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Published in final edited form as:

Am J Cardiol. 2015 June 15; 115(12): 1739–1745. doi:10.1016/j.amjcard.2015.03.022.

Status of Systemic To Pulmonary Arterial Collateral Flow After

the Fontan Procedure
Kevin K. Whitehead, MD, PhD, Matthew A. Harris, MD*, Andrew C. Glatz, MD, Matthew J.
Gillespie, MD, Michael V. DiMaria, MD, Neil E. Harrison, MD, Yoav Dori, MD, PhD, Marc S.
Keller, MD, Jonathan J. Rome, MD, and Mark A. Fogel, MD*
Division of Cardiology and Department of Radiology, Children’s Hospital of Philadelphia,
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Philadelphia, PA

Abstract
We recently validated a method of quantifying systemic to pulmonary arterial collateral flow using
phase-contrast magnetic resonance imaging velocity mapping (PC-MRI). Cross-sectional data
suggest decreased collateral flow in patients with total cavopulmonary connections (TCPC)
compared to those with superior cavopulmonary connections (SCPC). However, no studies have
examined serial changes in collateral flow from SCPC to TCPC in the same patients. We sought to
examine differences in collateral flow between patients with superior cavopulmonary connections
(SCPC) and total cavopulmonary connections (TCPC). We quantified collateral flow by two
independent measures from 250 single ventricle studies in 219 different patients, (115 SCPC and
135 TCPC studies, 31 patients with both) and 18 controls, during routine studies using through-
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plane PC-MRI. Collateral flow was indexed to body surface area, aortic flow and pulmonary
venous flow. Regardless of indexing method, SCPC patients had significantly higher collateral
flow than TCPC patients (1.64±0.8 vs. 1.03±0.8 L/min/m2, p<0.001). In 31 patients who had serial
exams, collateral flow as a fraction of aortic flow increased early after TCPC completion. In
TCPC patients, indexed collateral flow demonstrated a significant negative correlation with time
from TCPC. In conclusion, both SCPC and TCPC patients demonstrate substantial collateral flow,
with SCPC patients having higher collateral flow than TCPC patients overall. Based on the paired
subset analysis, collateral flow does not decrease in the short term after TCPC completion and
trends toward increasing. In the long term, however, collateral flow decreases over time after
TCPC completion.
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© 2015 Published by Elsevier Inc.

Address for Correspondence: Kevin K. Whitehead, MD, PhD, Cardiology, 8th Floor Main Bldg, 8NW71, Children’s Hospital of
Philadelphia, 34th and Civic Center Blvd., Philadelphia, PA 19104, Phone: 267-426-0358, Fax: 215-590-5825,
[email protected].
*Equal contributors
Disclosures: None
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our
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Keywords
single ventricle; collateral circulation; magnetic resonance imaging; blood flow; Fontan

INTRODUCTION
Systemic to pulmonary collateral flow has been implicated as an important factor in the
outcome of patients with cavopulmonary palliation for single ventricle physiology 1,2,
though considerable controversy exists over its role 1–5. Collateral flow has been difficult to
study systematically because there has previously been no reliable way to measure it.
Several groups, including the authors, have recently demonstrated that collateral flow can be
accurately measured in patients with superior cavopulmonary connections (SCPC) using
phase contrast velocity mapping by magnetic resonance imaging (PC-MRI).6,7 Our group
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and others have used this method to demonstrate an association between collateral flow and
longer hospitalization and duration of pleural effusions following Fontan completion.8–10
The current study reports the largest series to date of single ventricle patients both in cross-
section as well as serially who underwent the previously described non-invasive method to
test the hypotheses that collateral flow is different between SCPC and TCPC patients and
represents a significant hemodynamic burden, and that collateral flow regresses with
increasing age in TCPC patients.

METHODS
In a prospectively enrolled cohort, we investigated 285 consecutive studies in patients with
SCPC or TCPC physiology at the Children’s Hospital of Philadelphia who underwent CMR
from April 2008 to December 2012. 35 studies were excluded for significant accessory
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pulmonary blood flow (antegrade ventricle to pulmonary artery or residual aortopulmonary

shunt flow), significant stent or coil artifacts that severely degraded the required PC-MRI
sequences, or limited exams that did not obtain complete PC-MRI. In the resultant 250
studies, 115 with SCPC and 135 with TCPC were included in the analysis. Thirty one
patients had CMR studies performed both before and after TCPC completion, allowing for a
longitudinal paired analysis in a small subset. To establish a control group, we enrolled 18
two-ventricle patients (2 patients without heart disease, 8 with minor aortic arch anomalies
and no prior surgery as well as 8 post-operative 2-ventricle repair patients with no known
residual shunts) who had complete pulmonary vein flow and branch pulmonary artery
measurements. Eleven of these patients also had vena cavae PC-MRI.

All patients underwent CMR imaging consisting of routine anatomical assessment as well as
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comprehensive through-plane PC-MRI as part of their routine clinical evaluation or research

protocol. Retrospectively gated, through-plane PC-MRI cines were performed in the aorta
(native and/or neo-aorta), superior and inferior vena cavae (SVC and IVC), right and left
pulmonary arteries (RPA and LPA), and right and left pulmonary veins (RPV and LPV). We
previously described the typical protocol with parameters and positions used (see Figure
1).6,11 When two outflows were present (aorta and neo-aorta), they were measured
separately and summed for the total aortic flow. When possible (based on whether all the

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pulmonary veins on one side formed a common vein of sufficient length), all the pulmonary
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veins on one side were measured in one acquisition. In a subset of patients, descending
aortic flow (DAo) at the level of the diaphragm was measured and compared to IVC flow.
PC-MRI sequences were analyzed using Argus flow analysis software on a Leonardo
workstation (Siemens Medical Solutions, Malvern PA) to obtain the Aortic, SVC, IVC,
RPA, LPA, RPV and LPV flows (Q). All contours and values were reviewed by a single
observer (KKW). To account for baseline offset in the PC-MRI, a static reference region
was contoured on all aortic PC-MRI as close to the vessel of interest as possible. If
correction made > 10% difference in the aortic flow, the corrected value was used and static
reference regions were checked on the remaining PC-MRI sequences. The following
calculations were then made for each patient:

(1)
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(2)

(3)

(4)

(5)

(6a)
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(6b)

(7a)

(7b)

where Qcoll-syst and Qcoll-pulm represent the estimated collateral flow by comparing supply
and return of the systemic and pulmonary systems respectively. Qcoll is the mean estimator
of collateral flow. QP and QS are the total pulmonary venous and systemic venous blood
flows respectively. QVR is the total venous return to the heart and should equal the aortic
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flow leaving the heart. QRL is the right to left shunt, which is equivalent to IVC flow in a
SCPC and fenestration flow in a Fontan. In two SCPC patients in whom there was an LSVC
to coronary sinus, the LSVC was included in the IVC flow for calculation purposes as the
LSVC flow represented systemic venous return not connected directly to the pulmonary
arterial system.

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Collateral flow was normalized to a) body surface area to obtain an indexed flow, b) aortic
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flow as a percentage of the entire cardiac output and c) total pulmonary vein flow (QRPV +
QLPV) to determine the percent of pulmonary flow from collateral flow. As a further check
of internal consistency, total venous return to the heart was calculated (Equation 6) to
compare to the aortic flow in the SCPC patients. Ventricular volumes, (indexed to body
surface area) were also obtained when available. Estimated indexed collateral flow was
compared to indexed end diastolic ventricular volumes by linear regression. The two
methods of calculating collateral flow, as well as aortic outflow and venous return to the
heart, were tested for internal consistency using linear regression, Bland-Altman analysis,
and intra-class correlation. Collateral flow parameters among control, TCPC and SCPC
patients were compared initially using single factor ANOVA. When a significant difference
across groups was detected by ANOVA, individual pairwise comparisons were tested using
unpaired Student t-tests with Bonferroni correction for multiple comparisons. For the 31
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patients who had both SCPC and TCPC exams, their SCPC and TCPC exams were
compared using paired Student t-tests. The authors had full access to the data and take
responsibility for its integrity. All authors have read and agree to the manuscript as written.
The study was approved by the institutional review board and informed consent was
obtained.

RESULTS
A summary of the demographics is presented in Table 1. Excellent agreement was
demonstrated between Qcoll-syst and Qcoll-pulm for both SCPC and TCPC, with negligible
bias at 0.02 L/min, a pooled 2 S.D. range of −0.6 to 0.6 L/min (Figure 2), and an intra-class
correlation coefficient of 0.84 (p<0.001). Table 2 summarizes the comparison between
SCPC, TCPC and controls. Whether collateral flow is normalized to BSA, aortic flow, or
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total pulmonary flow, SCPC patients on average demonstrated significantly higher collateral
flow than TCPC patients. The pulmonary to systemic flow ratio (QP/QS, see Equations 4 and
5), was significantly higher for TCPC than for SCPC. This appeared to be secondary to a
significant decrease in QS, as QP was not significantly different in SCPC and TCPC patients.

The data for the 31 patients who had collateral flow quantified serially pre-Fontan and post-
Fontan are summarized in Table 3. In contrast to the larger cohort of TCPC patients, these
subjects were generally much younger at the time of their post-Fontan exam. Twenty six
Fontan completions were fenestrated and five were not. There was a trend toward an
increase in collateral flow after Fontan that did not attain statistical significance (p=0.09).
However, when collateral flow was expressed as a percentage of aortic flow, the increase
reached significance (p=0.02). Note that QS decreased significantly from SCPC to TCPC in
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the face of no significant change in aortic flow. The right to left shunt decreased
significantly as expected, but was still sizeable because the majority of the patients had
fenestrations. Two patients had flow reversal in the superior Fontan baffle (between the
fenestration and pulmonary arteries).

The TCPC population demonstrated a significant negative correlation (r=−0.56, p<0.001)

between time from TCPC and indexed collateral flow (Figure 3). We were unable to identify

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a significant relation between indexed collateral flow for SCPC patients and time from
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SCPC surgery.

In assessing the relationship between collateral flow and ventricular volumes, patients with
significant valve regurgitation or ventricular dysfunction (defined as total regurgitant
fraction of greater than 25% or ejection fraction of less than 45%) were excluded. 36
patients with TCPC did not have ventricular volume imaging. In the remaining 190 patients
(100 SCPC, 90 TCPC), indexed end-diastolic volume correlated modestly but significantly
with indexed collateral flow (Figure 4) (r=0.47, p<0.001).

Some institutions advocate descending aorta flow as a surrogate to IVC flow, as it is easier
to obtain. Both were obtained in 116 pts, of which 47 were SCPC. In general there was
excellent linear correlation between the descending aorta and IVC flows (r=0.97, y=1.05x
−0.001). The mean difference in descending aorta and IVC flow for all patients was
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0.08±0.28 L/min. In the SCPC population, there were 5 patients in which IVC flow
exceeded descending aorta flow by greater than 0.3 L/min. In 3 of these patients, there was
clear CMR angiographic evidence of venous decompressing vessels from the
cavopulmonary circulation to the lower body which would account for the difference. In the
two SCPC pts in which descending aorta flow exceeded IVC flow by greater than 0.3 L/min,
both had CMR angiographic evidence of arterial collaterals arising from the abdominal
aorta. As a check of internal consistency, there was excellent agreement between the venous
return to the heart and the aortic flow (Figure 5). The mean difference was 0.014±0.18 L/
min.

DISCUSSION
While the TCPC group on average demonstrated significantly lower collateral flow than the
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SCPC group, the paired analysis suggests a more complex relationship. The significant
increase in collateral flow as a fraction of aortic flow and the trend toward an increase in
indexed collateral flow demonstrates that early after TCPC completion, collateral flow may
actually increase. This is in the context of a significantly reduced right to left shunt after
Fontan completion and increased Qp/Qs. One might speculate that this is due to more flow
through existing collateral connections as a result of increased systemic vascular resistance,
growth of new collateral connections as a result of post-operative inflammation, or both. The
decrease in QS supports the notion that the increase in collateral flow is at least in part
related to increases in systemic vascular resistance. Because total aortic output did not
decrease significantly, the decrease in corrected QS is probably not related to changes in
preload. The negative correlation between time from TCPC surgery and collateral flow in
the TCPC group suggests that these collateral vessels tend to regress over time after Fontan
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completion, though the process appears to take years or decades. While a prospective
longitudinal study may be needed to confirm these relationships, they are not surprising in
light of experimental data on collateral formation. In animal models, decreased pulmonary
artery flow results in dramatic increases in systemic to pulmonary flow via bronchial and
other systemic arteries. Furthermore, in these models it has been demonstrated that
reestablishment of normal pulmonary blood flow results in collateral involution.12,13

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The study also demonstrates that the previously described method of quantifying collateral
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flow in SCPC patients extends to the TCPC population with good agreement between the
two methods of calculating collateral flow. Both TCPC and SCPC populations demonstrate
a significant hemodynamic burden from collateral flow, evidenced by the significant
correlation between indexed collateral flow and ventricular volume in patients with no other
identifiable source of volume load.

Few studies have focused on quantifying systemic to pulmonary collateral flow in Fontan
patients. Grosse-Wortmann and colleagues described a method similar to the one presented
here to quantify collateral flow in patients with both SCPC and TCPC. They reported results
for 8 TCPC patients, and were thus not powered to show any trends in TCPC collateral flow.
There were two important methodological differences: 1) use of descending aortic flow as a
surrogate for IVC flow and 2) measured aortic flow distal to the aortopulmonary
anastomosis in patients with aortic reconstructions. Using descending aorta instead of IVC
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flow may introduce errors in patients with SCPC because of both decompressing veins and
collateral vessels originating from the abdominal aorta. There was evidence of both of these
scenarios in our SCPC cohort. The excellent agreement between descending aorta flow and
IVC flow in general suggests either approach is usually acceptable, but using IVC flow will
avoid these potential error sources in specific patients. The lack of significant systematic
error between the two estimators in our present study, in contrast to the methodologies
reported previously, provides strong evidence that our described technique is more reliable.
While previous studies have attempted to correct the DAo flow by directly measuring
decompressing flow, our experience has been that decompressing vessels can be a network
of small vessels which often cannot be measured directly.

A separate study on fenestration flow by Grosse-Wortmann et al found that in 23 patients

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studied 12 months after Fontan surgery, fenestration flow constituted 31% of aortic flow,
and that there was flow reversal above the fenestration in 14 of the 23 patients.14 In contrast,
in our paired cohort, on average 6 months out from Fontan surgery, fenestration flow only
accounted for 11% of aortic flow, and only 2 of 27 patients with fenestrations had flow
reversal in the Fontan baffle. Despite our group being closer to surgery, the groups had
similar age at time of exam and fenestration sizes were comparable (all 4 mm in our group,
range of 3–6 mm, average 4.2 mm in the Grosse-Wortmann study). Despite having a lower
right to left shunt, our patients had similar collateral flow (37% vs. 34% of aortic flow).
There were more patients with systemic right ventricle in our group (18 vs. 9). Given the
assertion in that manuscript that fenestration flow is associated with untwisting, the lower
fenestration flow could be associated with decreased diastolic function in our cohort.
However, one of the two patients with Fontan flow reversal was a patient with HLHS.
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Finally, Prakash and colleagues reviewed their CMR database and found 78 TCPC and 38
SCPC patients in whom collateral flow could be retrospectively calculated, consisting
generally of older TCPC patients who had not undergone modern staged palliation. They
were able to demonstrate that collateral flow was significantly lower in the TCPC group.15

There are significant limitations to the study. There is no gold standard with which to
compare the current method of quantifying collateral flow. However, PC-MRI is a well-
validated method over a wide range of flow rates for both venous and aortic flows.11,16–18 It

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should be noted that there are known errors which can occur in PC-MRI measurements due
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to intravoxel velocity dispersion and baseline offsets. Attempts to control for these factors
are imperfect and while errors are generally less than 5%, the errors can be additive when
calculating the differences from multiple flow measures. We attempted to minimize these
errors by averaging the two collateral flow estimators, which should reduce the estimator

error by since there appears to be little systematic error between the two estimators. 19
While the control population is well matched to the TCPC group, it is not age-matched to
the SCPC group. However, there were no significant differences in collateral flow
measurements between the 6 control patients less than 5 years of age and the 12 greater than
5 years, which should largely mitigate these concerns. The cross-sectional design of the
larger dataset in our study imposes limitations on conclusions regarding the relationship
between time from surgery and collateral flow. Because evidence of decreasing collateral
flow over time from Fontan completion is drawn from a cohort and not from serial
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evaluations, they could represent evolving differences in patient care, selection bias, or
patient attrition rather than true time effects. Similarly, the lack of a relationship between
time and collateral flow in SCPC patients may be confounded by referral bias toward more
sick early SCPC patients, as young SCPC patients tend to be referred for problems whereas
pre-TCPC studies are generally performed routinely. A longitudinal study will be required to
confirm these time-related effects.

Acknowledgments
K.K.W. was supported in part by NIH K23 Grant HL089647 and M.A.F. was supported in part by NIH R01 Grant
HL090615, both from the National Heart, Lung and Blood Institute.

The authors would like to acknowledge Veronica O’Connor, BSN for her invaluable help in patient recruitment.
Supported in part by NIH grants K23 HL089647 and R01 HL090615 from the NHLBI.
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Figure 1. Imaging Positions for PC-MRI

Schematic showing the imaging planes used to calculate collateral flow for TCPC. The
yellow bars represent velocity map locations. SVC and IVC are superior and inferior vena
cava, RPA and LPA (shown in both left panels) are right and left pulmonary artery, RUPV,
RLPV, LUPV, and LLPV are the right and left upper and lower pulmonary veins, LPV is the
left common pulmonary vein, Ao is ascending aorta.
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Figure 2. Comparison of two collateral estimators for all patients

Top: Qcoll-pulm vs. Qcoll-syst demonstrating excellent correlation between the two methods of
estimating systemic to pulmonary collateral flow for both SCPC and TCPC. Bottom: Bland-
Altman plot of the difference between the two systemic to pulmonary collateral flow
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estimators (Qcoll-pulm − Qcoll-syst) vs. the average of the two estimators (both in L/min). The
thin line represents the mean difference between the estimators and the thick lines represent
two standard deviations around the mean difference.
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Figure 3. Effect of time from TCPC completion on collateral flow

TCPC patients tend to have lower indexed collateral flow (Qcoll) with increased time from
TCPC completion. No relationship was identified between collateral flow (Qcoll) in SCPC
pts indexed to body surface area vs. time from SCPC.
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Figure 4. Effect of collateral flow on ventricular size

Indexed end-diastolic volume of the ventricle compared to the amount of indexed collateral
flow demonstrates a significant correlation. Note that patients who had other reasons for
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significant RV dilation (at least moderate valve regurgitation and/or ventricular dysfunction)
were excluded.
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Figure 5. Venous return vs. aortic flow

Venous return to the heart compared to aortic flow demonstrates excellent internal
consistency in the flow measurements.
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Table 1

Demographics of SCPC and TCPC patients.

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SCPC TCPC
n 115 135

Age at SCPC (years) 0.51±0.21 0.76±0.96

Age at TCPC (years) N/A 3.2±2.4

Time from SCPC 2.1±1.2 9.0±6.5

Time from TCPC N/A 8.9±8.2

Right Ventricle morphology 79 (69%) 76 (56%)

Left Ventricle morphology 29 (25%) 54 (40%)

Mixed morphology 7 (6%) 5 (4%)

Hypoplastic Left Heart Syndrome 56 (49%) 47 (35%)

Heterotaxy Syndrome 16 (14%) 9 (7%)

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Tricuspid atresia 11 (10%) 25 (19%)

Double Inlet Left Ventricle 7 (6%) 11 (8%)

Pulmonary atresia with intact ventricular septum 5 (4%) 1 (1%)

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Table 2
SCPC vs. TCPC patients vs. controls
Values listed are mean ±S.D., p-values are unpaired t-test with Bonferroni correction for multiple measures.

SCPC TCPC p-value SCPC vs. TCPC Controls p-value SCPC vs. Ctrl p-value TCPC vs. Ctrl
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n 115 135 18

Age (years) 2.6±1.2 12.2±8.8 <0.001 10.1±7.4 <0.001 1.0

Body surface area (m2) 0.53±0.10 1.16±0.51 <0.001 1.05±0.49 <0.001 1.0

QAo (L/min/m2) 4.85±1.1 3.61±1.0 <0.001 3.9±0.9 0.007 1.0

Qcoll (L/min/m2) 1.64±0.8 1.03±0.8 <0.001 0.21±0.27 <0.001 <0.001

100xQcoll/QAo (%) 34%±12% 26%±15% <0.001 5%±6 % <0.001 <0.001

100xQcoll/QP (%) 48%±17% 29%±17% <0.001 5%±5 % <0.001 <0.001

QP (L/min/m2) 3.4±0.9 3.3±0.8 1.0 4.1±1.0 0.006 0.005

QS (L/min/m2) 3.2±0.9 2.6±0.6 <0.001 3.7±0.8 0.11 <0.001

QPA (L/min/m2) 1.7±0.6 2.3±0.6 <0.001 3.9±0.9 <0.001 <0.001

QP/QS 1.10±0.3 1.31±0.40 <0.001 1.13±0.2 1.0 0.20

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Table 3
Comparison of collateral flow measurements in 31 pts who had both pre and post TCPC
MRI’s and no other interval interventions
Author Manuscript

A significant decrease was seen in collateral flow indexed to aortic flow from SCPC to TCPC. There were
also significant increases in QP and QP/QS, as well significant decreases in QS and right to left shunt.

SCPC TCPC p-value

n 31 31

Age (years) 2.9±1.3 4.0±1.3

Time from TCPC (years) −0.37±0.5 0.62±0.3

QAo (L/min/m2) 4.6±0.7 4.4±1.0 0.13

Qcoll (L/min/m2) 1.5±0.7 1.7±1.0 0.09

Qcoll/QAo x100 (%) 31±13 37±17 0.02

Author Manuscript

Qcoll/QP x100 (%) 45±17 41±18 0.15

QP (L/min/m2) 3.2±0.7 4.0±1.0 <0.001

QS (L/min/m2) 3.2±0.7 2.8±0.8 0.002

QPA (L/min/m2) 1.7±0.6 2.2±0.8 0.001

QP/QS 1.1±0.4 1.5±0.6 <0.001

Right to Left Shunt (L/min/m2) 1.5±0.5 0.5±0.4 <0.001

Author Manuscript
Author Manuscript

Am J Cardiol. Author manuscript; available in PMC 2016 June 15.