Ann Thorac Surg 2006;81:1002-1007
© 2006 The Society of Thoracic Surgeons
Original article: Cardiovascular
Velocity-Encoded Magnetic Resonance Image Assessment of Regional Aortic Flow in Coarctation Patients
Tiffany J. Riehle, MD
a
,
c
,
John N. Oshinski, PhD
a
,
Marijn E. Brummer, MD
a
,
Jennifer Favaloro-Sabatier, MApStat
a
,
William T. Mahle, MD
b
,
c
,
Derek A. Fyfe, MD, PhD
b
,
c
,
*
,
Kirk R. Kanter, MD
a
,
c
,
W. James Parks, MD
b
,
c
a Emory University School of Medicine, Atlanta, Georgia
b Sibley Heart Center Cardiology, Atlanta, Georgia
c Children's Healthcare of Atlanta, Atlanta, Georgia
Accepted for publication July 5, 2005.
Abbreviations and Acronyms CoA = descending aortic diameter at the coarctation or juxtaductal site; CI = confidence interval; DA = descending aortic diameter at the diaphragm site;
P = pressure gradient; TE = echo time; TR = repetition time; VENC-MRI = velocity-encoded cine magnetic resonance imaging;
v
max
= maximum velocity
* Address correspondence to Dr Fyfe, Children's Healthcare of Atlanta, Department of Cardiology, 1405 Clifton Rd NE, Atlanta, GA 30322 (Email: tr7766{at}aol.com).
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Abstract
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BACKGROUND: During primary coarctation repair, collateral blood vessels contribute significantly to distal perfusion. We sought to determine if velocity-encoded cine magnetic resonance imaging (VENC-MRI) could provide insight into anatomy and hemodynamics of collateral flow in patients with unrepaired coarctation.
METHODS: Sixteen patients (median age, 6.2 years; range, 1 to 18) with discrete coarctation (65% severe, 29% mild-moderate) and 10 controls (median age, 12.0 years; range, 9 to 15) without left-sided heart lesions were referred for cardiac MRI. Flow volumes were calculated from VENC-MRI images at the coarctation (proximal), diaphragm (distal), and midway between the two points (midpoint). A means model, repeated-measure analysis, was performed for volumes.
RESULTS: In coarctation patients, flow volumes increased by 59% (p = 0.0002) from coarctation to diaphragm, primarily between the proximal and midpoint sites (by 77%, p < 0.0001). In controls, flow volumes decreased by 11% along the entire aortic study length. Coarctation volumes were lower than controls by 54% (p = 0.0003) at the proximal site but showed no statistical difference at the midpoint or diaphragm.
CONCLUSIONS: Coarctation flow volumes maximally increase in the upper thoracic aorta, but approach normal flow volumes in the lower thoracic region. Arteries arising from mid and lower thoracic level, such as those supplying the anterior spinal cord, may have nearly normal flow if collaterals are present. Velocity-encoded MRI can evaluate flow in patients who have poor collateral circulation to improve surgical planning and decrease neurologic complications of coarctation repair.
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Introduction
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Coarctation of the aorta is the third most common congenital cardiovascular malformation, and usually occurs as a discrete stenosis just distal to the left subclavian artery. Depending on the severity of aortic obstruction, collateral vessels may develop early in the neonatal period [1] to maintain distal perfusion. In animal models of discrete coarctation, there was an increased number and size of intercostals and internal thoracic arteries, with collaterals often entering near the coarctation [2]. In normal circulation, descending aortic flow volumes decrease distally as blood flows from the high-pressure aorta into low-pressure peripheral vessels [3, 4]. Conversely, coarctations have low descending aortic pressure so there is retrograde flow from collateral vessels into the descending aorta to improve distal perfusion. In computational models, collateral vessels reduce the pressure difference between the coarctation and downstream vessels, and were the main influence in downstream flow volumes [5].
Knowledge of collateral blood vessel hemodynamics may impact surgical planning and morbidity. During primary repair of discrete coarctation, well-developed collaterals maintain adequate distal perfusion pressure, which is important for spinal cord protection [6]. Paraplegia and bladder dysfunction is associated with anterior spinal cord ischemia [7], and correlates to low distal perfusion pressure [6]. Interestingly, the incidence of paraplegia in primary coarctation repair is lower (0.5% to 1.5%) than for other descending aortic operations (0.3% to 13%), possibly owing to the presence of collateral blood vessels [6]. The anterior spinal cord is supplied by the anterior spinal artery, which is functionally divided and has various contributing vessels. The poorest vascular segment is the middle division, supplied by middle to lower thoracic vessels [8, 9]. Any compromise to blood flow in these arteries can lead to spinal cord injury, including prolonged aortic cross-clamp time, hypotension, and interruption or absence of vital collateral circulation [710]. In a 20-year meta-analysis of paraplegia complicating aortic surgery on patients without collaterals, paraplegia occurred in 10% of patients, one fifth of whom had simple aortic cross-clamping done. A significantly lower percentage developed paraplegia if distal perfusion was augmented [11]. Thus, understanding the location and hemodynamics of collateral circulation may help to minimize a rare but important surgical risk.
Coarctation and collateral vessel morphology can be assessed by static, dynamic, and cross-sectional phase velocity magnetic resonance imaging (MRI) [4, 1215]. Velocity-encoded cine MRI (VENC-MRI) is an accurate method to measure flow volumes and velocities in patients with coarctation of the aorta and collateral vessels [3, 1618]. The purpose of this study was to use VENC-MRI to localize regional descending aortic flow volumes due to collateral vessels in patients with discrete coarctation.
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Material and Methods
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Study Groups
This was a retrospective study done on patients who had MRI evaluation from November 1992 to February 2002 at Children's Healthcare of Atlanta, in accordance with the standards of the Emory University and Children's Healthcare of Atlanta Institutional Review Boards (IRB 132.2002, approved March 7, 2002, and 02.122, approved April 18, 2002). The study group included 16 patients, median age 6.2 years (range, 1 to 18), who had discrete, previously unrepaired coarctation of the aorta. Since the study focus was on preoperative coarctations without confounding congenital heart disease, exclusion criteria included: previous surgical repair of the coarctation, complex diagnoses (parachute mitral valve, atrial septal defect, ventricular septal defect), and significant aortic stenosis (velocity gradient >1.04 m/s). Patients were compared with 10 controls with no coarctation, who were previously repaired tetralogy of Fallot patients referred for MRI evaluation of right ventricular volume and function. The control subjects had no left-sided heart abnormalities, and had a median age of 12.0 years (range, 9 to 15). The difference in median age between the controls and study group was not significant (p = 0.19). Medical records were reviewed for patient demographics and for arm-leg cuff blood pressure gradients, obtained before, but not necessarily the same day as, the MRI.
Static and Dynamic MR Imaging
All patients were evaluated on a GE Twinspeed and LX 1.5 T MR scanners (GE Medical Systems, Milwaukee, Wisconsin). Fast-field gradient imaging with echo train sequencing was acquired for slice localization, followed by double inversion image recovery sequence for black blood anatomic depiction: slice thickness, 7 to 9 mm; field of view, 26 to 32 mm; repetitition time/echo time (TR/TE), 1100/40 ms; flip angle, 90 degrees; and matrix, 256 x 160. Retrospectively gated steady-state free precession or fast card (FFE) imaging sequences were acquired in the axial, coronal, and selected sagittal oblique planes through the aortic arch and descending aorta to the level of the diaphragm. The parameters were similar except for the following: TR/TE, 3.9/2.0 ms; flip angle, 45 degrees; nex, 3 acquisitions; and matrix size, 192 x 160. Data were analyzed with a Sun SPARC10 workstation (Sun Microsystems, California) using the Flow program version 4.0 (AZL, Leiden, Netherlands) for quantitative flow analysis by two readers. The maximum diameter of the aorta at the coarctation site (CoA), and of the descending aorta at the diaphragm (DA) were measured from sagittal oblique and axial images. In controls, the proximal descending aorta in the juxtaductal region immediately below the left subclavian artery and the aorta at the diaphragm were compared with the study group. The severity of coarctation was determined by a ratio of CoA/DA diameters, and compared with similar ratios in controls.
Velocity-Encoded MR Imaging
Images best illustrating the descending aorta and coarctation site were used for planning velocity data acquisition, as seen in Figure 1. Velocity-encoded cine magnetic resonance imaging was a technique employed to measure flow volumes throughout a cardiac cycle at three selected locations within the descending aorta. Velocity-encoded cine magnetic resonance imaging through-plane imaging was obtained with a slice thickness, 5 mm; field of view, 30 mm (patient size determined); VENC (velocity), 200 to 500 cm/s (gradient dependent); TR/TE, 4 to 6 ms; flip angle, 20 to 30 degrees; matrix size, 128 x 256; temporal resolution, 30 phases per heartbeat. The three locations for VENC-MRI were designated proximal (at the coarctation site or juxtaductal region), distal (at the diaphragm), and midpoint (at a position midway between proximal and distal). Flow (cc/min) was measured at each of the three locations. Maximum velocities at the locations was also acquired and used to estimate peak pressure gradients at the coarctation site using the simplified Bernoulli equation (
P = 4v
max
2), where
P = pressure gradient, and v
max = maximum velocity.

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Fig 1. Oblique sagittal retrospectively gated steady-state free precession magnetic resonance imaging sequences image of a 12-year-old patient with discrete coarctation. The flow measurement plane is placed orthogonally to the blood flow at each location in the descending aorta: at the coarctation site, at the diaphragm, and halfway between both sites.
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Statistical Analysis
Repeated-measures analysis was performed for flow volume with a means model using SAS Proc Mixed (version 9.1; SAS Institute, Cary, North Carolina), which provided separate estimates of the means by location on the aorta and by patient group. A compound symmetry variance-covariance structure among the repeated measurements was assumed for flow volume, and robust estimates of the standard errors of parameters were used to perform statistical tests and construct 95% confidence intervals (CI). To compare the pairwise differences between the model-based group means (least-squares means) at each location, t-tests were used. The model-based means are unbiased with unbalanced and missing data, so long as the missing data are noninformative (missing at random). The reported p values are two-sided, and a p value of 0.05 or less was considered to indicate statistical significance.
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Results
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Anatomic Characteristics
Demographic and anatomic features evaluated by MRI are reported in Table 1. These include dilation of the ascending and descending aorta, arch hypoplasia, left ventricular hypertrophy, mitral regurgitation, and nonstenotic bicuspid aortic valve. There was no statistical difference in flow volumes between patients with and without bicuspid aortic valves (p = 0.11). Additionally, cuff blood pressure gradients varied between 20 and 74 mm Hg, and did not correlate by regression analysis to the degree of collateralization seen on MRI (r = 0.19, p = 0.2).
The coarctation severity was determined by the ratio of CoA/DA diameters, with ratios of 0.5 or less considered severe; greater than 0.50, mild-moderate; and 0.85 or greater, normal. Although the literature varies in description of coarctation severity, several reports have characterized a ratio of CoA/DA diameter of 0.5 or less to indicate significant coarctation [12, 13]. Table 2
shows the CoA/DA ratios, as well as the estimated peak pressure gradient, calculated from velocity measurements, through the coarctation site (CoA). Velocity could not be measured in 2 patients, owing to aliasing and turbulence. In the coarctation group, 11 patients (64.7%) had severe coarctations with ratios 0.21 to 0.50, whereas 5 (29.4%) had mild-moderate coarctations with ratios 0.60 to 0.75. All the controls had normal CoA/DA diameter ratios (0.85 to 1.30). The mean diameter ratio of the coarctation group (0.47 ± 0.16) was significantly different from that of the control group (1.11 ± 0.14).
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Table 2. Coarctation or Juxtaductal Site to Descending Aorta at the Diaphragm (CoA/DA) Ratios and Pressure Gradients for Coarctation Patients, Grouped by Coarctation Severity, Compared With Control CoA/DA Ratios
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Local Aortic Blood Flow Volumes
The coarctation and control groups model-based mean flow volumes at three selected levels within the aorta, with 95% CI bars, are depicted in Figure 2. Table 3
also shows the percent-change in volume between various sites. Flow volume from coarctation to diaphragm followed different patterns in each group. For coarctation patients, there was a 77% increase in blood flow from the proximal (1,191 cc/min, 95% CI: 750 to 1,632) to midpoint sites (2,102 cc/min, 95% CI: 1,518 to 2,686; p < 0.0001). Flow decreased insignificantly from midpoint (2,102 cc/min) to distal aorta (1,895 cc/min, 95% CI: 1,446 to 2,345; p = 0.08). Overall blood volume increased by 59%, or 705 cc/min (95% CI: 348 to 1,061) from coarctation to diaphragm (p = 0.0002). In the control group, volume steadily decreased throughout the aorta from proximal (2,567 cc/min, 95% CI: 2,012 to 3,122), to midpoint (2,512 cc/min, 95% CI: 1,967 to 3,057), to distal location (2,284 cc/min, 95% CI: 1,866 to 2,703). The only significant change in volume was an overall 11% decrease from proximal to distal (p = 0.02).

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Fig 2. Mean flow volumes at three locations in the descending aorta of coarctation patients (squares) and control patients (triangles): proximal, at the coarctation or juxtaductal site; distal, at the diaphragm; and midpoint, halfway between proximal and distal sites.
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Table 3. Mean and Percent Change in Flow Volume Between Various Locations Along the Descending Aorta, From the Coarctation or Juxtaductal Site (Proximal) to the Diaphragm (Distal)
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Flow volumes between the groups at each location along the aorta were examined. The coarctation group volume was lower than the controls by 1,377 cc/min (95% CI: 668 to 2,085), or 54%, at the proximal coarctation site (p = 0.0003). Although average patient volumes were lower than controls at the midpoint by 410 cc/min (95% CI: 389 to 1,209) and at the distal site by 389 cc/min, (95% CI: 225 to 1,004), these differences were not statistically significant (p = 0.31, p = 0.21, respectively).
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Comment
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In this study of coarctation patients, flow volumes increased by 59% (p = 0.0002) from coarctation to diaphragm, primarily in the upper thorax, by 77% (p < 0.0001). In controls, flow volumes decreased by 11% along the entire aortic study length. Although volumes were half those of controls proximally, by the midthorax, flow volumes approached normal. Collateral vessels increase aortic flow by the midthoracic region, thereby allowing adequate perfusion to critical vascular beds. These findings may impact the type of preoperative imaging done to assess collateral circulation and associated surgical risk factors.
The focus of this study was on coarctation patients without associated anomalies, to minimize confounding factors. Although 6 patients had bicuspid aortic valves, no patients had velocity gradients greater than 1.04 m/s; hence, these anomalies were hemodynamically insignificant.
Although surgical correction of aortic coarctation is a standard, well-tolerated procedure, ischemic-related neurologic injury is still a rare complication. No neurologic sequelae occurred in patients included in the present study. Several authors have recommended methods to decrease risk of spinal cord ischemia, such as decreased cross-clamp time, hypothermic circulatory arrest, and preserving collaterals [6, 8]. Coarctation repair often requires mobilization of portions of the aorta just distal to the anatomic narrowing. Our data demonstrate that majority of collateral vessels are found in this region. Some authors theorize that ligation of intercostals collaterals cannot injure the spinal cord, because flow is retrograde and does not supplying the cord [9]. Most surgeons actually prefer to preserve collaterals, which may be providing vital blood supply, and may involute postoperatively. In a more radical approach, some have minimized complications with temporary jump grafts, bypassing the coarctation in patients with low distal perfusion pressure or with evidence of poor collateralization by MRI [8, 10]. Thus, preoperative knowledge of high-risk patients, those with poor collateralization, may aid in surgical planning.
One preoperative noninvasive method of estimating hemodynamic significance of coarctation is with arm-leg blood pressure gradients. However, measured gradients have no statistical relation to percent stenosis or presence of collaterals in patients with residual coarctation, as measured by MRI [4]. Similarly, we have found that blood pressure gradients, measured near the time of MRI, did not correlate with degree of collateralization in subjects with native coarctation. The lack of correlation between cuff gradients and collateral flow as measured by MRI is particularly germane given that some surgeons may base their surgical approach on the reported cuff gradient. Araoz and colleagues [4] found significant correlation between percent stenosis and collateral visualization by MRI. Hence, MRI is a more accurate tool for assessing hemodynamic effects of coarctation than blood pressure gradients.
Collateral vessels are difficult to assess anatomically by conventional methods such as transthoracic Doppler echocardiography, but flow can be evaluated by VENC-MRI [14, 15, 1921]. Several studies using VENC-MRI reported coarctation flow increased distally [4, 16, 22]. Steffens and colleagues [22] found total aortic flow increased by 83% from coarctation to the diaphragm in patients with moderate to severe coarctation, compared with 7% decrease in normal subjects. Similarly, in Holmqvist and coworkers [16], flow increased near the coarctation in proportion to degree of collateral circulation. In surgically created animal models of coarctation, volume percent change increased rapidly along the descending aorta, owing to collateral vessel development [18]. Furthermore, VENC-MRI has been used for serial follow-up of subjects with thoracic aorta abnormalities [23].
The current study supports the previous findings of an increase in flow volumes due to collateral blood vessel contribution. More importantly, we localized the region of maximum increase to the upper thorax. Flow volumes increase in coarctation patients presumably due to reverse flow from collaterals. As evidenced by the significant upper thoracic flow increase, the majority of collaterals have already contributed to aortic flow volume by the midthoracic level. There is significant volume difference between subject groups at the proximal site, but insignificant difference at the midpoint and distal locations. Whether from flow increase due to collaterals in coarctation patients, or volume decrease due to natural run-off in controls, both study groups have similar flow volumes in the lower thorax.
Thus, arteries arising from middle and lower thoracic levels, such as those contributing to the sparsely supplied middle division of the anterior spinal artery, may have nearly normal flow if collaterals are present. That may be why patients with collaterals undergoing primary coarctation repair have lower incidence of neurologic complications [6].
Limitations
Several limitations exist in this retrospective study. First, measurements from MRI have several potentials for error. Slice thickness and orthogonal image planes cause variability in area measurement [24]. Nevertheless, correlation of diameter measurements to invasive measurements is similar for MRI and angiography [12, 24]. Magnetic resonance imaging velocity and flow volume measurements have a reported inaccuracy of 5% to 10% for large vessels, and they may be higher for smaller vessels owing to complex flow [16]. As no patient in this study had small aortic diameter, such as may be encountered in a newborn, the lower limit of applicability of VENC-MRI is not known.
Furthermore, there is discrepancy between velocity (and calculated pressure gradients) and coarctation severity, possibly due to inherent error in MRI sampling due to angles of flow vectors. Other studies have used MRI to visualize complex, helical flow patterns in the thoracic aorta with regional turbulence and vortices [17, 25]. We have previously noted that vortices distal to the coarctation site may become laminar after a length equivalent to four aortic diameters downstream [26]. Aliasing and turbulence near the coarctation may cause underestimation of velocity changes and pressure gradients [17, 27]. In this study, we attempted to minimize error in velocity and flow volumes by analyzing flow at a midpoint level in the aorta.
Pressure gradients are also influenced by the coarctation stenosis. In the simplified Bernoulli equation, (
P = 4v
max
2), the loss-coefficient is 4; however, a loss-coefficient based on severity of stenosis could improves estimated pressure gradients [26].
Another limitation of this study is that controls were not truly normal, but were repaired tetralogy of Fallot patients. Although the aortic anatomy was assumed normal, the controls may have abnormal compliance of their overall vasculature.
Finally, although VENC-MRI offers an opportunity for surgical planning, the retrospective design of this study prevented exploration of how this data would specifically alter surgical strategy, and no formal outcome study has been performed.
In conclusion, VENC-MRI is an accurate method to detect early collateral flow [16], but can be time consuming and unnecessary for some patients. We suggest using VENC-MRI for certain preoperative patients: those who either have uncertain stenosis severity or in whom no collaterals are seen by other methods. Blood pressure gradients are not good indicators of stenosis or collateralization, and Doppler echocardiography also has limitations. If anatomy or hemodynamics are in question, further testing by VENC-MRI may be warranted. If by VENC-MRI, collaterals are seen preoperatively, then the vascular distribution of the anterior spinal cord may be adequately supplied. If, however, there is poor collateralization, and risk of poor perfusion to the vital middle and lower thoracic regions, surgeons may take protective measures during coarctation repair. Knowledge of regional flow increase due to collateral blood vessels may aid surgical planning and decrease neurologic complications of coarctation repair.
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Acknowledgments
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The authors would like to thank Pei-Hsiu Huang, MD, for his assistance in data collection.
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