Cardiovascular responses to exercise in healthy adults have been investigated by many studies (2,4,10,12,14,24) and are today well understood. On the other hand, data regarding cardiac responses to exercise in children are limited. Nevertheless, it seems important to determine whether the physiological and morphological specificities of prepubertal children have an impact on their cardiovascular responses to exercise.
In the pediatric literature, most of the studies have not collected data on adults, but instead compared data on children with adult values reported in other studies. However, several factors inherent to the protocol (i.e., body position (12,20) and pedaling rate (11)), and the methodological procedure employed (i.e., Doppler echocardiography or nuclear angiography) (4) as well as the aerobic potential (i.e., maximal oxygen uptake (V̇O2max), expressed in mL·min−1·kg−1) of the subjects (4,8,10,14,26) have been found to influence functional cardiac parameters. Consequently, direct comparisons of children and adults, by using a similar methodological procedure, are required to compare children’s and adults’ cardiovascular responses to exercise.
Among the studies that have directly compared children and adults, several studies have compared their cardiovascular responses to exercise at a given absolute metabolic rate or oxygen uptake (V̇O2) (9,29,30). These investigations mostly reported that children had a lower cardiac output (𝑄̇) and a higher arteriovenous oxygen uptake ((A-v)O2) at a given absolute V̇O2 (9,29,30). However, since children exercise at a higher relative exercise intensity, the comparison with adults appears to be limited (24). A more valid approach would be to compare children and adults at a same relative exercise intensity. Using such an approach, some studies have demonstrated that peak cardiac responses, scaled to body surface area (BSA), are not age-related when the aerobic potential of the subject is taken into account (16,24). To the best of our knowledge, only one study (24) has directly compared the patterns of rise during exercise in 𝑄̇, stroke volume (SV), heart rate (HR), and (A-v)O2. The main result of this investigation was the absence of any age-related differences in patterns of these variables during a progressive exercise performed until exhaustion. However, this study and any other studies have dealt with the underlying mechanisms responsible for the patterns of SV during a progressive exercise performed until exhaustion in children and adults.
To get an insight into the determinants of SV during exercise, the latter should be considered as a result of an adaptation of both the central and peripheral cardiovascular systems. Actually, SV is regulated by two opposing factors, the strength of contraction of the myocardium and the arterial pressure against which it expels the blood (afterload). The energy of contraction of the myocardium depends on Starling’s law of the heart, and therefore on the preload of the left ventricle, and on contractility, corresponding to the innate strength with which a myocyte contracts for a given initial stretch.
The development of indirect methodologies of left ventricular chamber size assessment has enabled investigators to study cardiovascular dynamics during exercise. Some echocardiographic parameters used in the literature represent good indications of preload (left ventricular end-diastolic dimension (LVEDD)), afterload (systemic vascular resistance (SVR)), and myocardium contractility (left ventricular shortening fraction (LVSF)). Moreover, Rowland and Blum (21) recently observed a high degree of reproducibility for estimating these parameters during exercise in prepubertal children.
This present study used Doppler and two-dimensional echocardiography to assess SV, 𝑄̇, and left ventricular dimensions during a progressive upright cycle exercise until exhaustion in active but untrained healthy children and adults. Our purpose was to test whether the patterns of HR, SV, and 𝑄̇, as well as the underlying mechanisms of SV (i.e., preload, afterload, and myocardium contractility) were similar in children and adults.
Approach to the problem and experimental design.
In order to investigate the age-related differences in cardiovascular responses to exercise, prepubertal boys and young adults underwent a progressive upright cycle exercise until exhaustion. Gas exchanges were measured continuously. A cardiovascular evaluation was performed at rest and during the final minute of each workload: HR, SV, and 𝑄̇ were calculated by Doppler echography from the suprasternal notch, LVEDD and left ventricular end-systolic dimension (LVESD) were measured by two-dimensional echography, and arterial pressures were assessed by manual sphygmomanometry. All these cardiac parameters were compared between boys and men at rest, at similar submaximal relative intensity and during maximal exercise.
Seventeen healthy boys with a mean age of 11.7 ± 0.6 yr and 23 young adult men with a mean age of 21.2 ± 2.7 yr agreed to participate in this study. All the subjects were nonobese and taking no medication that would affect aerobic exercise performance. None of the subjects in either group had any clinical or historical evidence of cardiovascular disease or hypertension, and all had a normal 12-lead electrocardiogram at rest. The children were volunteers from local schools. Most of them participated in several sports such as judo, soccer, or cycling, but none of them performed any sport intensively. They were examined clinically and the pubertal status was assessed using Tanner stages (28). All the boys were Tanner stage 1. The adult subjects were students and reported regular exercise habits (jogging, football, and handball). This study received approval from the local ethics committee, and written informed consent was obtained from all the children’s parents and all the adult subjects.
Maximal exercise protocol.
Each subject underwent a progressive upright cycle test until exhaustion on a mechanically braked ergometer (Ergomeca, Z.A. Le Pradet, France). Specific equipment was developed to limit body motions and to obtain quality echocardiographic recordings during exercise (Fig. 1). Before each test, the height and the distance of the crank gear was adjusted to ensure a similar angle of 120 degrees between the trunk and the legs for all the subjects. The pedaling rate was kept constant at 70 rpm for both the boys and the men. Initial workloads were 35 W and 70 W for the children and adults, respectively. Then, the increments were 17.5 W and 35 W for children and adults, respectively, with 2-min-30 and 3-min stages.
Gas exchanges were measured continuously during the resting period and the maximal test. Cardiovascular evaluation was performed at the end of the resting period, during the final minute of each workload, and during the last minute of the test. During the first 30 s, LVEDD and LVESD were measured by means of M-mode echocardiography. Then, during the following 30 s, 𝑄̇ was assessed by the Doppler technique. Blood pressures were measured in the right arm at the same time.
Expired gas analysis.
Gas exchanges (ventilation, oxygen uptake, and carbon dioxide output) were measured for each breath by means of a Cardiopulmonary Exercise System (MedGraphics, CPX-D, Medical Graphic Corporation, St. Paul, MN). Subjects wore a nose clip and respired through a mouthpiece. Inspired and expired gas flows were continuously monitored by means of a pneumotachograph connected to a MedGraphics respiratory flow transducer. Gas concentrations were evaluated using rapidly responding gas analyzers. Before each test, the gas analyzers were calibrated against precision analyzed gas mixtures (CO2, 4%; O2, 15%; precision, 0.1% certified by the manufacturer). Maximal oxygen uptake (V̇O2max) was achieved when at least two of the following criteria were achieved: 1) maximal HR was near the maximal theoretical maximal HR, 2) maximal respiratory exchange ratio was greater than 1.1, and 3) the subjects were unable to maintain the pedaling rate despite verbal encouragement.
Echocardiography Doppler measurements.
Echocardiography Doppler measurements were carried out according to the recommendations of the American Society of Echocardiography. Measurements of LVEDD and LVESD were performed with a 3.5-MHz transducer using standard M-mode echocardiography guided by two-dimensional echocardiography (Sigma HVD 44, Kontron Médical, ZA Les Gâtines, Plaisir, France). These measurements were made just distal to the tips of the mitral valve leaflets, as determined by parasternal and short axis views. The largest distance from the posterior edge of the ventricular septum to the left ventricular endocardial surface was recorded as LVEDD. The LVESD was determined as the shortest distance from the free wall endocardial echo in systole to the ventricular septum. LVSF was calculated as the quotient (LVEDD − LVESD)/LVEDD × 100. Each value was averaged from five to seven measurements. Values were indexed to square root body surface area according to Daniels et al. (7).
SV and 𝑄̇ were estimated using the standard Doppler echocardiography technique, according to the methodological procedure used by Rowland et al. (23). This method has been validated against direct method in both children (1) and adults (13). Briefly, SV was estimated as the product of the aortic root area (see below) and integral of ascending blood velocity and time. The velocity of blood in the ascending aorta was recorded with a 2.0-MHz continuous wave Doppler transducer (Pedof, Kontron Médical, ZA Les Gâtines, Plaisir, France) directly from the suprasternal notch. The outline contour of the velocity curve over time (VTI) was traced manually. The end of each VTI was taken as the observed closure of the aortic valve. Values for VTI were averaged from five to seven curves, with the highest values demonstrating crisp spectral envelopes. The maximal systolic diameter of the ascending aorta was measured at rest before each test by two-dimensional echocardiography in the parasternal long axis view with the subject in the pedaling position. The measurement was recorded from inner to inner edge at the level of the insertion of the aortic valve leaflets. The resting value was used for all resting and exercise SV calculations (3). The cross-sectional area of the ascending aorta was calculated from the mean diameter, considering the aorta to be circular. The following derived variables were calculated from primary measurements: SV = VTI × aortic root area; 𝑄̇ = SV × HR. Values were indexed to body size area. Arteriovenous oxygen difference was calculated as V̇O2/𝑄̇.
All records were analyzed blindly on two separate days by an experienced operator as well as on another day by a different cardiologist in order to assess intraobserver and interobserver variability, respectively. Since both intraobserver and interobserver variability were low (coefficient of variation lower than 6% for all cardiac parameters), values presented in the present article were those obtained by the first cardiologist.
Blood pressure measurements.
Auscultatory cuff blood pressures were obtained in the right arm using manual sphygmomanometry. Muffling of the Korotkoff sounds defined diastolic pressure (DAP). Mean arterial pressure (MAP) was calculated as one third of the pulse pressure plus the diastolic pressure. SVR was calculated as the quotient of MAP divided by 𝑄̇.
The results are presented as mean ± SD. Comparison of cardiac variables during submaximal exercise were expressed in terms of relative exercise intensity, and only values of submax-1 (between 30% and 45% of maximal aerobic power), submax-2 (between 55% and 70% of maximal aerobic power), and submax-3 (between 80% and 90% of maximal aerobic power) exercise intensities were reported. For each cardiac variable, and at each exercise intensity, the comparison between the children and adults was performed by two-way analysis of variance (group × exercise intensity) with repeated measures. Differences in peak/rest ratios between the boys and men were assessed by a nonparametric Mann-Whitney test. The relationship between 𝑄̇ and V̇O2 (L·min−1) for the two groups was assessed by linear regression, and the differences in slopes and intercepts were evaluated by a covariance of heterogeneous regression lines (StatView 5.0 software, SAS Institute, Inc., Cary, NC). Statistical significance for all analyses was defined as P < 0.05.
The average body mass of the boys was 39.0 ± 7.0 kg, height was 150.1 ± 8.4 cm, and body surface area was 1.29 ± 0.15 m2. For the men, these values were 67.5 ± 6.2 kg, 179.6 ± 6.2 cm, and 1.85 ± 0.10 m2, respectively. The bioenergetic parameters determined during the maximal aerobic test are presented in Table 1. Whatever the exercise intensity, V̇O2 indexed to body mass was not significantly different between the boys and men. At maximal exercise, V̇O2max levels were 53.1 ± 7.3 and 52.9 ± 7.3 mL·min−1·kg−1 in the children and adults (NS), respectively, indicating that these two groups had the same aerobic potential.
Submaximal responses to exercise were evaluated at similar intensities for both the boys and the men. Average percentages of maximal aerobic power were 38.6 ± 4.8% and 37.8 ± 4.8% (NS) for submax-1 exercise intensity, 61.7 ± 4.7% and 61.3 ± 4.3% (NS) for submax-2 exercise intensity, 83.0 ± 4.6% and 83.9 ± 4.1% (NS) for submax-3 exercise intensity, for the boys and men, respectively.
Resting, submaximal, and peak values of cardiac variables obtained by Doppler echocardiography are presented in Table 1. 𝑄̇ was higher at rest and during all exercise intensities in the adults than in the children. The higher 𝑄̇ values were explained only by higher SV, since no difference was observed for HR at rest and during all exercise workloads. However, no significant differences were observed in cardiac index and stroke index at rest and at all intensity levels (Figs. 2 and 3) in both groups. The significant rise in 𝑄̇ from rest to maximal exercise resulted from a continuous increase in HR until maximal exhaustion, and an increase in SV only between rest and submax-1 exercise intensity in both groups. Average values of the ratio SVmax/SVrest were 1.33 and 1.30 in the children and adults, respectively (NS).
Regression lines for 𝑄̇ versus V̇O2, evaluated from submaximal exercise data were as follows: boys, 𝑄̇ = 5.10 + 4.54 V̇O2 (P < 0.001); and men, 𝑄̇ = 6.24 + 4.58 V̇O2 (P < 0.001). The slopes of these relationships were similar (NS), whereas differences existed regarding y intercepts (P < 0.05).
Arteriovenous oxygen uptake data are presented in Table 1. For both groups, (A-v)O2 rose progressively from rest to maximal exercise. Mean values were higher in the men for all exercise intensities.
Cardiac parameters obtained by M-mode echocardiography are presented in Table 2. LVEDD and LVESD were greater in the adults whatever the conditions (i.e., rest and exercise). However, when these data were related to square root BSA, no significant differences were obtained between the boys and men (Fig. 3). For the boys and men, respectively, average values of the ratio LVEDDmax/LVEDDrest were 0.94 ± 0.08 and 0.96 ± 0.08 (NS) and average values of the ratio LVESDmax/LVESDrest were 0.76 ± 0.07 and 0.74 ± 0.09 (NS).
In both groups, patterns of LVEDD and LVESD indexed to square root BSA are presented in Figure 4. LVEDD remained fairly constant from rest to submax-1 exercise, and then declined gradually until maximal exercise. LVESD decreased continuously from rest to maximal exercise, with a more rapid fall at the onset of exercise. Consequently, LVSF rose continuously throughout the test (Fig. 5). At maximal exercise, LVSF reached 49.1 ± 6.9 in boys and 50.3 ± 4.5 in men (NS).
DAP and SAP are presented in Table 3. At rest and during submaximal and maximal exercise, no significant differences were observed between DAP of the boys and men, whereas SAP was significantly higher in the adults. During exercise, similar patterns of DAP and SAP were obtained for the boys and men. Although DAP remained constant from rest to maximal exercise, SAP rose until exhaustion. The patterns of SVR are presented in Figure 6. SVR was significantly higher in the boys at rest and at all exercise intensities. In both groups, SVR fell rapidly at the onset of exercise and declined more slowly thereafter up to maximal exercise.
The major finding of this study was a lack of any age-related differences in central cardiovascular responses during progressive cycle exercise until exhaustion in subjects having the same aerobic potential. However, peripheral cardiovascular variables distinguished the men from the boys, since (A-v)O2 was higher and SVR lower in adults than in children at rest and during exercise.
Cardiovascular adaptation during exercise depends on numerous factors, such as aerobic potential of the subjects or the methodological procedure used. In our study, we compared directly a group of prepubertal boys with a group of young adults, using a similar methodological procedure (i.e., same cardiovascular evaluation method, same upright position, and same pedaling rate). Moreover, both groups had a similar aerobic potential, since no significant differences were found in mean V̇O2max expressed relative to body mass (53.1 ± 7.3 and 52.9 ± 7.3 mL · min−1 · kg−1 in boys and men, respectively). These V̇O2max levels were in accordance with those previously described in active but non–endurance-trained boys (6,24,29) and men (2,14,24).
According to the Fick equation, the rise in V̇O2 during exercise resulted in an adaptation of both the central (𝑄̇) and peripheral ((A-v)O2) cardiovascular systems. Regarding the central factors, the rise in 𝑄̇ resulted from changes in both HR and SV. In our study, HR increased significantly with exercise intensity from rest to maximal exercise in both groups (Table 1). On the other hand, SV rose significantly at the onset of exercise and remained fairly constant until maximal exercise (Table 1). This pattern of SV conformed to the classic literature description of a plateau of SV at a workload of approximately 40% of V̇O2max in slightly trained children (9,22,24,25) and adults (2,8,12,14,24) evaluated in an upright position. When 𝑄̇ and SV were related to BSA, no significant differences were obtained between the boys and men at rest, during submaximal and maximal exercise (Figs. 2 and 3). These results were in accordance with previous studies (16,24). They indicated that 𝑄̇ responses to a similar exercise intensity were not age-related in subjects having the same aerobic potential. They indicated also that the contribution of SV and HR in the production of 𝑄̇ was similar in the boys and men during exercise. This was in accordance with the one study available in the pediatric literature, by Rowland et al. (24), showing no significant difference in the patterns of HR, SV, and 𝑄̇ between boys and men during a progressive exercise performed until exhaustion. However, when regarding the peripheral factors, our results reported a significantly higher (A-v)O2 in adults than in children at rest and during submaximal and maximal exercise. This finding was in accordance with other reports (16,24). Using the same methodological procedure, Rowland et al. (24) reported maximal (A-v)O2 of 13.9 ± 3.0 and 17.2 ± 4.5 mL·dL−1, respectively, in boys and men. These values are similar to those reported in our study (Table 1). In a longitudinal study performed in circumpubertal children, Cunningham et al. (6) found the highest increase in (A-v)O2 in the year before the peak height velocity. These age-related differences are partly explained by a greater hemoglobin (Hb) concentration after the pubertal period (5). During exercise, another explanation for the lower (A-v)O2 in children could be their reduced capacity for redistribution of blood volume from nonexercising tissue to the active muscle (24). More studies are needed to understand further these age-related differences in (A-v)O2.
In brief, during a progressive exercise performed until exhaustion, the only parameter of the Fick equation that distinguished the men from the boys at a similar relative exercise intensity was a higher (A-v)O2 in the adults, since no significant differences were found in values of SV and 𝑄̇ indexed to body surface area. From rest to maximal exercise, patterns of HR, SV, and therefore 𝑄̇ were strictly similar in boys and men.
It must be highlighted that a similar SV adaptation during exercise in the boys and men might not be necessarily explained by the same underlying mechanisms. The main interest of this study was to investigate these mechanisms, considering SV as a result of a combination of preload, afterload, and myocardium contractility. To the best of our knowledge, no study has directly compared in the same experiment these mechanisms in children and adults. The major finding of the present study was that SV adaptations during exercise in boys and men were attributable to similar mechanisms. In fact, similar patterns of LVEDD (i.e., index of preload), SVR (i.e., index of afterload), and LVSF (i.e., index of myocardium overall contractility) were found in the boys and men. In children, most of the studies that have dealt with left ventricular dimensions have been performed during submaximal exercise only, with subjects in a conventional supine position to optimize echocardiography measurements (18,19). Two recent studies used echocardiography in semisupine (25) and upright (21) positions until exhaustion, but did not compare their results with a group of adult subjects.
In our children and adults, LVEDD seemed to increase slightly from rest to submax-1 exercise, and then decrease until maximal exercise. Rowland and Blum (21) reported a similar pattern in prepubertal children in an upright position. In their study, LVEDD increased from 39.9 ± 3.2 mm at rest to 41.1 ± 2.5 mm at 50 W in a group of prepubertal boys performing an upright cycle exercise test. LVEDD increased to a similar extent in our study in the children, from 44.4 ± 3.8 mm at rest to 45.8 ± 4.9 mm during the first workload. Other studies performed in children reported a regular decrease in LVEDD from rest to maximal exercise, without an initial increase at the onset of exercise (18,19,25). However, these studies were performed in supine or semisupine positions, which probably improved cardiac filling at rest and then limited the increase in cardiac filling during the transition from rest to exercise. LVESD decreased from rest to maximal exercise in our children and adults (Table 2). This pattern was in accordance with previous data reported in children (18,19,21,25) and adults (12,20,27) and was the consequence of several regulatory mechanisms. In adults, the extent to which the mechanism of Frank-Starling accounts for changes in LVSF and SV has been debated for decades. In the present study, the decrease in LVESD in both groups resulted in an improvement in the systolic function despite a decrease in LVEDD, thus demonstrating increased myocardial contractility under catecholamine influence without any intervention of the Frank-Starling mechanism. This result has been supported by many studies performed in an upright position that concluded a limited intervention of this mechanism in humans during a moderate to high level of exercise (10,14). Moreover, SVR decreased similarly in both groups until exhaustion (Fig. 6). Since arterial pressure depends partly on SVR, less of the contractile energy was consumed in raising the pressure during the isovolumetric phase, and more was used for blood ejection in circulation. The higher decrease in SVR at the beginning of exercise in the boys and men suggested that peripheral vasodilatation played a major role in the decrease in LVESD and therefore in the rise of SV at the onset of exercise. LVSF, a marker of overall contractility, resulted in LVEDD and LVESD patterns. For both the children and the adults, our results showed a continuous and similar increase in LVSF from rest to maximal exercise. As exercise intensity increased, SV was maintained by increased myocardial contractility to expel a similar volume of blood in a shorter systolic ejection time (24,25).
To the best of our knowledge, no other studies have compared directly LVEDD, LVESD, LVSF, and SVR in boys and men having a similar aerobic potential. In the present study, no significant differences were found between the boys and men in LVEDD, LVESD scaled to square root body surface area, and LVSF at rest and during submaximal and maximal exercise. The values of the left ventricular diameters and LVSF of our children and adults agreed with other studies using echography in children (21,25) and adults (27) with similar aerobic potentials. On the other hand, SVR was significantly higher in our children than in the adults at rest and during exercise (Fig. 6). A similar result was reported by Turley and Wilmore (29). The higher SVR in their children was explained by their higher muscle blood flow induced by the small muscle mass used to achieve the same absolute rate of work as in the adults. However, in our study, this explanation was not valid because the boys and the men were exercising at a similar relative exercise intensity. Another explanation for these differences in SVR between boys and men could be attributed to the calculation of SVR by means of the Poiseuille law. An error in the assessment of 𝑄̇ or MAP could induce an error in SVR. In our study, 𝑄̇ was estimated using a similar Doppler echocardiography procedure for both groups, and the equation of the regression lines conformed with the literature in children and in adults (24). Moreover, MAP was conventionally estimated as the product of the diastolic pressure plus one third of the pulse pressure. Initially used at rest, this method provides a valid estimation of MAP over a wide range of exercise intensities (15). Thus, the higher SVR levels in children were probably reliable and not calculation dependent. Further studies are required to understand to a greater extent the effect of the higher afterload on the left ventricular function during exercise in children.
We did not use invasive methods to assess 𝑄̇ and left ventricular dimensions, as they would have been inappropriate in a healthy population. Even if several sources of errors may be associated with the measurement of 𝑄̇ by the Doppler technique, such as the accuracy of the measurement of the aortic diameter, maintenance of a constant Doppler angle, or the existence of a turbulent flow, the values found for both groups indicated that this method provided valid calculations of 𝑄̇ and SV during exercise in the children and adults. Moreover, the reproducibility of this method was investigated in our laboratory. It has been shown that Doppler echocardiography is highly reproducible (coefficient of variation < 8%) on test-retest measurements during submaximal and maximal exercise in children and adults (17). We used time-movement echocardiography to assess left ventricular dimension to exercise. This technique has been validated against the radionuclide angiography method both at rest and during exercise (4). Rowland and Blum (21) recently obtained a good reproducibility of the assessment of left ventricular size by two-dimensional echography during exercise in children. However, echocardiography measurements of left ventricular dimensions are sometimes difficult to interpret during heavy exercise because of the body motions induced by pedaling and the high respiratory frequency. To resolve these problems, specific equipment was developed to limit body motions. The specific position adopted seemed to be optimal to obtain quality echocardiography images during high intensities and maximal exercise. This position could be considered as an upright position. Indeed, the ratios of SVmax/SVrest, in our study 1.30 and 1.33 in the boys and men, respectively (NS), were similar to those reported in other studies performed in an upright position in children (24) and adults (12). In our study, the left ventricular dimensions were determined after the exercise test from recordings obtained during exercise. Only good-quality images were selected to improve analysis. This procedure was especially important during high-intensity exercise when the expansion of the lung was greater, and helped to provide a valid determination of cardiac dynamics for both healthy boys and men.
In conclusion, this study failed to reveal any age-related differences in cardiovascular adaptation during a progressive upright exercise until exhaustion. Both groups used similar mechanisms for increasing SV and 𝑄̇. The increase in SV only at the onset of exercise for both the children and the adults resulted from a constant cardiac filling at the beginning of exercise (probably because of the improvement in the cardiac filling rate by the peripheral pump in a shorter diastolic time), and a major decrease in afterload. SV then remained fairly constant, as a consequence of a decrease in both LVEDD and LVESD. The only variables that distinguished the boys from the men were a lower (A-v)O2 and a higher SVR in the children than in the adults. More studies are required to understand further the effect of pubertal status on the peripheral cardiovascular system (1,13).
Address for correspondence: Stéphane Nottin, Laboratoire de Physiologie des Adaptations Cardiovasculaires à L’Exercice, Faculté des Sciences, Département STAPS, 33 rue Louis Pasteur, 84000 Avignon, France; E-mail: firstname.lastname@example.org.
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Keywords:©2002The American College of Sports Medicine
PREPUBERTAL BOYS; CARDIAC OUTPUT; STROKE VOLUME; LEFT VENTRICULAR DIMENSIONS; EXERCISE