with an estimated prevalence of 30–50 000 patients/year in Europe . One of the treatment options for this patient category is electrical neurostimulation, either transcutaneous electrical nerve stimulation (TENS) with level B evidence, or spinal cord stimulation (SCS) with level A evidence . Patients describe the sensation of electrical stimulation as a tickling, pleasant feeling, in particular during angina. Small randomized trials have demonstrated a safe reduction in angina by electrical neurostimulation, enabling patients to prolong exercise without aggravating myocardial ischaemia. [2–6]
The effect of electrical neurostimulation on coronary flow has been studied in two mechanistic trials. The first trial showed that electrical neurostimulation increased resting coronary flow velocity in a not significantly diseased coronary artery . The second trial used Doppler flow wires in two coronary arteries and showed a decreased coronary flow in the stenotic artery with a concomitant increase in the nonstenotic artery, accompanied by a decrease in ST-T segment depression . This suggests that the myocardial area jeopardized by ischaemia is supplied with blood by an alternative pathway through the coronary collateral circulation . In a pilot study we observed trends that seemed to confirm this hypothesis . In this study the collateral perfusion was determined in an acute coronary occlusion model, during PCI. The collateral perfusion as Pw/Pa ratio can be calculated by dividing the wedge pressure during balloon inflation by the aorta pressure . Pharmacological intervention with adenosine was shown to improve collateral perfusion with ± 10%. In the present study we thought to investigate the effect of electrical neurostimulation on collateral perfusion, defined as a difference in Pw/Pa ratio.
Study population and Design
Percutaneous Coronary Intervention (PCI) procedure
All medication was continued until cardiac catheterization. All patients received aspirin (600 mg) and clopidogrel (600 mg) orally the day before PCI. At the beginning of the catheterization, all patients received heparin (5000 IU) intravenously as a bolus. In all patients cardiac catheterization was performed using the percutaneous femoral approach. A 6F sheath was inserted into the right femoral artery. A 6F guiding catheter was used for the insertion of a 0.36-mm (0.014-in) fiberoptic pressure-monitoring guide wire (Pressureguide, Radi Medical Systems AB, Uppsala, Sweden). The pressure wire was respectively, set at zero, calibrated, advanced through the catheter, equilibrated, introduced into the coronary artery, and positioned distal to the stenosis as previously described by Pijls et al. This technique has been shown to have a low variability and an excellent reproducibility [11, 13]
Transcutaneous Electrical NeuroStimulation (TENS)
The patients were treated with conventional TENS providing a continuous flow of symmetrical rectangular biphasic pulses (Schwa Medico, Pierenkemper GMBH; Wetzlarerstr. 41–43, D-35630 Ehringhausen, Germany). The frequency of stimulation was 100 Hz and the pulse-width 200 microsec. Before the PCI procedure the TENS electrodes were applied to the chest; the current was then increased to assess the motor threshold for each patient (i.e. the maximal tolerable stimulation without muscle activation). Active TENS was set at 90% of motor threshold (expressed in mA) . Patients experienced the sensation of electrical neurostimulation in the area, where the electrodes were placed. Electrical neurostimulation produces electrical disturbance on the ECG, although the cardiac rhythm can still be observed reliably, accurate ST shift analysis is not feasible. During TENS off, the stimulator was switched off, with the electrodes still applied to the chest.
Intra Coronary (IC) Pressure Measurements
At baseline the IC pressure drop over the stenosis (Pd/Pa ratio) was determined by simultaneous measurement of aortic pressure (Pa, mm Hg) and the distal coronary artery pressure (Pd mm Hg), under resting conditions, no hyperaemia was induced. The IC collateral flow (Pw/Pa ratio) was determined by simultaneous measurement of aortic pressure (Pa, mm Hg) and the distal coronary artery pressure during balloon occlusion (Pw, mm Hg) . Pa was measured at the tip of the guiding catheter; Pw was measured with the pressure wire. Central venous pressure was assumed to be 5 mm Hg.
Coronary angiography analysis
Angiograms were stored on digital media and analyzed visually for information of the number of diseased vessels. Collateral filling was graded according to the Rentrop classification: 0 = no filling of any collaterals, 1 = filling of side branches of the coronary artery by collaterals without visualization of the epicardial segment, 2 = partial filling of the epicardial coronary artery by collaterals, 3 = complete filling of the epicardial coronary artery by collaterals .
Nominal variables were compared using the Mann Whitney U test. Continuous, normally distributed variables are expressed as mean ± SD, these variables were compared between group 1 and 2 using the Student t-test. The Pw/Pa ratio during first and second ischaemic episode were compared using student t-test for paired data. Relations between the angiographic presence of collaterals or the number of diseased vessels and the Pw/Pa ratio were investigated, using the highest value of Pw/Pa ratio per patient. Additional analyses were performed, to compare characteristics of patients with and without an effect of electrical neurostimulation. Patients were dichotomized for absolute increase of Pw/Pa ratio of more or less than the mean Pw/Pa ratio value. All tests were two-sided and a p-value of <0.05 was considered significant. Statistical analysis was performed by using SPSS v12.0 software (SPSS Inc. Chicago, IL, USA).
N = 30
N = 30
68 ± 9
66 ± 11
28 ± 4
28 ± 4
Number of diseased vessels
1 vessel disease
2 vessel disease
3 vessel disease
Long acting nitrates
IC Pressure measurements
Coronary Angiographic analysis
Characteristics of groups dichotomized for effect of electrical neurostimulation
N = 28
N = 32
66 ± 10
67 ± 11
29 ± 5
27 ± 3
Number of diseased vessels
1 vessel disease
2 vessel disease
3 vessel disease
Long acting nitrates
Electrical neurostimulation resulted in 41 out of the 60 patients (68%) in improvement of the Pw/Pa ratio. The mean absolute change in Pw/Pa ratio in the 60 patients was 0.02 ± 0.03. There were 28 patients with a Pw/Pa ratio change in excess of this mean value, they were compared with 32 patients with a Pw/Pa ratio change less than the mean value. Additional analysis of these groups showed similar values for the stenosis related pressure drop under resting conditions (0.72 ± 0.26 vs. 0.79 ± 0.18, p = 0.24), and for electrical neurostimulation characteristics as reflected by motor threshold (7.4 ± 2.3 mA vs. 7.7 ± 2.5 mA, p = 0.66). Baseline clinical and angiographic characteristics of patients with and patients without an effect of electrical neurostimulation are shown in table 2.
In this study of 60 patients with significant coronary artery disease, the Pw/Pa ratio increased when electrical neurostimulation was active for 5 + 1 minutes and decreased when electrical neurostimulation was off for 5 + 1 minutes. The functional collateral perfusion was assessed by distal coronary pressure measurements during acute coronary occlusion. The target lesions of the patients included in this study were all visually significant stenoses on the coronary angiogram, also shown by non-invasive evidence of myocardial ischemia and reflected by the Pd/Pa ratio over the stenoses under resting conditions.
Electrical neurostimulation and perfusion
Some studies found no effect of electrical neurostimulation on the coronary or systemic haemodynamics and postulated an anti-ischaemic effect secondary to a decrease in myocardial oxygen consumption [16–18]. Where other studies have shown that electrical neurostimulation reduced afterload, following systemic vasodilatation  and a fall in systolic blood pressure possibly by reduced sympathetic activity . Our results show no significant change of the systolic blood pressure (Pa) by electrical neurostimulation in this study protocol. Other findings have resulted in a hypothesis that electrical neurostimulation has anti-ischaemic effects by increasing collateral perfusion . Other mechanisms that may explain the anti-ischaemic effects of electrical neurostimulation as reflected by less ST-T segment depression, include homogenization of myocardial perfusion documented in a study using positron emission tomography, and an increase in intracoronary blood flow velocity measured with a Doppler technique in patent coronary arteries [7, 8]. In our pilot study we found a trend towards an increase of the Pw/Pa ratio by electrical neurostimulation,  and therefore we performed this study, to prove or disprove the concept that electrical neurostimulation increases functional collateral perfusion as represented by the Pw/Pa ratio.
Collateral perfusion offers an alternative pathway of blood supply towards the ischaemic myocardial area, thereby decreasing myocardial ischaemia. The often limited functional significance of collateral blood supply makes improvement of coronary collateral circulation an interesting treatment target. Many different diagnostic methods have been developed to investigate the functional significance of coronary collaterals. A classification system for collateral filling from patent vessels to diseased vessels was developed by Rentrop using coronary angiography . This technique has a major limitation, as only spontaneous visible collateral vessels exceeding 100 microns in diameter can be visualized . A rather crude measure for coronary collaterals is the absence of myocardial ischaemia during coronary occlusion [23, 24]. More accurate, non-invasive diagnostic techniques to investigate coronary collaterals are positron emission tomography, [25, 26] and myocardial contrast echocardiography . Hemodynamic variables, reflecting the collateral circulation are excellent markers of the functional significance of collaterals, provided that these variables are measured in a reproducible and accurate manner [13, 28, 29]. Several studies have compared the various methods and have investigated whether different methods were complementary for the assessment of collaterals [30–33]. In a trial to measure the effect of adenosine on the collateral perfusion, pressure as well as flow velocity recordings were assessed . Both outcome measures showed similar changes in collateral perfusion. Pharmacological intervention with adenosine was shown to have a comparable impact on collateral perfusion as we have found with electrical neurostimulation.
Mechanism of collateral perfusion improvement
De Marchi et al found that sympathetic stimulation using the cold pressor test increased coronary collateral flow . Pohl et al found that exercise increased coronary collateral perfusion,  and that beta-blockade tended to reduce these effects, in agreement with previous clinical studies [34, 36]. The few experimental investigations on vasomotor properties of coronary collateral vessels suggest that the sympathetic nervous system might predominantly exert a β-receptor-mediated (i.e. vasodilative) effects on coronary collaterals [37, 38].
Electrical neurostimulation was found to decrease total body norepinephrine (NE) by 18% (p = 0.02) . During pacing NE levels increased by 47% (p = 0.02), while total cardiac norepinephrine spillover remained unchanged during pacing and active SCS. They suggest that the antiischemic effects of electrical neurostimulation are not exerted via cardiac sympathetic activity, although the overall sympathetic activity is decreased. Recently, 5 minutes of electrical neurostimulation at 90% of motor threshold was found to induce cutaneous vasodilation, mediated via antidromic activation of sensory fibers . Whether this mechanism accounts for the increase in collateral perfusion has not been elucidated yet.
In clinical practice electrical neurostimulation is often used for 1–3 hours. Since neurostimulation was active in our trial for only 5 + 1 minutes, only short-term effects of electrical neurostimulation can be studied. That PCI can be used as an investigational tool of acute myocardial ischemia was already proven in 1986 by Serruys . Since electrical neurostimulation disturbes the ECG, we were not able to perform additional ST shift analyses. Nevertheless, the relation between collateral perfusion and ischemia has already been investigated by others [13, 32, 42].
We assumed the central venous pressure (CVP) to be 5 mm Hg, but we did not measure the actual CVP in the individual patients. Nevertheless, this seems a reasonable assumption as we excluded all patients with clinical signs of heart failure, obstructive or restrictive pulmonary disease, and all patients had normal left ventricular function.
Clinical implications and future research
Our results indicate an acute positive effect of electrical neurostimulation on collateral perfusion. Our data do not allow conclusions with regard to the magnitude and/or durability of the collateral flow augmentation induced by electrical neurostimulation, but our data should be interpreted as "proof of concept", that electrical neurostimulation alleviates myocardial ischemia by an increase in collateral perfusion. Further studies are needed to investigate the magnitude and durability of the effects of neurostimulation on collateral perfusion.
We gratefully thank all co-workers of the catheterization laboratory.
- Mannheimer C, Camici P, Chester MR, Collins A, DeJongste M, Eliasson T, Follath F, Hellemans I, Herlitz J, Luscher T, Pasic M, Thelle D: The problem of chronic refractory angina; report from the ESC Joint Study Group on the Treatment of Refractory Angina. Eur Heart J. 2002, 23: 355-370. 10.1053/euhj.2001.2706.View ArticlePubMedGoogle Scholar
- Braunwald E, Epstein SE, Glick G, Wechsler AS, Braunwald NS: Relief of angina pectoris by electrical stimulation of the carotid-sinus nerves. N Engl J Med. 1967, 277: 1278-1283.View ArticlePubMedGoogle Scholar
- Di Pede F, Zuin G, Giada F, Pinato G, Turiano G, Bevilacqua M, Cazzin R, Raviele A: Long-term effects of spinal cord stimulation on myocardial ischemia and heart rate variability: results of a 48-hour ambulatory electrocardiographic monitoring. Ital Heart J. 2001, 2: 690-695.PubMedGoogle Scholar
- Hautvast RW, De Jongste MJ, Staal MJ, van Gilst WH, Lie KI: Spinal cord stimulation in chronic intractable angina pectoris: a randomized, controlled efficacy study. Am Heart J. 1998, 136: 1114-1120. 10.1016/S0002-8703(98)70171-1.View ArticlePubMedGoogle Scholar
- Jessurun GA, De Jongste MJ, Hautvast RW, Tio RA, Brouwer J, van Lelieveld S, Crijns HJ: Clinical follow-up after cessation of chronic electrical neuromodulation in patients with severe coronary artery disease: a prospective randomized controlled study on putative involvement of sympathetic activity. Pacing Clin Electrophysiol. 1999, 22: 1432-1439. 10.1111/j.1540-8159.1999.tb00346.x.View ArticlePubMedGoogle Scholar
- Mannheimer C, Eliasson T, Augustinsson LE, Blomstrand C, Emanuelsson H, Larsson S, Norrsell H, Hjalmarsson A: Electrical stimulation versus coronary artery bypass surgery in severe angina pectoris: the ESBY study. Circulation. 1998, 97: 1157-1163.View ArticlePubMedGoogle Scholar
- Chauhan A, Mullins PA, Thuraisingham SI, Taylor G, Petch MC, Schofield PM: Effect of transcutaneous electrical nerve stimulation on coronary blood flow. Circulation. 1994, 89: 694-702.View ArticlePubMedGoogle Scholar
- Jessurun GA, Tio RA, De Jongste MJ, Hautvast RW, Den Heijer P, Crijns HJ: Coronary blood flow dynamics during transcutaneous electrical nerve stimulation for stable angina pectoris associated with severe narrowing of one major coronary artery. Am J Cardiol. 1998, 82: 921-926. 10.1016/S0002-9149(98)00506-2.View ArticlePubMedGoogle Scholar
- Kolibash AJ, Bush CA, Wepsic RA, Schroeder DP, Tetalman MR, Lewis RP: Coronary collateral vessels: spectrum of physiologic capabilities with respect to providing rest and stress myocardial perfusion, maintenance of left ventricular function and protection against infarction. Am J Cardiol. 1982, 50: 230-238. 10.1016/0002-9149(82)90171-0.View ArticlePubMedGoogle Scholar
- de Vries J, Anthonio RL, DeJongste MJL, Jessurun GA, Tio RA, Zijlstra F: The effect of electrical neurostimulation on collateral perfusion. Neth Heart J. 2006, 14: 209-214.PubMedPubMed CentralGoogle Scholar
- Pijls NHJ, van Son JA, Kirkeeide RL, De Bruyne B, Gould KL: Experimental basis of determining maximum coronary, myocardial, and collateral bloodflow by pressure measurements for assessing functional stenosis severity before and after percutaneous transluminal coronary angioplasty. Circulation. 1993, 87 (4): 1354-1367.View ArticlePubMedGoogle Scholar
- Seiler C, Fleisch M, Billinger M, Meier B: Simultaneous intracoronary velocity- and pressure-derived assessment of adenosine-induced collateral hemodynamics in patients with one- to two-vessel coronary artery disease. J Am Coll Cardiol. 1999, 34: 1985-1994. 10.1016/S0735-1097(99)00470-2.View ArticlePubMedGoogle Scholar
- Pijls NH, Bech GJ, el Gamal MI, Bonnier HJ, De Bruyne B, Van Gelder B, Michels HR, Koolen JJ: Quantification of recruitable coronary collateral blood flow in conscious humans and its potential to predict future ischemic events. J Am Coll Cardiol. 1995, 25: 1522-1528. 10.1016/0735-1097(95)00111-G.View ArticlePubMedGoogle Scholar
- Linderoth B, Foreman RD: Physiology of spinal cord stimulation: Review and update. Neuromodulation. 1999, 2: 150-164. 10.1046/j.1525-1403.1999.00150.x.View ArticlePubMedGoogle Scholar
- Rentrop KP, Cohen M, Blanke H, Phillips RA: Changes in collateral channel filling immediately after controlled coronary artery occlusion by an angioplasty balloon in human subjects. J Am Coll Cardiol. 1985, 5: 587-592.View ArticlePubMedGoogle Scholar
- Mannheimer C, Eliasson T, Andersson B, Bergh CH, Augustinsson LE, Emanuelsson H, Waagstein F: Effects of spinal cord stimulation in angina pectoris induced by pacing and possible mechanisms of action. BMJ. 1993, 307: 477-480.View ArticlePubMedPubMed CentralGoogle Scholar
- Norrsell H, Eliasson T, Albertsson P, Augustinsson LE, Emanuelsson H, Eriksson P, Mannheimer C: Effects of spinal cord stimulation on coronary blood flow velocity. Coron Artery Dis. 1998, 9: 273-278. 10.1097/00019501-199809050-00005.View ArticlePubMedGoogle Scholar
- Sanderson JE, Woo KS, Chung HK, Chan WW, Tse LK, White HD: The effect of transcutaneous electrical nerve stimulation on coronary and systemic haemodynamics in syndrome X. Coron Artery Dis. 1996, 7: 547-552. 10.1097/00019501-199607000-00010.View ArticlePubMedGoogle Scholar
- Mannheimer C, Carlsson CA, Emanuelsson H, Vedin A, Waagstein F, Wilhelmsson C: The effects of transcutaneous electrical nerve stimulation in patients with severe angina pectoris. Circulation. 1985, 71: 308-316.View ArticlePubMedGoogle Scholar
- Emanuelsson H, Mannheimer C, Waagstein F, Wilhelmsson C: Catecholamine metabolism during pacing-induced angina pectoris and the effect of transcutaneous electrical nerve stimulation. Am Heart J. 1987, 114: 1360-1366. 10.1016/0002-8703(87)90537-0.View ArticlePubMedGoogle Scholar
- Hautvast RW, Blanksma PK, De Jongste MJ, Pruim J, van der Wall EE, Vaalburg W, Lie KI: Effect of spinal cord stimulation on myocardial blood flow assessed by positron emission tomography in patients with refractory angina pectoris. Am J Cardiol. 1996, 77: 462-467. 10.1016/S0002-9149(97)89338-1.View ArticlePubMedGoogle Scholar
- Rockstroh J, Brown BG: Coronary Collateral Size, Flow Capacity, and Growth: Estimates From the Angiogram in Patients With Obstructive Coronary Disease. Circulation. 2002, 105: 168-173. 10.1161/hc0202.102120.View ArticlePubMedGoogle Scholar
- Piek JJ, Koolen JJ, Hoedemaker G, David GK, Visser CA, Dunning AJ: Severity of single-vessel coronary arterial stenosis and duration of angina as determinants of recruitable collateral vessels during balloon angioplasty occlusion. Am J Cardiol. 1991, 67: 13-17. 10.1016/0002-9149(91)90091-X.View ArticlePubMedGoogle Scholar
- Miwa K, Fujita M, Kameyama T, Nakagawa K, Hirai T, Inoue H: Absence of myocardial ischemia during sudden controlled occlusion of coronary arteries in patients with well-developed collateral vessels. Coron Artery Dis. 1999, 10: 459-463. 10.1097/00019501-199910000-00005.View ArticlePubMedGoogle Scholar
- Demer LL, Gould KL, Goldstein RA, Kirkeeide RL: Noninvasive assessment of coronary collaterals in man by PET perfusion imaging. J Nucl Med. 1990, 31: 259-270.PubMedGoogle Scholar
- Garza D, Tosh AV, Roberti R, Dalal P, Reimers C, Ongseng F, Ventura B, Pompliano J, Horowitz SF: Detection of coronary collaterals using dipyridamole PET myocardial perfusion imaging with rubidium-82. J Nucl Med. 1997, 38: 39-43.PubMedGoogle Scholar
- de Marchi SF, Schwerzmann M, Fleisch M, Billinger M, Meier B, Seiler C: Quantitative contrast echocardiographic assessment of collateral derived myocardial perfusion during elective coronary angioplasty. Heart. 2001, 86: 324-329. 10.1136/heart.86.3.324.View ArticlePubMedPubMed CentralGoogle Scholar
- Pijls NH, Van Gelder B, Van der Voort P, Peels K, Bracke FA, Bonnier HJ, el Gamal MI: Fractional flow reserve. A useful index to evaluate the influence of an epicardial coronary stenosis on myocardial blood flow. Circulation. 1995, 92: 3183-3193.View ArticlePubMedGoogle Scholar
- Piek JJ, Koolen JJ, Metting van Rijn AC, Bot H, Hoedemaker G, David GK, Dunning AJ, Spaan JA, Visser CA: Spectral analysis of flow velocity in the contralateral artery during coronary angioplasty: a new method for assessing collateral flow. J Am Coll Cardiol. 1993, 21: 1574-1582.View ArticlePubMedGoogle Scholar
- van Liebergen RA, Piek JJ, Koch KT, de Winter RJ, Schotborgh CE, Lie KI: Quantification of collateral flow in humans: a comparison of angiographic, electrocardiographic and hemodynamic variables. J Am Coll Cardiol. 1999, 33: 670-677. 10.1016/S0735-1097(98)00640-8.View ArticlePubMedGoogle Scholar
- Seiler C, M F, A G, B M: Coronary collateral quantitation in patients with coronary artery disease using intravascular flow velocity or pressure measurements. Journal of the American College of Cardiology. 1998, 32: 1272-1279. 10.1016/S0735-1097(98)00384-2. [http://isi4.isiknowledge.com/portal.cgi?DestApp=WOS&Func=Frame]View ArticlePubMedGoogle Scholar
- Matsuo H, Watanabe S, Kadosaki T, Yamaki T, Tanaka S, Miyata S, Segawa T, Matsuno Y, Tomita M, Fujiwara H: Validation of collateral fractional flow reserve by myocardial perfusion imaging. Circulation. 2002, 105: 1060-1065. 10.1161/hc0902.104719.View ArticlePubMedGoogle Scholar
- Vogel R, Zbinden R, Indermuhle A, Windecker S, Meier B, Seiler C: Collateral-flow measurements in humans by myocardial contrast echocardiography: validation of coronary pressure-derived collateral-flow assessment. Eur Heart J. 2006, 27: 157-165. 10.1093/eurheartj/ehi585.View ArticlePubMedGoogle Scholar
- de Marchi SF, Schwerzmann M, Billinger M, Windecker S, Meier B, Seiler C: Sympathetic stimulation using the cold pressor test increases coronary collateral flow. Swiss Med Wkly. 2001, 131: 351-356.PubMedGoogle Scholar
- Pohl T, Wustmann K, Zbinden S, Windecker S, Mehta H, Meier B, Seiler C: Exercise-induced human coronary collateral function: quantitative assessment during acute coronary occlusions. Cardiology. 2003, 100: 53-60. 10.1159/000073039.View ArticlePubMedGoogle Scholar
- Kyriakides ZS, Kolettis T, Antoniadis A, Nikolaou N, Sbarouni E, Tzanalaridou E, Kremastinos DT: Beta-adrenergic blockade decreases coronary collateral blood flow in patients with coronary artery disease. Cardiovasc Drugs Ther. 1998, 12: 551-559. 10.1023/A:1007735320115.View ArticlePubMedGoogle Scholar
- Harrison DG, Chilian WM, Marcus ML: Absence of functioning alpha-adrenergic receptors in mature canine coronary collaterals. Circ Res. 1986, 59: 133-142.View ArticlePubMedGoogle Scholar
- Maruoka Y, McKirnan MD, Engler RL, Longhurst JC: Functional significance of alpha-adrenergic receptors in mature coronary collateral circulation of dogs. Am J Physiol. 1987, 253: H582-H590.PubMedGoogle Scholar
- Norrsell H, Eliasson T, Mannheimer C, Augustinsson LE, Bergh CH, Andersson B, Waagstein F, Friberg P: Effects of pacing-induced myocardial stress and spinal cord stimulation on whole body and cardiac norepinephrine spillover. Eur Heart J. 1997, 18: 1890-1896.View ArticlePubMedGoogle Scholar
- Tanaka S, Komori N, Barron KW, Chandler MJ, Linderoth B, Foreman RD: Mechanisms of sustained cutaneous vasodilation induced by spinal cord stimulation. Auton Neurosci. 2004, 114: 55-60. 10.1016/j.autneu.2004.07.004.View ArticlePubMedGoogle Scholar
- Serruys PWJC: Transluminal coronary angioplasty: an investigational tool and a non operative treatment of acute myocardial ischemia. 1986, University Hospital Rotterdam, The NetherlandsGoogle Scholar
- Sand NP, Rehling M, Bagger JP, Thuesen L, Flo C, Nielsen TT: Functional significance of recruitable collaterals during temporary coronary occlusion evaluated by 99mTc-sestamibi single-photon emission computerized tomography. J Am Coll Cardiol. 2000, 35: 624-632. 10.1016/S0735-1097(99)00587-2.View ArticlePubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2261/7/18/prepub
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