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Ann Thorac Surg 2001;71:889-898
© 2001 The Society of Thoracic Surgeons
a The Childrens Heart Center, Atlanta, Georgia, USA
b Department of Cardiothoracic Surgery at Emory University School of Medicine, Atlanta, Georgia, USA
c School of Biomedical Engineering, Georgia Institute of Technology, Atlanta, Georgia, USA
d Department of Chemical Engineering, Cleveland State University, Cleveland, Ohio, USA
Accepted for publication August 25, 2000.
Address reprint requests to Dr Sharma, The Childrens Heart Center, 52 Executive Park S, Atlanta, Georgia 30329
e-mail: sharmas{at}kidsheart.com
| Abstract |
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Methods. Twelve patients with TCPC underwent sedated three-dimensional, multislice magnetic resonance phase contrast imaging. Seven patients had intraatrial lateral tunnel TCPC and 5 had extracardiac TCPC.
Results. In all patients in both groups a disordered flow pattern was observed in the inferior caval portion of the TCPC. Flow at the TCPC site appeared to be determined by connection geometry, being streamlined at the superior vena cavapulmonary junction when the superior vena cava was offset and flared toward the left pulmonary artery. Without caval offset, intense swirling and dominance of superior vena caval flow was observed. In TCPC with bilateral superior vena cavae, the flow patterns observed included secondary vortices, a central stagnation point, and influx of the superior vena cava flow into the inferior caval conduit. A comparative analysis of in vivo flow and our previous in vitro flow data from glass model prototypes of TCPC demonstrated significant similarities in flow disturbances. Three-dimensional magnetic resonance phase contrast imaging in multiple coronal planes enabled a comprehensive semiquantitative flow analysis. The data are presented in traditional instantaneous images and in animated format for interactive display of the flow dynamics.
Conclusions. Flow in the inferior caval portion of the TCPC is disordered, and the TCPC geometry determines flow characteristics.
| Introduction |
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In our in vitro experiments we studied three different designs of the TCPC with quantitative assessment of energy losses and correlated the losses with flow visualization [7, 10, 11]. This gave information regarding connections that would conserve energy and those that were particularly detrimental in this regard. On the basis of this information, we modified our TCPC design. Currently, at our institution, two types of TCPC are performed by us: A lateral intraatrial tunnel and an extracardiac conduit.
The flow characteristics within the TCPC are time varying and likely to be spatially complex. Magnetic resonance phase contrast imaging has become established as the only method available for providing time-dependent velocity mapping of flow, which gives both direction and magnitude of flow. It is unique in its ability to acquire three-dimensional velocity encoding. When such acquisition is done in multiple slices in the coronal planes through the TCPC, a reasonably complete representation of flow characteristics is obtained.
The purpose of this study was to define the in vivo flow characteristics of the above mentioned two types of TCPC by magnetic resonance phase contrast imaging and compare the results with our previous in vitro flow analysis for possible further energy conserving refinements of TCPC design.
| Material and methods |
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The patients were operated on by surgeons KRK and VKHT and all patients had undergone a previous bidirectional Glenn anastomosis. Table 1 describes the basic diagnosis of patients studied, the age at time of scan, elapsed time between operation and scan, the type of conduit used, and the status of the fenestration. Two patients with bilateral superior vena cavae (SVC) underwent bilateral Glenn anastomoses. All patients operated on by KRK underwent Intraatrial lateral TCPC and the patients operated on by VKHT underwent an extracardiac TCPC and these conduits will be referred to as inferior caval conduits (ICC). The median time elapsed between date of operation and date of scan was 13 months (Table 1). All patients in the study group had undergone echocardiography within 6 months of the scan and the status of the fenestrations in the inferior caval conduit was determined by the echocardiogram.
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Once slice locations were determined, velocity data were acquired using a cine PC gradient-echo pulse sequence. Three to five contiguous coronal slices with a thickness of 5 mm were acquired during this phase of the examination. Velocity was encoded in each slice along three principal directions: superiorinferior, rightleft, and anteriorposterior. Respiratory and retrospective electrocardiographic gating were used to acquire 16 phases in each axis during the cardiac cycle. This was done with a temporal resolution of 31 milliseconds, Respiratory gating was such that acquisitions were done at the nadir of respiratory excursion. Imaging data were held fixed for each acquisition; these values are summarized in Table 2. The total examination time was approximately 75 minutes. To minimize imaging artifacts associated with movement of patients during the acquisition, the patients less than 10 years of age were sedated with intravenous nembutal (4 to 6 mg/kg). The patients were continuously monitored by pulse oximetry and electrocardiogram. None of the patients demonstrated any significant arterial oxygen desaturation or any bradycardia.
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| Results |
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The 2 patients with bilateral SVCs formed a subtype of TCPC connection. These patients did not have any additional systemic or pulmonary venous anomalies to suggest heterotaxy syndrome. Both patients had an intraatrial ICC that connected between the two superior caval connections and little closer to the right SVC (Fig 4).
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Inferior caval conduit and SVC flow
Figures 2, 4, and 5are vector maps of coronal slices that demonstrate SVC and ICC flow. Figures 2 and 4 (patients 1 and 7, respectively) represent examples of the intraatrial type of TCPC and Figure 5 is an extracardiac type of TCPC (patient 11). The flow depicted is representative of flows seen in the ICC and SVC of the total patient group. Each figure has a vector scale in centimeters per second with assignment of red hues to the component of velocity directed anteriorly and blue hues to that directed posteriorly. Figure 1 shows the three sagittal views of the TCPC as obtained by slicing the coronal planes along the lines shown in the inset. We observed that the ICC flow had overall lower velocities (shorter arrow lengths) than the SVC flow. The SVC flow was observed to be smooth and streamlined in all patients. It appeared to be posteriorly directed (Fig 1). The ICC flow, as observed in Figures 1, 2, 4, and 5, was disordered in all patients. Circular swirling flow was noted in several areas. Multiple stagnation points with very small vectors were observed in random places along the pathway (arrows). Figure 5 demonstrates an area of increased velocity flow directed anteriorly in the lower portion of the ICC. It appears to originate from the region of hepatic veins. This type of flow was observed in 7 of 12 patients. In 1 patient a reversal of flow into the hepatic vein was observed in diastole for the duration of two phases.
The animation displays all 16 phases that were acquired. The high velocity flow in the lower ICC appeared to originate from the region of the hepatic veins and was observed to be phasic, present in the mid-phases corresponding with late systole and early diastole. This is best seen in the animation of Figure 5. The animation of Figure 4 also shows a similar area of increased velocity directed anteriorly. However, it appears more complex as it appears to originate from a circular swirl. The stagnation points in the patients did not appear to have any fixed spatial or temporal relationship. Details of circular swirling can be observed. We were unable to localize the fenestration in patients in whom we believed it to be open by echocardiography. In all patients the disordered flow appeared to be present throughout the conduit and was not more pronounced near the walls. In Figure 5 a waist is noted at the midconduit level corresponding to the waist noted from the magnitude image (Fig 3B). Flow upstream from this region appears more uniform, albeit in later phases; it is also disordered. However, flow downstream from this junction appears more disordered.
Flow at connection site
No offset
In 1 patient, with no offset (Fig 2 and Fig 6), there was a direct collision of caval flow with intense interaction. At the site of collision, however, a linear region of low velocity flow was noted. This is referred to as the line of stagnation and is better depicted in the Figure 2 animation. The dominance of SVC velocity was evident by a stagnation line that was closer to the ICC end (arrow). Adjacent to the collision site an anteriorposterior/inferiorsuperior swirl was observed and was best seen in the sagittal view (Fig 1). At this site, the flow from the SVC was first directed posteriorly and then it curved around to turn inferior and then anteriorly. This pattern was noted throughout the length of the connection site and gave rise to a helical flow pattern.
In the animation (Fig 2 animation) the dominance of SVC flow is fully appreciated with the line of stagnation displaced more inferiorly. The nature of the intense caval interaction was better defined. The circular flow pattern can now be fully observed with a rotational axis that lies predominantly in the anteriorposterior and superiorinferior planes. This feature is easier to see in the orthogonal plane to Figure 2, which is represented in Figure 1 animation.
With offset
Figure 5 is a representative case of caval offset at the connection and shows the SVC offset and flared preferentially toward the left PA and the extracardiac ICC brought to the right of this junction. Streamlined flow with unidirectionality of arrows was noted toward the left PA from the SVC in all 5 patients. In 3 patients, flow from the right side of the SVC turned toward the right PA to set up a swirling secondary flow in the region of offset between the two caval flows. From this swirling, mixing of caval flows was evident. The patients with intraatrial type of TCPC (patients 4, 6, 8, 9) who had their intraatrial ICC brought to the left of the SVC connection site and flared open, demonstrated relatively smooth flow at connection site, albeit with secondary circular swirls.
Figure 5 animation demonstrates that the swirling vortex at the offset junction appears to have a predominant rightleft and superiorinferior rotational axis. In this animation a smaller swirl is noted in the inferior portion of the PA opposite the SVC connection. This swirl possibly occupies the site of the main PA stump and appears to cushion the SVC flow that splits toward the right PA.
Bilateral SVC
Figure 4 is a vector map that demonstrates the TCPC with bilateral SVC. In this instantaneous phase, the dominant SVC flow is noted to influx into the ICC. An area of circular swirling is observed at the proximal left PA just lateral to the left SVC. The ICC appears dilated and disordered flow is observed in it.
In the patients with bilateral SVC, the animation alone gave a full appreciation of the rhythmic alternation of flows to the PAs from the two SVCs and the ICC, each of which lasts about three phases (Fig 4 animation). The central stagnation is observed only in early phases. Secondary circular swirling lateral to the left PA is observed to be phasic. There is clear demonstration of ICC flow split to both PAs with the appearance of a more dominant flow toward the left PA as compared to the split toward the right PA.
Branch PA flow
Figure 7 shows the proximal branch PAs, which were located in the posterior slice of our patients. Left PA flow appeared to be streamlined in all 5 patients in whom the SVC was flared toward the left PA (Fig 5). Localized swirling flows were noted in both branch PAs in patients with bilateral SVCs (Fig 4). The biphasic nature of flow in the PA branches was readily seen in the animation where flow was observed to slow considerably in the midportion of the phases. During the phase of slowing a helical pattern of swirling was observed.
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| Comment |
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To date, a comprehensive analysis of the flow characteristics in different designs of TCPC has not been made. Magnetic resonance phase contrast imaging-derived flow visualization offers interactive and intuitive appreciation of flow characteristics and lends itself to comparison with in vitro flow visualization. We observed flow characteristics that have not been described thus far.
Inferior caval conduit flow
Surprisingly, we found a significantly disordered flow pattern in the ICC of all our patients. This flow pattern appeared to be independent of type of connection, presence or absence of fenestration, or type of graft material used. Our findings differ from Fogel and colleagues [14] who, using bolus tagging magnetic resonance imaging methods, found no evidence of disordered flow anywhere in the systemic venous pathway. However, they did note the highest velocity as well as the maximum variation in velocity at the midbaffle level of the inferior caval pathway and speculated several causes for this variation in flow velocity, including the effects of motion of nearby cardiac structures, the effects of respiration, and the effects of synthetic material. Although we agree with these speculations, other possibilities exist. Larado and associates [15] have studied the effect of inferior vena cava to extracardiac conduit diameter ratio in their in vitro TCPC animal model. They measured 13% higher energy dissipation in the models with conduit diameter 1.5 inferior vena cava than compared to 1.0 IVC and attributed this to flow expansion effects that cause flow separation and loss of streamlined flow. Our observations of disordered ICC flow could be partially explained by the same phenomenon as some of our patients demonstrated that the ICC was larger than the IVC. However, this was not systematically studied by us as it was not anticipated at the time of scan acquisition. Nevertheless, our study does support the following additional speculations of disordered ICC flow.
Irrespective of the cause, we believe the disordered flow in ICC is likely to cause significant energy loss and needs further elucidation, including a detailed flow analysis of the hepatic veinIVC conduit junction.
Relationship of connection geometry and flow
A number of different caval connections were studied and a significant relationship emerged between the geometry of connection and flow. When the cavae were not offset from each other, intense caval flow interaction was observed. In this interaction the dominant flow was from the SVC. This is a consequence of the smaller size of the SVC compared to the ICC. Although, the ICC contributes about 60% of the flow to the connection [3], its larger size reduces the velocity required to deliver this flow and hence there is a lower kinetic energy per unit mass of blood in it than is in the SVC. When the SVC was flared preferentially toward the left PA and ICC toward the right PA the interaction was less, although secondary swirls were noted. When the opposite type of flaring and offset was done as in the intraatrial type of TCPC, again the flow interaction was less. When the SVC was flared in a manner that directed flow toward the ICC, influx of SVC flow into the ICC resulted in disordered flow. These observations underscore the importance of connection geometry in conserving energy as is borne out by our in vitro studies of similar connection geometry [11].
Branch pulmonary artery flow
The branch PAs by virtue of lying in different planes were difficult to image completely. However, the proximal branches were visible and demonstrated secondary swirls that were most likely generated from the connection site. Helical flow patterns noted in our in vitro study could not be observed in vivo in the branch PAs. However, at the connection site of the zero offset patient such helical patterns were observed and we believe that these would be present at least to some extent in the branches, as the genesis of helical flow patterns is the caval interaction of flow. Morgan and colleagues [17] have described circular swirling patterns in the branch PAs of their TCPC patients. Their analysis was performed in the cross-sectional plane of the branch PAs and perhaps it is a more sensitive method for analyzing branch PA flow. Branch PA flow observed in our study was biphasic and agrees with other studies in this regard [18, 19].
Comparative analysis of in vivo and in vitro flow patterns
The range of in vitro glass models studied by us included designs that resembled the geometry of TCPC that are done at our institution and thus the in vivo and in vitro flow dynamics could be compared. This was also enabled by our ability to visualize flow by both methods (Fig 8).
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When the cavae were not offset but flared, there was intense caval flow interaction producing a circular anteriorposterior swirl that extended toward the PAs. This was more noticeable in the sagittal views (Fig 1). Similar circular swirls were noted in the geometry matched in vitro model. Morgan and colleagues [17], who described similar circular swirls in cross-sectional views of the PA, calculated high circumferential shear stresses due to this swirling motion and speculated the effects of this on the cell lining. Although our study did not measure shear stresses, our in vitro data quantified high-energy losses in the "zero" offset TCPC design. From hemodynamic principles, we know that large shearing stresses lead to energy losses and thus from our data it can be inferred that energy losses are likely to be significant in the TCPC without offset.
Animation
The in vivo flow data in our study is presented as semiquantitative with resolution of three-dimensional velocity vector in multiple slices. This gives time-dependent, directional, and magnitude information about flow along the plane of the connection. We believe a descriptive account with or without the aid of instantaneous images of an inherently dynamic process falls far short of an accurate portrayal of flow. Moreover, in many of our patients flow disturbances were of a different nature in different cardiac phases and hence, no single instantaneous frame or series of frames would be representative of the complete flow characteristics. An animated display of such a dataset gives better understanding of flow characteristics to the viewer. Furthermore, data can be interactively viewed either in a loop format with speed controls or frame by frame advancement as determined by the viewer. Thus, an intuitive sense for the flow disturbances can be derived that is not achievable by any other means. We believe that our animated presentation of representative flow disturbances is a useful and currently unique method of sharing complex fluid dynamic information.
Clinical implications
Ideally, for designing the optimal geometry of TCPC for conserving energy losses, direct in vivo assessment of pressure measurement and its correlation with energy losses should be done. However, because no method enables this, indirect means of assessing flow energetics are used. Our in vitro study used glass phantoms in which both pressure measurements and flow visualization were performed. The study patients yielded in vivo semiquantitative flow visualization. With comparative analysis of these methods, and keeping in mind anatomic space constraints, some cautious clinical implications can be made.
First, our and other studies [13] have shown the advantages of caval offsetting and, we believe, that within any given anatomic space constraints, offsetting should be incorporated as the first step in all TCPC designs. Whether the SVC should be offset more toward the left PA as in the extracardiac TCPC group or toward the right PA as in our intraatrial TCPC group, has not been determined by this study.
Second, if space permits, the TCPC should be flared open in all directions. If this is not possible due to space constraints then flaring should be done in such a fashion that the caval flows are not directed toward each other (Fig 9A). Thus, when the SVC is offset toward the left PA, the predominant flare should also be toward the left PA (Fig 9C).
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Limitations
The nature of flow in the TCPC is complex and has cardiac and respiratory factors that influence it, as pointed out by Fogel and colleagues [14]. In our study, the impact of respiration on flow dynamics was not studied and is a limitation as the effects can be significant. Instead, in our study each phase was acquired at the nadir of respiratory cycle thus minimizing its effect. At this time our study is limited to a semiquantitative analysis of flow within the TCPC. From our acquired data a quantitative calculation of energy loss is possible. However, the quantitative methods need validation and we are in the process of establishing that validation. The complexity of flow disturbances in the TCPC may not be fully characterized by studying the flow only along coronal planes and in this regard our study is somewhat limited. Time constraints on the magnet prevented us from acquiring data in the axial planes along the TCPC pathway of our patients. Such an acquisition would have been useful for also confirming the flow disturbances noted in the coronal planes.
In conclusion, from this study we found that there is disordered flow in the inferior caval conduit of all our patients with TCPC. The flow dynamics at the cavopulmonary connection appear to be geometry dependent. Geometries that include caval offset and appropriate flaring appear to have favorable flow dynamics both in vivo and in vitro.
| Acknowledgments |
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| Footnotes |
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In addition, a video clip of this procedure can be viewed on the Internet at: http://www.sts.org/section/atsvideo/
| References |
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