CLINICAL STUDIES
Long-term physical exercise and quantitatively assessed human coronary collateral circulation
Susanna Senti, MDa,
Martin Fleisch, MDa,
Michael Billinger, MDa,
Bernhard Meier, MD, FACCa and
Christian Seiler, MD, FACCa
a Section of Cardiology, University Hospital, Bern, Switzerland
Manuscript received December 15, 1997;
revised manuscript received March 19, 1998,
accepted March 20, 1998.
Address for correspondence: Dr. Christian Seiler, University Hospital, Section of Cardiology, Inselspital, Freiburgstrasse, CH-3010 Bern, Switzerland
christian.seiler{at}insel.ch
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Abstract
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Objectives. This prospective, cross-sectional study sought to determine an association between the level of long-term physical activity as well as other clinical and angiographic variables and an index of collateral flow to the vascular region undergoing percutaneous transluminal coronary angioplasty (PTCA).
Background. There is limited and conflicting information about the effect of physical exercise on the coronary collateral circulation in humans, partly because previous studies lacked a quantitative means of assessing collateral channels.
Methods. In 79 patients (mean [±SD] age 58 ± 10 years) with coronary artery disease undergoing PTCA (no transmural myocardial infarction), a coronary collateral flow index was determined as the ratio between the intracoronary (IC) distal flow velocity time integral during (Vioccl [cm]) and after (Viø-occl [cm]) PTCA of the stenosis. Vioccl/Viø-occl was measured by a 0.014-in. Doppler guide wire, from which an IC electrocardiogram (ECG) was also recorded. Patients without ECG ST-T wave changes during PTCA were considered to have sufficient collateral channels (n = 29); those with ST-T wave changes were considered to have insufficient collateral channels (n = 50). The level of long-term physical activity was determined by a structured interview (score from 1 to 4). Univariate and multivariate analyses were used to find associations between physical activity as well as 30 other clinical and angiographic variables and the collateral flow index.
Results. Long-term physical activity during leisure time, but not during work hours, and the severity of the stenosis undergoing PTCA were found to be independently and directly associated with sufficient versus insufficient collateral channels and with Vioccl/Viø-occl (leisure time physical activity [LTPA] score 3.3 ± 0.9 vs. 2.4 ± 1.0, p = 0.0002; percent diameter stenosis 88 ± 12% vs. 80 ± 14%, p = 0.001;  , p = 0.0002 for trend).
Conclusions. In patients with coronary artery disease, the level of long-term physical activity during leisure time and the severity of the stenosis undergoing PTCA are directly associated with the quantitative degree of collateral flow.
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Abbreviations and Acronyms
| | CAD | = coronary artery disease | | ECG | = electrocardiogram, electrocardiographic | | IC | = intracoronary | | LTPA | = leisure time physical activity | | PTCA | = percutaneous transluminal coronary angioplasty | | Vioccl | = flow velocity–time integral obtained distal to occluded stenosis | | Viø-occl | = flow velocity–time integral obtained distal to dilated stenosis | | WPA | = work-related physical activity |
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Higher levels of physical activity and cardiorespiratory fitness have been found to be associated with decreased mortality from coronary artery disease (CAD) (1–3). In a meta-analysis (4) of 10 cardiac rehabilitation program trials, including 4,347 postinfarction patients, exercise training was also shown to exert a secondary preventive effect on all-cause and cardiovascular mortality. The protective effect of sustained physical activity may be attributible to an array of adapations of the cardiocirculatory system, such as reduced activity of the sympathetic nervous system in fit compared with unfit people (5), less potential for platelet activation in active versus sedentary people (6), improved vasodilation capacity (7) and a less atherogenic lipoprotein profile (8). In patients with established CAD, exercise-induced, augmented development of the coronary collateral circulation could theoretically be a factor in the improved outcome compared with that of more sedentary patients (9–15). However, investigations in humans with CAD undergoing exercise programs have been controversial regarding the effect of such procedures on the growth of coronary anstomoses between nonischemic and ischemic myocardial regions (9,12). A major factor contributing to this dispute has been the lack of a truly quantitative means of measuring collateral flow in patients. Only a semiquantitative angiographic grading method for estimating the extent of spontaneously visible collateral channels (16) or acutely recruitable collateral channels during angioplasty has been achieved in patients (17,18). Potentially quantitative methods for collateral assessment analyzing the collateral perfusion pressure during percutaneous transluminal coronary angiography (PTCA) (19) and the blood flow velocity spectrum of the collateral donor vessel have been validated only against the semiquantitative angiographic "gold" standard (20,21). The recently developed ultrathin Doppler or pressure guide wires for providing an index for collateral flow during PTCA in very remote vascular areas have been evaluated extensively and have been shown to accurately measure collateral flow relative to "normal" flow through the patent vessel (22–24).
The purpose of this prospective, cross-sectional study was to test the hypothesis that the degree of long-term physical activity in patients with CAD is directly associated with an index of collateral flow to the vascular region undergoing PTCA. Other clinical and angiographic variables were also investigated in relation to coronary collateral channels sufficient or insufficient to prevent myocardial ischemia during PTCA.
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Methods
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Patients.
Seventy-nine patients (mean ± SD age 58 ± 10 years; 62 men, 17 women) with one- to two-vessel CAD and without a Q wave myocardial infarction were included in the study. All patients underwent PTCA because of CAD-related symptoms of at least one stenotic lesion.
This investigation was approved by the institutional ethics committee, and all patients gave informed consent to participate in the study.
The study cohort was classified into two groups: patients with coronary collateral channels sufficient (n = 29) and those with insufficient collateral channels (n = 50) to prevent electrocardiographic (ECG) signs of myocardial ischemia during balloon occlusion of the stenosis to be revascularized. Myocardial ischemia was defined as ST segment changes (>1 mm) on an intracoronary (IC) ECG lead obtained from the angioplasty guide wire in all patients (25) (Fig. 1).
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Figure 1 Schematic diagram of the heart showing the left anterior descending (LAD) and the left circumflex coronary arteries. The Doppler guide wire is positioned in the left circumflex coronary artery distal to the stenosis (occluder symbol) to be dilated. The IC (i.c.) ECG lead is obtained from the Doppler guide wire. During balloon occlusion of the stenosis, an instantaneous flow velocity signal (cm/s) and a flow velocity trend over 90 s (both shown on the black panel to the right) can be recorded. Compared with the status shortly before occlusion (white arrow), there are almost no flow velocity signals. The velocity-derived collateral flow index (no unit) is calculated as distal flow velocity time integral during (Vioccl or peak velocity integral [PVi] [cm]; in this case, 2.3 cm) divided by that after occlusion and after cessation of reactive hyperemia (Viø-occl [cm]; in this case, 23 cm). During stenosis occlusion, marked ST segment elevation on the IC ECG lead is present (arrowheads) (i.e., this patient has insufficient collateral channels. The difference between distal IC pressure and mean aortic pressure further illustrates the period of stenosis occlusion and also the low collateral flow index present in this case. APV = average peak velocity (cm/s; BAPV = basal average peak velocity (cm/s); DPVi = diastolic peak velocity time integral (cm); PAPV = peak average peak velocity; SPVi = systolic peak velocity time integral (cm).
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Cardiac catheterization and coronary angiography.
All patients underwent left heart catheterization for diagnostic purposes. Aortic pressure was measured using the PTCA guide catheter. Biplane left ventricular angiography was performed, followed by coronary angiography. Coronary artery stenoses were assessed quantitatively as percent diameter reduction using the guide catheter for calibration. The angiographic degree of collateral circulation (0 to 3) was determined according to the extent of epicardial coronary artery filling through collateral channels with contrast medium from the contralateral side before PTCA: 0 = no filling of the distal vessel through collateral channels; 1 = small side branches filled; 2 = major side branches of the main epicardial vessel filled; 3 = main epicardial vessel filled by collateral channels (16,17).
IC Doppler flow velocity measurements.
IC Doppler flow velocity measurements were performed using a 0.014-in. (1/3-mm diameter) PTCA Doppler guide wire with a 12-MHz piezolectric crystal at its tip (FloWire, EndoSonics). Validation of this Doppler guide wire has been previously described (26).
A velocity-derived index of collateral flow to the balloon-occluded vascular region relative to normal rest flow during vessel patency was determined as the ratio of the flow velocity– time integral distal to the occluded stenosis (Vioccl [cm]) divided by that obtained at identical location after PTCA (i.e., not occluded: Viø-occl [cm]): Vioccl/Viø-occl (Fig. 1) (23). In patients revealing bidirectional velocity signals, anterograde and retrograde signals were added to obtain Vioccl. Vioccl/Viø-occl >0.30, that is, collateral flow to the vascular region of interest >30% relative to the flow through the patent vessel after PTCA, has been shown to prevent myocardial ischemia at rest during vessel occlusion (22,23).
Determination of physical activity and other clinical variables.
The level of physical activity during work hours and leisure time was determined by a structured, standardized 30-min interview (27) covering the period of 1 to 2 years preceeding the actual hospital stay. The determination of the work-related physical activity score (WPA) included questions regarding the time on the job spent sitting or walking (assigned weight 0 to 4 according to frequency quintiles), the distance walked getting to and from the job (assigned weight 0 to 6, maximum >3 km), the type or types of transportation used to and from the job, the frequency of lifting or carrying heavy things (frequency tertiles assigned 0 to 6) and the work hours per week (assigned weight 0 to 5). The WPA score (1 to 4) was calculated according to the summed accumulated weights. A leisure time physical activity score (LTPA score 1–4) was calculated according to the type and frequency of activity engaged in during time off from the job (Table 1).
Additionally, the medical history and clinical and laboratory data were recorded. Both the interview on physical activity and that on clinical history were performed by an observer (S.S.) not involved in the acquisition and analysis of coronary collateral flow index data.
Study protocol.
After diagnostic coronary angiography, an interval of at least 10 min was allowed for dissipation of the effect of the nonionic contrast medium (iopamidol, 755 mg/ml) on coronary flow velocity and vasomotion. Repeated IC boluses of 0.2 mg of nitroglycerin were given to maintain a constant epicardial coronary artery diameter, thus to preventing any influence of changing epicardial vessel diameters on coronary flow indexes (28). The Doppler guide wire was positioned distal to the stenosis to be dilated. During the entire protocol, an IC ECG obtained from the Doppler guide wire and a three-lead surface ECG were recorded. Distal Vioccl was determined repetitively during balloon occlusion. After balloon deflation and cessation of reactive hyperemia, distal nonocclusive Viø-occl was determined.
After the patient’s return to the ward from the catheterization laboratory, the interview on physical activity, medical history and the recording of clinical data were performed.
Statistical analysis.
Univariate analysis
Between-group (sufficient and insufficient collateral channels) comparison of continuous data was performed with an unpaired two-sided Student t test. Continuous variables are provided as mean value ± SD. A chi-square test was used for comparison of categoric variables among the two study groups. Linear regression analysis and factorial analysis of variance were performed to determine a statistical trend between the collateral flow index and physical exercise scores and to calculate differences in the collateral flow index between the four physical exercise scores, respectively.
Multivariate analysis
A multivariate stepwise regression analysis (StatView) was performed that included all clinical and angiographic variables showing a statistically significant association with the two study groups by univariate analysis. Statistical significance was denoted at p < 0.05.
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Results
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Patient characteristics and CAD history.
There were no statistically significant differences among the two groups with sufficient and insufficient collateral channels with regard to patient age; gender; hemodynamic variables during cardiac catheterization, such as heart rate and blood pressure; frequency of cardiovascular risk factors, and drugs used (Table 2). There was a tendency to shorter duration of CAD and angina pectoris in patients with sufficient versus insufficient collateral channels (Table 3). Patients with sufficient collateral channels tended to be in a higher New York Heart Association functional class, tended to perform better on the exercise test before PTCA and more often had unstable angina pectoris than those with insufficient collateral channels (Table 3).
Coronary angiography.
The two study groups did not differ regarding the number of one- and two-vessel CAD, location of the stenosis to be dilated, dominance in vascular supply of the myocardium, total number of coronary stenoses (>50% diameter stenosis) and number of patients with serial stenoses in the vessel undergoing PTCA (Table 3). However, in patients with sufficient collateral channels a proximal location of the lesion was dilated more often, and the stenosis undergoing PTCA was more severe, than in those with insufficient collateral channels (Table 3, Fig. 2).
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Figure 2 Linear regression trend (y = 100 – 10x, r = 0.36, p = 0.0008) of stenosis severity (percent diameter stenosis) of the lesion to be dilated between patients with sufficient and insufficient collateral channels. Stenosis severity was significantly higher in patients with sufficient collateral channels than in those with insufficient collateral channels. Triangles = mean value; vertical lines = ±SD.
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Coronary collateral channels and physical activity score.
The variables indicative of degree of collateral circulation were significantly different between the two study groups; that is, patients with sufficient collateral channels had less angina pectoris during PTCA and had a higher angiographic degree of collateral circulation than those with insufficient collateral channels (Table 4). Vioccl/Viø-occl was 0.58 in the group with sufficient and 0.21 in patients with insufficient collateral channels (p = 0.0001). The left anterior descending coronary artery was the predominant collateral-supplying vessel in the group with sufficient collateral channels.
Physical activity scores
There was no significant difference in WPA scores between patients with sufficient and those with insufficient collateral channels. However, LTPA scores were significantly higher in patients with sufficient than in those with insufficient collateral channels (Table 4, Fig. 3). There was also a direct and significant association between LTPA score and Vioccl/Viø-occl, whereas no such relation was found for WPA score and Vioccl/Viø-occl (Fig. 4). Vioccl/Viø-occl values for WPA scores 1 to 4 were 0.38 ± 0.28, 0.27 ± 0.16, 0.40 ± 0.20 and 0.26 ± 0.11, respectively (p = NS) (Fig. 4). Vioccl/Viø-occl values for LTPA scores 1 to 4 were 0.22 ± 0.12, 0.26 ± 0.2, 0.32 ± 0.17 and 0.48 ± 0.26, respectively (p < 0.0001) (Fig. 4).
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Figure 3 Plot of individual LTPA data in patients with sufficient versus those with insufficient coronary collateral channels. There was a significant difference in LTPA score during leisure time between the two groups. Symbols as in Figure 2.
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Figure 4 Linear regression trends between individual collateral flow index data (no unit) and physical activity scores during working hours (left) and leisure time (right). There was a statistically significant trend between collateral flow index and leisure time physical activity score; p values between different activity scores were obtained by analysis of variance.
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Multivariate analysis.
Variables significantly associated with the study groups on univariate analysis were also included in the multivariate analysis: frequency of unstable angina pectoris, exercise score during leisure time (LTPA score), percent diameter stenosis of the lesion undergoing PTCA, occurrence of proximal stenosis location and contralateral vessel. The following regression equation was found (sufficient collateral channels assigned group 1, insufficient collaterals assigned group 2):  .
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Discussion
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The present study reveals that chronic physical activity during leisure time and the severity of the stenotic lesion to be dilated are factors directly associated with the amount of collateral flow to the occluded vascular region. The principal issues to be discussed are what indicators there are for or against a causality of the aforementioned relations or whether some patients with CAD are physically more active because their coronary collateral channels are developed more extensively than those of sedentary patients.
Physical exercise and coronary collateral channels: data from published reports.
In his account of angina pectoris, Heberden (29) writes of a patient with angina who was nearly cured of his symptoms by sawing wood for 30 min each day. The question of a selection bias (i.e., whether the patient chooses to saw wood because he is healthier to start with than the sedentary patient) arises irrespective of the study design of a case report; a retrospective, observational study; or a prospective investigation. This is due to the fact that randomized, controlled studies of physical activity and health benefits are not feasable because highly motivated, physically active people cannot be forced to participate in the control group and vice versa (30). Conversely, selection bias is not prevalent in animal studies on the subject of physical exercise and the coronary collateral circulation. Improvement of function and increase in the size of the collateral circulation in animals with occluded or stenotic coronary arteries have been shown repeatedly after exercise (31–35). Experimental animals have been mainly dogs and pigs, models that represent different forms of collateral growth more (pig) or less (dog) similar to that of humans (36). One of the principal methodologic advantages in experimental investigations is the possibility of directly measuring collateral flow, a prerequisite to assess any effect of physical exercise on collateral development.
So far, and with the exception of the present study, the effect of exercise training on the collateral circulation in patients with CAD has been assessed qualitatively by measurement of the rate–pressure product, using radionuclide methods and coronary angiography (14,37–47). An increase in rate–pressure product at the onset of myocardial ischemia has been shown by several investigators using different exercise programs (38–40) and may have been related to an increased myocardial oxygen supply from collateral growth. Most studies using radionuclide methods included only a few patients undergoing various exercise protocols (41,42,44). Of five such investigations (14,41–44), only two have revealed a reduction in reversible ischemia at higher workloads after a 1-year exercise program (14,44). The largest of the radionuclide studies (142 patients) has not documented a reduction in reversible ischemia at higher workloads in the 71 patients assigned to a 1-year exercise program (43). Qualitative coronary angiographic studies of collateral development in response to exercise have concluded that collateral growth occurs only with worsening CAD (40,45,46).
Much of the variable results of the aforementioned studies appear to be related to the choice of methodology by which the response of collateral channels to exercise has been assessed. Data from previous, mainly animal, studies have indicated several possible mechanisms by which collateral growth can be promoted.
Coronary collateral growth: role of ischemia and vasculogenesis.
Myocardial ischemia (biochemical paradigm)
One presently held view of collateral formation is that it occurs in response to coronary stenosis-induced myocardial ischemia, with either directly induced growth factor production or with resultant focal necrosis leading to cytokine production by leukocytes and monocytes with growth factor receptor upregulation (48). The angiogenic growth factors (49) promote capillary sprouting between the contralateral and ipsilateral (i.e., ischemic) vessels and thus lead to a reduction of minimal vascular resistance. The amount of ischemic myocardial tissue is certainly a direct determinant of the collateral growth stimulus in this scenario; that is, the size of the vascular territory downstream of a stenotic lesion (50) and the severity of the stenosis are key players in this regard. That high degree and proximally located stenoses are associated with more extensive collateral channels is a finding repeatedly documented in previous studies (51,52). The results of the present investigation concur with those data, and the direct correlation between physical exercise and collateral flow can be interpreted as causal on the basis of more severe ischemia being induced by more strenuous exercise. Work-related physical activity appears not to induce myocardial ischemia to the same degree as activity during leisure time and is, therefore, not related to the amount of collateral channels. The tendency of the right coronary artery as the ipsilateral vessel to be predominant in the group with sufficient collateral channels argues against the size of ischemia as a promotor of collateral growth because it supplies a smaller territory than the left coronary artery. In contrast to the recently published study by Piek et al. (52) revealing a direct association between the duration of angina pectoris and the recruitability of collateral channels, we found an insignificant tendency to a shorter course of angina in patients with more extensive collateral channels. This finding may represent a certain, although weak, argument for the notion that the higher leisure time physical activity is simply an expression of well developed collateral channels.
Vasculogenesis
The paradigm of recapitulated vasculogenesis as the mechanism promoting collateral growth is a biophysical one, starting from a stenosis-induced perfusion pressure gradient along preexistent coronary anastomoses from the nonstenotic to the ipsilateral vascular region, which leads to increased fluid shear stress with endothelial activation of the preformed collateral channels and a subsequent vascular remodeling, which finally decreases the pressure gradient (48). The result of the present and other studies of an independent association between high degree stenoses and widespread collateral channels perfectly agrees with the mechanism of vasculogenesis being the promotor of collateral growth. It is also compatible with a causal relation between physical exercise and collateral development because physical activity results in a larger pressure gradient across the stenosis.
Study limitations
The principal limitation of the present investigation is that it is cross-sectional, not longitudinal. However, because many of the longitudinal studies on exercise and coronary collateral channels published so far have not included a control group (38,41), the qualitative methodologic difference of our study seems not to be that large in this regard. The use of a much more sensitive method to assess collateral channels in the present versus previous studies appears to be sufficient to detect respective differences among various rather crudely estimated physical exercise levels. Inaccuracies in the characterization of physical activity by interview because of imprecise recall or recall bias, among other problems, are reflected in the large data variability in Figures 3 and 4. Determination of physical fitness using an exercise stress test is therefore regarded as a more reliable tool for studies such as the present one. The tendency, for patients with sufficient versus insufficient collateral channels to perform exercise better (Table 3) further supports the association found between the leisure time physical activity score and the collateral flow index.
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Footnotes
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This study was supported by a grant from the Swiss Heart Foundation, Bern (Dr. Seiler) and by Grant 32-49623.96 from the Swiss National Science Foundation, Bern (Dr. Seiler).
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C. Berry, K. P. Balachandran, P. L. L'Allier, J. Lesperance, R. Bonan, and K. G. Oldroyd
Importance of collateral circulation in coronary heart disease
Eur. Heart J.,
February 1, 2007;
28(3):
278 - 291.
[Abstract]
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P. Knaapen, L. J. Klein, R. Nijveldt, T. Germans, A. C. van Rossum, and C. C. de Cock
Coronary Collaterals in Full Effect
Circulation,
September 19, 2006;
114(12):
e501 - e502.
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M. Billinger, L. Raeber, C. Seiler, S. Windecker, B. Meier, and O. M. Hess
Coronary collateral perfusion in patients with coronary artery disease: effect of metoprolol
Eur. Heart J.,
April 1, 2004;
25(7):
565 - 570.
[Abstract]
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T. Pohl, C. Seiler, M. Billinger, E. Herren, K. Wustmann, H. Mehta, S. Windecker, F. R. Eberli, and B. Meier
Frequency distribution of collateral flow and factors influencing collateral channel development: Functional collateral channel measurement in 450 patients with coronary artery disease
J. Am. Coll. Cardiol.,
December 1, 2001;
38(7):
1872 - 1878.
[Abstract]
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S F de Marchi, M Schwerzmann, M Fleisch, M Billinger, B Meier, and C Seiler
Quantitative contrast echocardiographic assessment of collateral derived myocardial perfusion during elective coronary angioplasty
Heart,
September 1, 2001;
86(3):
324 - 329.
[Abstract]
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Abstract
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