(Circulation. 1995;92:1860-1865.)
© 1995 American Heart Association, Inc.
Articles |
Contribution of Superior Vena Caval Flow to Total Cardiac Output in Children
A Doppler Echocardiographic Study
Presented in part at the 67th Scientific Session of the American Heart Association, Dallas, Tex, November 13-18, 1994.
From the University of Tennessee School of Medicine, Department of Pediatrics, Division of Cardiology, and the Department of Biostatistics and Epidemiology (K.L.A.), Memphis, Tenn.
Correspondence to Mubadda Salim, MD, Le Bonheur Children's Medical Center, 777 Washington Ave, Ste 215, Memphis, TN 38105.
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Abstract |
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Background After a cavopulmonary anastomosis, the superior vena caval flow, by virtue of being the effective pulmonary blood flow, is the most important factor influencing the systemic arterial saturation. Determination of the amount of this blood flow will allow a better understanding of the physiology of the circulation after this anastomosis. The purposes of this study were to determine the volumetric flow in the superior vena cava and to evaluate its contribution to the cardiac output as children grow.
Methods and Results Using two-dimensional and Doppler echocardiography, we measured the diameter of and mean flow velocities in the superior venae cavae and the pulmonary arteries of 145 healthy children. We calculated the volumetric flow in each vessel and determined the ratio of superior vena caval flow to total cardiac output. Cardiac output and superior vena caval flow increased with increasing age and body surface area. The superior vena caval flow accounted for 49% of cardiac output in newborn infants. This contribution increased to a maximum of 55% at the age of 2.5 years. Afterward, there was a slow decline in the ratio of superior vena caval–pulmonary arterial flow; it reached the adult value of 35% by 6.6 years of age.
Conclusions There is a maturational change in the superior vena caval contribution to total cardiac output in children. This is most likely related to somatic growth and changes in body segment proportions. This flow maturation may explain the higher systemic saturation in infants compared with older children after cavopulmonary anastomosis.
Key Words: cardiac output • regional blood flow • circulation • echocardiography • hemodynamics
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Introduction |
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Fetal lamb studies showed that 22.5% of systemic venous return to the right atrium is from the superior vena cava.1 2 In human adults, 35% of the cardiac output returns through the superior vena cava; the remainder, through the inferior vena cava and the coronary sinus.3 Few data exist regarding the distribution of systemic venous return to the heart in neonates, infants, and children. There are changes in the ratio of upper to lower body segments4 and in regional body surface area5 and thus regional blood flows as the human grows from newborn to adult. For example, the newborn infant's head accounts for 19% of the total body surface area compared with only 9% in an adult.5
The Glenn6 cavopulmonary shunt and the Fontan procedure7 channel systemic venous return directly to the pulmonary circulation. These operations are used to palliate a variety of complex congenital cardiac defects. Thus, information regarding caval flow would be important in our understanding of the physiological effects of these anastomoses. Therefore, the aims of this study were to evaluate quantitatively, by Doppler echocardiography, the superior vena caval volumetric flow and to determine its relative contribution to cardiac output in infants and children. Our previous data, in infants only, demonstrated a nearly equal distribution of blood flow in the superior and inferior venae cavae.8 The goal of this study was to define this distribution over the first 6.6 years of human growth.
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Methods |
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Study Subjects
Newborn infants (in the first week of life) were recruited from the well baby nursery of the Regional Medical Center in Memphis, Tenn. These infants were receiving standard medical care in the newborn nursery. The children were recruited from the pediatric clinics of the University of Tennessee during routine health maintenance visits. All infants and children had normal cardiovascular physical examinations and were in stable hemodynamic state. No children were acutely ill or were taking any medications at the time of the study. Children with conditions that may have caused an increase in their cardiac output, such as fever or anemia, were excluded. The protocol was approved by the University of Tennessee Institutional Review Board, and informed parental consent was obtained.
Doppler Echocardiography
A complete echocardiographic study
was performed
with a multiple-plane imaging approach; only children with normal
cardiac anatomy were included. Each child was examined in the
supine position. Variation in flow with changes in body position were
not part of the study design, in part to maintain the same
physiological conditions in all patients regardless
of age. To eliminate any possible effects of sedation on the cardiac
output and regional blood flows, no sedatives were used. We performed
these studies on infants and children in the awake and calm state. If
at any time a child became agitated, the study was stopped until the
child became calm. A bottle of formula was offered at times to help
soothe the child. If all failed, the study was terminated, and the
subject was excluded. Only completed studies, ie, studies that
recorded both the superior vena caval and pulmonary flows,
were included. All ultrasound recordings were obtained with a
Toshiba ultrasonoscope (model SH-140-Japan) using a 2.5-, 3.75-, or
5-MHz transducer and were recorded on super VHS videotape for later
analysis. Color-flow, pulse-wave, and continuous-wave
Doppler studies were used to assess intracardiac flows.
Pulmonary arterial flow velocities were
interrogated by color-flow Doppler to exclude infants or children
with patent ductus arteriosus. Pulmonary arterial
blood flow velocities were recorded from the parasternal short-axis
view. The pulse-wave Doppler sample volume was placed in the middle
of the main pulmonary artery distal to the pulmonary
valve and proximal to the pulmonary artery bifurcation. The
transducer was angled until the maximal frequency shift was
obtained.
Superior vena caval flow velocities were recorded from the subxyphoid sagittal view. The pulse-wave Doppler sample volume was placed in the superior vena cava just proximal to the cavoatrial junction. The Doppler beam was angled in a similar fashion to achieve the maximal frequency shift. We found this approach easier to use than the suprasternal notch window, especially in young children. In addition, it provided higher superior vena caval flow velocities than the suprasternal notch view. To time flow events, a simultaneous ECG was recorded with the Doppler flow velocities. Flow profiles were displayed as the frequency shift versus time at 50-mm/s sweep speed. The RR interval was measured from the same beats used to assess the velocity integral.
The pulmonary artery ID was measured in the parasternal short-axis view distal to the pulmonary valve (ie, the distance between the luminal bright edges of the pulmonary artery) from a midsystolic frame. The superior vena caval ID was measured from the subxyphoid sagittal view in most children. In some older children, because of the long distance between the transducer and the superior vena caval orifice, the diameter was assessed from a right parasternal view to obtain a more accurate measurement. The superior vena caval diameter was measured at the right atrial–superior vena caval junction. To eliminate any possible respiratory or cardiac cycle effects, superior vena caval diameter was measured from several different frames. Previous studies on chronically instrumented dogs demonstrated that the average change in the superior vena caval diameter secondary to cardiac pulsation was approximately 2% of the diameter.9 In addition, during thoracotomy in humans, the superior vena caval diameter looked roughly unchanged during positive pressure ventilation.10 These minimal changes cannot be distinguished with current echocardiographic measurement devices.
The mean velocity of blood flow was calculated from the integral of the Doppler velocity tracings. Flow time and heart rate were measured from the same beat. Because superior vena caval flow occurs throughout the cardiac cycle, its flow time was equal to the cardiac cycle. Pulmonary arterial flow time was equal to the time from the beginning to the end of the pulmonary arterial flow profile. Five or more cardiac cycles were analyzed for each patient. Because all infants and children were in normal hemodynamic state and fully hydrated during the echocardiographic study, we assumed that both the pulmonary artery and the superior vena cava had completely circular cross sections.
The equations used for flow were as follows: cardiac output=pulmonary flow=pulmonary artery cross-sectional areaxmean flow velocity in the main pulmonary artery (as recorded during the ejection phase of the cardiac cycle)xright ventricular ejection timexheart rate; superior vena caval flow=superior vena caval cross-sectional areaxmean superior vena caval flow velocityx60 (beat durationxheart rate=60 for superior vena caval flow). Body surface area was calculated according to the method of Haycock et al.11
Statistics
Data analysis was performed off-line with a
Dextra-200
digitizer (Micro Five, model 5.000, Samsung Electronics Co Ltd).
Statistical analyses were performed on a VAX mainframe with the
SAS REG procedure. Multiple regression analyses
were used to determine the best predictor equation for the superior
vena cava to pulmonary arterial flow ratio, with
age, height, weight, body surface area, sex, and race as independent
variables. Log and power transformations of the independent
variables were included in the statistical models in an attempt to
define the best fit. A value of P=.05 was used to determine
significance. Data are presented as mean±SD.
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Results |
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A total of 145 infants and children had complete data. Their mean age was 1.6±2.0 years (range, 1 day to 6.6 years). Their mean weight was 9.7±6.8 kg (range, 2.6 to 32.5 kg); their mean height was 73.3±24.0 cm (range, 32.0 to 136.5 cm). The mean body surface area was 0.44±0.23 m2 (range, 0.17 to 1.11 m2). All subjects had normal growth parameters.
Pulmonary artery anterograde flow occurred only during
systole. On the superior vena caval flow pattern, there were three
distinct waveforms during each cardiac cycle (Fig 1
).
The initial positive waveform (S in Fig 1) represented
anterograde flow during ventricular systole, ie,
the X descent on the normal jugular venous waveform during atrial
diastole. The second positive waveform of
anterograde flow (D) occurred during ventricular
diastole and represented the Y descent on the
jugular venous waveform; it coincided with the rapid
ventricular filling phase. The third, a negative waveform
(A), represented the retrograde flow during atrial systole,
ie, the "a" wave on the jugular venous tracing.12 We
were unable to demonstrate an H wave (an anterograde flow wave
in late diastole before the retrograde A flow wave) in
infants, presumably because of their high heart rates. In older
children with slower heart rates, however, the H wave was demonstrable.
The amplitude of the superior vena caval flow pattern, and hence the
amount of venous return, varied with respiration. We did not attempt to
quantify these variations. We attempted to correct for the respiratory
influence on flow velocity by averaging consecutive beats whenever
possible from the tracings for both the pulmonary artery and
the superior vena cava.
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The mean velocities of blood flow in the superior vena cava and the
pulmonary artery were 40±6 and 60±12 cm/s (range, 26 to 57
and 34 to 121 cm/s), respectively. The mean heart rate was 121±23 and
123±23 beats per minute [bpm] (range, 70 to 170 and 72 to 196
bpm),
respectively (the difference was not significant). As expected, heart
rate decreased with increasing age. The pulmonary artery and
superior vena caval diameters and flows correlated with age and body
surface area (Figs 2A through 2D and 3A through
2D). The best correlation of vessel diameter and flow
was with the square root of both age and body surface area (see the
Table). For the entire study population, the mean
indexed cardiac output was 5.2±1.4
L · min-1 · m-2, and the mean
indexed superior vena caval flow was 2.5±0.7
L · min-1 · m-2. The
relations between the ratio of superior vena caval flow to
pulmonary arterial flow and age, body surface area,
height, and weight were nonlinear. Polynomial analyses showed a
significant correlation of the ratios of superior vena caval to
pulmonary flows with age (P<.0035), weight
(P<.04), and body surface area (P<.03). The
correlation with height was nonsignificant. The best fit was with age
(Fig 4 and the Table). There was an increase in
the
contribution to the total cardiac output of the superior vena cava to a
maximum of 55% at the age of 2.5 years. Afterward, a slow decrease in
the contribution of the superior vena caval flow occurred that matched
that of an adult3 after the age of 6.6 years.
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Discussion |
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This study was designed to determine the amount of blood flow in the superior venae cavae of infants and children and the ratio of this flow to total cardiac output as the human grows from infancy to childhood. Similar studies using echocardiography in human fetuses13 and adults14 15 16 described flow patterns in the superior vena cava in normal and diseased hearts but did not attempt to measure the blood flow volume. Mohiaddin et al,3 using cine magnetic resonance velocity mapping, measured superior vena caval flow in adult subjects and found it to be equal to 35% of the systemic cardiac output. To the best of our knowledge, no reports have measured superior vena caval flow in children. This lack of data may be related to the difficulty of using invasive procedures in healthy children for research purposes. Moreover, the use of magnetic imaging is possible but requires prolonged sedation and, as such, may be considered somewhat invasive. Moreover, data from an animal study showed that the portion of the cardiac output returning through the superior vena cava decreased after the administration of anesthesia compared with that in the normal awake animal.17 Echocardiography provides a noninvasive method for assessing both cardiac anatomy and flow in awake, nonsedated subjects.
We were able to evaluate the amount of blood flow in the superior vena cava and the pulmonary artery in healthy children. The diameter of and flow in the pulmonary arteries of children increased with both increasing age and body surface area. Likewise, the increases in both the superior vena caval diameter and flow were strongly correlated with age and body surface area. The rate of increase of superior vena caval flow exceeded the rate of increase of pulmonary arterial flow during the first 3 years of life. This phenomenon resulted in an "age-dependent" relation, where the contribution of the superior vena caval flow to the cardiac output was 49% at birth and increased to 55% by the age of 2.5 to 3 years. Afterward, the superior vena caval contribution to total cardiac output declined and presumably the inferior vena caval contribution increased until the ratio of venous return in these veins reached the reported adult value by the age of 6.6 years.
These data provide insights into cardiac hemodynamics after palliative surgery of selected cyanotic congenital cardiac lesions with either the classic or the bidirectional cavopulmonary shunt. These types of anastomoses produce mixing of a volume of blood that is fully saturated with a volume of lower body venous return that is desaturated. The final systemic saturation depends on the ratio of these two volumes. We previously reported the ratio of superior vena caval flow to total cardiac output that was based on catheterization data of children after bidirectional cavopulmonary anastomosis.18 These catheterization-derived ratios were in complete agreement with the echocardiography- and Doppler-derived ratios reported here. We now show the range of superior vena caval flow over the initial 6 years of life. The changes in the amount of superior vena caval flow during the childhood years can explain the well-known phenomenon of the apparent "failure" of the cavopulmonary shunt (ie, decreased systemic arterial saturation) at the age of 6 to 8 years.19 This failure was observed with both the classic and bidirectional cavopulmonary anastomoses.19 20 21 22 23 In the numerous patients reported with late cavopulmonary shunt failure, there was no other physiologically sound explanation.21 No increase in the pulmonary vascular resistance was observed in these patients.23 Moreover, there was no microscopic or angiographic evidence of pulmonary vascular obstructive disease or of chronic pulmonary embolism.21 23 A few patients developed systemic venous collaterals that reduced their effective pulmonary blood flow by diverting part of the superior vena caval flow to the systemic venous circulation and thus bypassing the lungs.23 Therefore, the late "failure" of a classic or bidirectional Glenn procedure may result from the changes in flow distribution observed with growth, which reduce the proportion of the cardiac output that passes through the cavopulmonary anastomosis to become oxygenated. Before the widespread use of the Fontan operation, late failure of the cavopulmonary shunt was treated with a left-sided aortopulmonary shunt, thus increasing the effective pulmonary blood flow.21 23 Currently, completion of a bypass of the right side of the heart by the Fontan procedure relatively early in life prevents the manifestations of late cavopulmonary shunt failure.24 In a recent review of 66 patients after bidirectional cavopulmonary anastomosis, Gross et al25 reported lower systemic arterial saturations in older children compared with the younger ones. None of the older children with systemic desaturation had any significant pulmonary arteriovenous fistulae.
The diameter of the pulmonary artery in our study was 20% larger than that reported by Snider et al.26 This difference may be related to the measurement of the diameter from a midsystolic frame (in our study) rather than from an end-diastolic frame.26 Moreover, our method for measuring the pulmonary artery diameter may explain differences in mean indexed cardiac output in our study compared with previous reports.27 28 Robson et al29 demonstrated, by using a midsystolic frame to measure the pulmonary artery diameter, a similar cardiac index in the aorta and the pulmonary artery. Moreover, these indexes were similar to those reported here.
One limitation of this study is the use of only the pulmonary artery to measure cardiac output. Using the aorta or one of the AV valves to assess cardiac output would have allowed us to compare calculations. However, in the nonsedated child, this would have prolonged the study and increased apprehension. In addition, we did not correct for respiratory variation; we did, however, measure 5 or more consecutive beats for flow in both pulmonary arteries and superior venae cavae. This has been shown to minimize the variability of flow caused by respiration.30 Also, respiratory changes in the superior vena caval diameter were not always present in animal studies during normal respiration.17
In conclusion, there is a maturational change in the contribution of the superior vena caval flow to total cardiac output. This change explains the systemic arterial saturations of approximately 85% in infants (with 50% of the cardiac output provided by the superior vena cava) after cavopulmonary anastomosis. The decrease in systemic arterial saturation in these patients to approximately 60% in the later childhood years is related to a reduction of the proportional flow from the superior vena cava to 35% of cardiac output. Such information is crucial to our understanding of the physiology of cavopulmonary anastomosis and the timing of further interventions.
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Acknowledgments |
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We wish to thank Sheldon Korones, MD, Gerald Presbury, MD, Eniko Pivnick, MD, and the Pediatric House staff at the University of Tennessee, Memphis, for their assistance.
Received January 17, 1995; revision received April 13, 1995; accepted April 20, 1995.
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A. C. Lardo, S. A. Webber, A. Iyengar, P. J. del Nido, I. Friehs, and E. G. Cape BIDIRECTIONAL SUPERIOR CAVOPULMONARY ANASTOMOSIS IMPROVES MECHANICAL EFFICIENCY IN DILATED ATRIOPULMONARY CONNECTIONS J. Thorac. Cardiovasc. Surg., October 1, 1999; 118(4): 681 - 691. [Abstract] [Full Text] [PDF]
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A. E. Ensley, P. Lynch, G. P. Chatzimavroudis, C. Lucas, S. Sharma, and A. P. Yoganathan Toward designing the optimal total cavopulmonary connection: an in vitro study Ann. Thorac. Surg., October 1, 1999; 68(4): 1384 - 1390. [Abstract] [Full Text] [PDF]
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A. Gerdes, J. Kunze, G. Pfister, and H.-H. Sievers Addition of a small curvature reduces power losses across total cavopulmonary connections Ann. Thorac. Surg., June 1, 1999; 67(6): 1760 - 1764. [Abstract] [Full Text] [PDF]
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M. A. Fogel, P. M. Weinberg, J. Rychik, A. Hubbard, M. Jacobs, T. L. Spray, and J. Haselgrove Caval Contribution to Flow in the Branch Pulmonary Arteries of Fontan Patients With a Novel Application of Magnetic Resonance Presaturation Pulse Circulation, March 9, 1999; 99(9): 1215 - 1221. [Abstract] [Full Text] [PDF]
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H.-H. Sievers, A. Gerdes, J. Kunze, and G. Pfister Superior Hydrodynamics of a Modified Cavopulmonary Connection for the Norwood Operation Ann. Thorac. Surg., June 1, 1998; 65(6): 1741 - 1745. [Abstract] [Full Text] [PDF]
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W. P. Santamore, O. Barnea, C. J. Riordan, M. P. Ross, and E. H. Austin Theoretical optimization of pulmonary-to-systemic flow ratio after a bidirectional cavopulmonary anastomosis Am J Physiol Heart Circ Physiol, February 1, 1998; 274(2): H694 - H700. [Abstract] [Full Text] [PDF]
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L. Mace, P. Dervanian, J. Losay, T. A. Folliguet, J.-M. Grinda, S. Abdelmoulah, J.-F. Verrier, F. Santoro, and J.-Y. Neveux Bidirectional Inferior Vena Cava-Pulmonary Artery Shunt Ann. Thorac. Surg., May 1, 1997; 63(5): 1321 - 1325. [Abstract] [Full Text]
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