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Pulmonary Blood Flow Patterns in Patients With Fontan Circulation
CARDIOVASCULAR
Pulmonary Blood Flow Patterns in Patients With Fontan Circulation Alfred Hager, MD, Sohrab Fratz, MD, Markus Schwaiger, MD, Rüdiger Lange, MD, John Hess, MD, and Heiko Stern, MD Departments of Pediatric Cardiology and Congenital Heart Disease, and Cardiovascular Surgery, German Heart Center, Munich, Technical University of Munich, and Department of Nuclear Medicine, Technical University of Munich, Munich, Germany
Background. After Fontan surgery there is no subpulmonary ventricle to modify pulmonary blood flow. The influence of the cardiac cycle on pulmonary blood flow patterns in various types of Fontan patients is unknown. Methods. Blood flow patterns were investigated using phase-velocity cine magnetic resonance imaging in the pulmonary artery of 17 patients (21.1 ⴞ 7.3 years old, 6 females) with Fontan circulation. These patterns were compared with those of 12 healthy volunteers (26.3 ⴞ 6.0 years old, 10 females) obtained in the superior vena cava and the main pulmonary artery. Measurements were sampled for a period of about 3 minutes to rule out respiratory effects. Blood flow patterns were depicted by interpolating the variable number of measured phases in every patient to 100 phases and normalizing flow to mean blood flow in that vessel. Then, average flow patterns
were calculated throughout the patient groups to depict a typical pattern. Results. In Fontan patients, peaks and troughs are highly variable. In averaged flow patterns for the whole Fontan group, only a slight late diastolic flow acceleration could be detected. This is in contrast to the pattern of the control subjects in whom typical systolic peaks and late diastolic troughs could be found in both the superior vena cava and in the pulmonary artery. Conclusions. There are no typical pulmonary blood flow patterns of cardiac origin in patients with Fontan circulation, except for slight late diastolic flow acceleration representing diastolic inflow restriction.
I
the influence of different surgical Fontan modifications and that of atrioventricular regurgitation on pulmonary blood flow patterns were depicted.
n 1971 Fontan and Baudet [1] reported on a palliative operation in patients with tricuspid atresia. The new idea was to direct venous blood flow into the pulmonary arteries without a pumping chamber in between. Initially it was thought that the right atrium was needed as a pumping chamber for pulmonary perfusion. The present modification, a total cavopulmonary connection [2, 3] with an extracardiac conduit or lateral intraatrial tunnel from the inferior vena cava to the right pulmonary artery, clearly shows that no kind of pumping structure proximal to the pulmonary vessels is necessary to establish pulmonary blood flow. A slightly elevated central venous pressure and a suction pump distal to the pulmonary vascular bed are thought to be the hemodynamic driving force of pulmonary blood flow. The aim of this study was to assess pulmonary blood flow patterns by phase-velocity cine magnetic resonance imaging (MRI) and to investigate the influence of the cardiac cycle on these patterns. These were compared with patterns obtained in the superior vena cava and pulmonary artery of healthy volunteers. Furthermore,
Accepted for publication July 10, 2007. Address correspondence to Dr Hager, Department of Pediatric Cardiology and Congenital Heart Disease, Deutsches Herzzentrum München, Technische Universität München, Lazarettstr 36, München, D-80636, Germany; e-mail: [email protected].
© 2008 by The Society of Thoracic Surgeons Published by Elsevier Inc
(Ann Thorac Surg 2008;85:186 –91) © 2008 by The Society of Thoracic Surgeons
Patients and Methods Patients Seventeen patients with Fontan circulation who underwent an MRI for clinical reasons were analyzed. Patients without stable atrial rhythm were excluded. Multiple different diagnoses led to the Fontan-like palliation in these patients: tricuspid atresia in 7 patients; double-inlet left ventricle in 7 patients; heterotaxy syndrome with atrioventricular discordance, double-outlet right ventricle, and pulmonary stenosis in 2 patients; and mitral valve atresia with ventricular septal defect in 1 patient. Demographic and clinical data are presented in Table 1. Surgical techniques consisted of a right atrial to right infundibular connection (AVC) [4], a right atrial to pulmonary arterial connection (APC) [5], and a lateral tunnel total cavopulmonary connection (TCPC) [3]. Only patients with a TCPC had a prior bidirectional Glenn anastomosis. None of the patients had fenestrations or other substantial shunts on atrial or ventricular level. None of the patients had substantial stenoses. Grading of the systemic atrioventricular valve regurgitation according to the American Society of Echocardiography [6] was extracted from the echocardiography reports of the last 0003-4975/08/$34.00 doi:10.1016/j.athoracsur.2007.07.029
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Table 1. Demographic and Clinical Data Variable Number Sex (M/F) Diagnoses Tricuspid atresia Double-inlet left ventricle Heterotaxy Mitral valve atresia, VSD Age at surgery (y) Years after surgery Age at MRI (y, mean ⫾ SD) (range) Atrioventricular valve regurgitation (number of patients with grade 0/1/2/3/4)
AVC
APC
TCPC
Control Subjects
3 2/1
9 4/5
5 4/1
12 2/10
3
4 3 2
4
9.0 ⫾ 7.5 15.5 ⫾ 4.3 24.5 ⫾ 11.8 (11–35) 1/1/1/0/0
8.5 ⫾ 5.3 14.3 ⫾ 1.2 22.8 ⫾ 5.1 (16–32) 3/3/2/1/0
1 7.7 ⫾ 7.4 8.4 ⫾ 2.7 16.1 ⫾ 7.0 (11–28) 3/2/0/0/0
APC ⫽ atriopulmonary connection; AVC ⫽ atrioventricular connection; MRI ⫽ magnetic resonance imaging; TCPC ⫽ (lateral tunnel) total cavopulmonary connection; VSD ⫽ ventricular septal defect.
visit in our outpatient department. Twelve healthy volunteers served as a control group. The study was approved by the local ethical board. All patients and control subjects gave informed consent that their data would be published anonymously. Preliminary data of the study were presented as abstract and presentation at the 24th Congress of the European Society of Cardiology in Vienna, Austria [7] and at the 38th Annual Meeting of the Association for European Pediatric Cardiology in Amsterdam, The Netherlands [8].
Magnetic Resonance Imaging The cine MRI was performed using a 1.5-T scanner (Philips ACS-NT, Koninklijke Philips Electronics N.V., Eindhoven, The Netherlands). A conventional phasesensitive gradient echo sequence was used in a doubleoblique plane perpendicular to the dominant flow direction in the vessel. The following acquisition variables were used: repetition time 14 ms, echo time 6 to 7 ms, slice thickness 6 mm, flip angle 30 degrees, receiver bandwidth 31.25 kHz, rectangular field of view 240 to 350 mm, matrix 256 ⫻ 256, number of excitations 2. The highest flow velocity estimated to be encoded was selected by the operator before each acquisition to avoid aliasing. It ranged from 0.7 to 2.0 m/s. Respiratory and flow compensation was used in subjects to minimize ghosting artifacts. Data were sampled for a period of about 3 minutes to rule out any respiratory effects. Data were reconstructed with retrospective electrocardiographic gating to provide 19 to 33 magnitude (anatomic) and velocity-encoded images per cardiac cycle. Blood flow velocity curves were measured in the left and right pulmonary arteries of the patients. The measurements of the left pulmonary artery were used for further analysis because of better depiction, especially in the TCPC group with their short distance from the cavopulmonary anastomosis to the origin of the right upper lobe artery. The right pulmonary artery was used only in 2 patients (1 with APC and 1 with TCPC) because of limited image quality in the left pulmonary artery.
26.3 ⫾ 6.0 (17–39)
SD ⫽ standard deviation;
In the control group, velocities were measured in the superior vena cava and the main pulmonary artery. Data analysis was performed off-line using commercially available software (MRI-Flow, Medis Medical Imaging Systems bv, Leiden, The Netherlands). Mean flow velocity across the entire cross section of the vessel was calculated for each of the reconstructed 19 to 33 phases.
Depiction of Blood Flow Patterns First, flow measurements were linearly interpolated from the variable number of 19 to 33 phases for every cardiac cycle to 100 phases in each patient. Therefore, each new phase represented 1% of the cardiac cycle length. Second, flow values at every single phase were normalized to the total flow in the whole cardiac cycle of that vessel. After these two steps the calculated values expressed the percentage of total blood flow that constituted that single phase. Finally, these values, interpolated to 100 phases and normalized to total flow, were averaged for several vessels and patient groups to outline typical peaks and troughs in that specific vessel for that specific patient group.
Results Fontan patients showed highly variable flow patterns in the pulmonary artery (Fig 1A). After averaging for the whole Fontan group, no typical peaks and troughs could be found except a slight flow acceleration at late diastole (Fig 2). Averaged pulmonary blood flow patterns resembled neither that in the superior vena cava of healthy volunteers, showing a clear systolic flow peak decelerating into early diastole (the diastolic peaks are also highly variable and disappeared after averaging), nor that in the normal pulmonary artery, with flow almost confined to a single systolic peak (Fig 2). Comparing Fontan subgroups, this late diastolic flow acceleration is only minimally enhanced in patients with AVC and APC compared with patients with TCPC (Fig 3).
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Fig 1. Comparison of blood flow patterns. The x-axis shows the phase of the cardiac cycle from phase 1 as the start of the systole to phase 100 (⫽ 0) as the end of diastole. The y-axis shows the flow normalized to the mean blood flow in that vessel, with 0 and 1 representing no and mean blood flows, respectively. The bar at the bottom outlines the period of systole estimated from the mean heart rate. (A) Pulmonary artery of 17 patients after Fontan surgery. (B) Superior vena cava of 12 healthy control subjects. (C) Pulmonary artery of 12 healthy control subjects.
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Fig 2. Averaged blood flow pattern, outlining the typical peaks and troughs, in the pulmonary artery of 17 patients after Fontan surgery (heavy solid line), compared with that in the superior vena cava (⫻) and in the pulmonary artery (Œ) of 12 healthy control subjects. The x-axis shows the phase of the cardiac cycle and the y-axis shows the normalized flow. The pulmonary artery of Fontan patients showed no typical patterns, except for a slight late diastolic peak, the superior vena cava of the control subjects showed a clear systolic flow peak decelerating into early diastole, and the pulmonary artery of control subjects showed flow almost confined to a single systolic peak.
Furthermore, there was also only a trivial enhancement of this diastolic flow acceleration in patients with no or trivial atrioventricular valve regurgitation (grade 0 and 1) compared with those with mild or moderate regurgitation (grade 2 and 3). None of our patients had severe regurgitation (grade 4). Comparative patterns are depicted in Figure 4.
Comment We reported averaged pulmonary blood flow patterns of patients with the Fontan circulation. With this method, we sought to outline peaks and troughs that are typical for that specific type of circulation after exclusion of respiratory effects. In the Fontan circulation almost none of them were present, except for a slight late diastolic flow acceleration. This acceleration is slightly enhanced in patients with the APC and AVC Fontan modifications and in patients with no or minimal atrioventricular valve regurgitation. Many Doppler and MRI studies showed that there is some pulsation in the pulmonary blood flow of Fontan
patients. Some authors described a biphasic pattern [9], some a monophasic pattern [10]. However, the timing of the peaks and troughs were not consistent. In our study with averaged blood flow patterns, this variability in presence and timing eliminated all peaks and troughs seen in the individual pattern. Therefore, a typical pulmonary blood flow pattern for the Fontan circulation could not be delineated. Second, our algorithm to normalize measured flows to flow patterns allowed us to calculate group patterns and to compare them directly. We found that patients after different types of Fontan operations showed almost the same flow patterns. The impact of the atrial contraction was rather small. Two MRI studies [9, 11] and many Doppler studies [12–15] identified the lack of pulsation and postulated the importance of respiration in that type of circulation in lateral tunnel TCPC, as it was the idea of this modification to achieve laminar flow inside the connection by accepting the loss of pulsation caused by atrial or infundibular contractions [2]. On the other hand in APC, a Doppler study had determined the importance of atrial contraction [16]. We found only minor differFig 3. Blood flow patterns in the pulmonary artery of 17 patients with various modifications of Fontan surgery. The x-axis shows the phase of the cardiac cycle and the y-axis the normalized flow. There was no significant difference in the patterns between the 3 patients with atrioventricular connection (‚), the 9 patients with atriopulmonary connection (Œ), and the 5 patients with total cavopulmonary connection (⫻).
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Fig 4. Blood flow patterns in the pulmonary artery of 17 patients after Fontan surgery with various degrees of atrioventricular valve regurgitation. The x-axis shows the phase of the cardiac cycle and the y-axis the normalized flow. There was no significant difference in the patterns between the 13 patients with trivial or no atrioventricular valve regurgitation () compared with the 4 patients with mild or moderate regurgitation (⫻).
ences among these groups, even in the AVC group in which at least some systolic flow from a ventricular contraction was expected. This might be attributable to a longer follow-up after surgery in our patients, especially in the AVC and APC groups. Dilatation and scarring of the atrial myocardium and calcification of the patch material might have contributed to the almost absent flow propagation owing to atrial contraction. Furthermore, methodological issues might have hampered the Doppler studies. Movements of the vessel in relation to the sample probe cannot be avoided in Doppler studies. The Doppler method measures peak velocities dependent on a small area inside the vessel, chosen by the investigator. This sample area can easily be shifted by cardiac movements directly transmitted to the investigated vessels. Postprocessing in cine MRI ensures that flow is integrated from velocities over the whole cross section of the vessel even if the vessel is moving. Finally, we want to speculate about the end-diastolic flow augmentation. If we had measured these patterns in the pulmonary veins, we would have diagnosed an atrial filling restriction as the diastolic peak exceeded the systolic peak [17]. However, it has to be assumed that this effect is transmitted to the pulmonary artery in the Fontan circulation with passive pulmonary blood flow only enhanced by a suctioning systemic ventricle. Ventricular filling restriction because of the lack of preload was also described in a recent tissue Doppler study [18]. The authors reported that this restrictive filling pattern is the normal pattern in Fontan patients with preserved ventricular function. The same group published a case report [19] of a patient with tricuspid atresia after TCPC and severe mitral regurgitation showing a (pseudo) normal diastolic function that switched to the restrictive pattern after mitral valve repair. This is also in accordance with our finding that patients with more than trivial atrioventricular regurgitation showed a lesspronounced end-diastolic flow acceleration (Fig 4). This regurgitation volume caused an early filling of the ven-
tricle in diastole and impaired the hemodynamically important suctioning mechanism. It is even more speculative to find an explanation of why patients with TCPC have less flow acceleration at the end of diastole than APC or AVC patients (Fig 3). Maybe in these patients the systemic ventricle has a reservoir (right atrium with or without a right infundibulum) to suction from in front of the pulmonary vascular bed, whereas the ventricle in TCPC patients has to suction from the systemic veins directly (enhancing systemic blood flow). Thus, TCPC, if necessary combined with an atrioventricular valve repair, should be the preferred surgical approach to the Fontan circulation to get an optimal smooth flow in the whole cardiac cycle, at both the venous and the arterial levels.
Thanks to Alexander Gratz for proofreading the manuscript.
References 1. Fontan F, Baudet E. Surgical repair of tricuspid atresia. Thorax 1971;26:240 – 8. 2. de Leval MR, Kilner P, Gewillig M, Bull C. Total cavopulmonary connection: a logical alternative to atriopulmonary connection for complex Fontan operations. Experimental studies and early clinical experience. J Thorac Cardiovasc Surg 1988;96:682–95. 3. Puga FJ, Chiavarelli M, Hagler DJ. Modifications of the Fontan operation applicable to patients with left atrioventricular valve atresia or single atrioventricular valve. Circulation 1987;76(Suppl):III-53– 60. 4. Bjork VO, Olin CL, Bjarke BB, Thoren CA. Right atrial-right ventricular anastomosis for correction of tricuspid atresia. J Thorac Cardiovasc Surg 1979;77:452– 8. 5. Kreutzer G, Galindez E, Bono H, De Palma C, Laura JP. An operation for the correction of tricuspid atresia. J Thorac Cardiovasc Surg 1973;66:613–21. 6. Zoghbi WA, Enriquez-Sarano M, Foster E, et al. Recommendations for evaluation of the severity of native valvular regurgitation with two-dimensional and Doppler echocardiography. J Am Soc Echocardiogr 2003;16:777– 802.
7. Hager A, Fratz S, Hess J, Schwaiger M, Stern H. Pulmonary blood flow pattern in patients with Fontan circulation depicted by cine magnetic resonance imaging. In: 24th Congress of the European Society of Cardiology, Vienna/ Austria, September 2003; Eur Heart J 2003;24(Abstr Suppl September 2003):357[A]. 8. Hager A, Fratz S, Hess J, Schwaiger M, Stern H. Pulmonary blood flow pattern in patients with Fontan circulation depicted by cine MRI. In: 38th Annual Meeting of the Association for European Pediatric Cardiology, Amsterdam/NL, May 28 –31, 2003; Cardiol Young 2003;13(Suppl 1):20[A]. 9. Be’eri E, Maier SE, Landzberg MJ, Chung T, Geva T. In vivo evaluation of Fontan pathway flow dynamics by multidimensional phase-velocity magnetic resonance imaging. Circulation 1998;98:2873– 82. 10. Fogel MA, Weinberg PM, Hoydu A, et al. The nature of flow in the systemic venous pathway measured by magnetic resonance blood tagging in patients having the Fontan operation. J Thorac Cardiovasc Surg 1997;114:1032– 41. 11. Hjortdal VE, Emmertsen K, Stenbog E, et al. Effects of exercise and respiration on blood flow in total cavopulmonary connection: a real-time magnetic resonance flow study. Circulation 2003;108:1227–31. 12. Penny DJ, Hayek Z, Redington AN. The effects of positive and negative extrathoracic pressure ventilation on pulmonary blood flow after the total cavopulmonary shunt procedure. Int J Cardiol 1991;30:128 –30.
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13. Penny DJ, Redington AN. Doppler echocardiographic evaluation of pulmonary blood flow after the Fontan operation: the role of the lungs. Br Heart J 1991;66:372– 4. 14. Redington AN, Penny D, Shinebourne EA. Pulmonary blood flow after total cavopulmonary shunt. Br Heart J 1991;65: 213–7. 15. Kaulitz R, Bergman P, Luhmer I, Paul T, Hausdorf G. Instantaneous pressure-flow velocity relations of systemic venous return in patients with univentricular circulation. Heart 1999;82:294 –9. 16. Qureshi SA, Richheimer R, McKay R, Arnold R. Doppler echocardiographic evaluation of pulmonary artery flow after modified Fontan operation: importance of atrial contraction. Br Heart J 1990;64:272– 6. 17. Nishimura RA, Tajik AJ. Evaluation of diastolic filling of left ventricle in health and disease: Doppler echocardiography is the clinician’s Rosetta Stone. J Am Coll Cardiol 1997;30:8 –18. 18. Eicken A, Petzuch K, Marek J, et al. Characteristics of Doppler myocardial echocardiography in patients with tricuspid atresia after total cavopulmonary connection with preserved systolic ventricular function. Int J Cardiol 2007; 116:212– 8. 19. Petzuch K, Eicken A, Marek J, Vogel M, Schreiber C, Hess J. Tissue Doppler echocardiography before and after the surgical reconstruction of an insufficient mitral valve in a patient with Fontan circulation. Pediatr Cardiol 2006;27: 508 –10.
Notice From the American Board of Thoracic Surgery The 2008 Part I (written) examination will be held on Monday, December 1, 2008. It is planned that the examination will be given at multiple sites throughout the United States using an electronic format. The closing date for registration is August 1, 2008. Those wishing to be considered for examination must apply online at www.abts.org. To be admissible to the Part II (oral) examination, a candidate must have successfully completed the Part I (written) examination.
© 2008 by The Society of Thoracic Surgeons Published by Elsevier Inc
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Ann Thorac Surg 2008;85:191
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0003-4975/08/$34.00
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Ann Thorac Surg 2008;85:186 –91
Pulmonary Blood Flow Patterns in Patients With Fontan Circulation Alfred Hager, MD, Sohrab Fratz, MD, Markus Schwaiger, MD, Rüdiger Lange, MD, John Hess, MD, and Heiko Stern, MD Departments of Pediatric Cardiology and Congenital Heart Disease, and Cardiovascular Surgery, German Heart Center, Munich, Technical University of Munich, and Department of Nuclear Medicine, Technical University of Munich, Munich, Germany
Background. After Fontan surgery there is no subpulmonary ventricle to modify pulmonary blood flow. The influence of the cardiac cycle on pulmonary blood flow patterns in various types of Fontan patients is unknown. Methods. Blood flow patterns were investigated using phase-velocity cine magnetic resonance imaging in the pulmonary artery of 17 patients (21.1 ⴞ 7.3 years old, 6 females) with Fontan circulation. These patterns were compared with those of 12 healthy volunteers (26.3 ⴞ 6.0 years old, 10 females) obtained in the superior vena cava and the main pulmonary artery. Measurements were sampled for a period of about 3 minutes to rule out respiratory effects. Blood flow patterns were depicted by interpolating the variable number of measured phases in every patient to 100 phases and normalizing flow to mean blood flow in that vessel. Then, average flow patterns
were calculated throughout the patient groups to depict a typical pattern. Results. In Fontan patients, peaks and troughs are highly variable. In averaged flow patterns for the whole Fontan group, only a slight late diastolic flow acceleration could be detected. This is in contrast to the pattern of the control subjects in whom typical systolic peaks and late diastolic troughs could be found in both the superior vena cava and in the pulmonary artery. Conclusions. There are no typical pulmonary blood flow patterns of cardiac origin in patients with Fontan circulation, except for slight late diastolic flow acceleration representing diastolic inflow restriction.
I
the influence of different surgical Fontan modifications and that of atrioventricular regurgitation on pulmonary blood flow patterns were depicted.
n 1971 Fontan and Baudet [1] reported on a palliative operation in patients with tricuspid atresia. The new idea was to direct venous blood flow into the pulmonary arteries without a pumping chamber in between. Initially it was thought that the right atrium was needed as a pumping chamber for pulmonary perfusion. The present modification, a total cavopulmonary connection [2, 3] with an extracardiac conduit or lateral intraatrial tunnel from the inferior vena cava to the right pulmonary artery, clearly shows that no kind of pumping structure proximal to the pulmonary vessels is necessary to establish pulmonary blood flow. A slightly elevated central venous pressure and a suction pump distal to the pulmonary vascular bed are thought to be the hemodynamic driving force of pulmonary blood flow. The aim of this study was to assess pulmonary blood flow patterns by phase-velocity cine magnetic resonance imaging (MRI) and to investigate the influence of the cardiac cycle on these patterns. These were compared with patterns obtained in the superior vena cava and pulmonary artery of healthy volunteers. Furthermore,
Accepted for publication July 10, 2007. Address correspondence to Dr Hager, Department of Pediatric Cardiology and Congenital Heart Disease, Deutsches Herzzentrum München, Technische Universität München, Lazarettstr 36, München, D-80636, Germany; e-mail: [email protected].
© 2008 by The Society of Thoracic Surgeons Published by Elsevier Inc
(Ann Thorac Surg 2008;85:186 –91) © 2008 by The Society of Thoracic Surgeons
Patients and Methods Patients Seventeen patients with Fontan circulation who underwent an MRI for clinical reasons were analyzed. Patients without stable atrial rhythm were excluded. Multiple different diagnoses led to the Fontan-like palliation in these patients: tricuspid atresia in 7 patients; double-inlet left ventricle in 7 patients; heterotaxy syndrome with atrioventricular discordance, double-outlet right ventricle, and pulmonary stenosis in 2 patients; and mitral valve atresia with ventricular septal defect in 1 patient. Demographic and clinical data are presented in Table 1. Surgical techniques consisted of a right atrial to right infundibular connection (AVC) [4], a right atrial to pulmonary arterial connection (APC) [5], and a lateral tunnel total cavopulmonary connection (TCPC) [3]. Only patients with a TCPC had a prior bidirectional Glenn anastomosis. None of the patients had fenestrations or other substantial shunts on atrial or ventricular level. None of the patients had substantial stenoses. Grading of the systemic atrioventricular valve regurgitation according to the American Society of Echocardiography [6] was extracted from the echocardiography reports of the last 0003-4975/08/$34.00 doi:10.1016/j.athoracsur.2007.07.029
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Table 1. Demographic and Clinical Data Variable Number Sex (M/F) Diagnoses Tricuspid atresia Double-inlet left ventricle Heterotaxy Mitral valve atresia, VSD Age at surgery (y) Years after surgery Age at MRI (y, mean ⫾ SD) (range) Atrioventricular valve regurgitation (number of patients with grade 0/1/2/3/4)
AVC
APC
TCPC
Control Subjects
3 2/1
9 4/5
5 4/1
12 2/10
3
4 3 2
4
9.0 ⫾ 7.5 15.5 ⫾ 4.3 24.5 ⫾ 11.8 (11–35) 1/1/1/0/0
8.5 ⫾ 5.3 14.3 ⫾ 1.2 22.8 ⫾ 5.1 (16–32) 3/3/2/1/0
1 7.7 ⫾ 7.4 8.4 ⫾ 2.7 16.1 ⫾ 7.0 (11–28) 3/2/0/0/0
APC ⫽ atriopulmonary connection; AVC ⫽ atrioventricular connection; MRI ⫽ magnetic resonance imaging; TCPC ⫽ (lateral tunnel) total cavopulmonary connection; VSD ⫽ ventricular septal defect.
visit in our outpatient department. Twelve healthy volunteers served as a control group. The study was approved by the local ethical board. All patients and control subjects gave informed consent that their data would be published anonymously. Preliminary data of the study were presented as abstract and presentation at the 24th Congress of the European Society of Cardiology in Vienna, Austria [7] and at the 38th Annual Meeting of the Association for European Pediatric Cardiology in Amsterdam, The Netherlands [8].
Magnetic Resonance Imaging The cine MRI was performed using a 1.5-T scanner (Philips ACS-NT, Koninklijke Philips Electronics N.V., Eindhoven, The Netherlands). A conventional phasesensitive gradient echo sequence was used in a doubleoblique plane perpendicular to the dominant flow direction in the vessel. The following acquisition variables were used: repetition time 14 ms, echo time 6 to 7 ms, slice thickness 6 mm, flip angle 30 degrees, receiver bandwidth 31.25 kHz, rectangular field of view 240 to 350 mm, matrix 256 ⫻ 256, number of excitations 2. The highest flow velocity estimated to be encoded was selected by the operator before each acquisition to avoid aliasing. It ranged from 0.7 to 2.0 m/s. Respiratory and flow compensation was used in subjects to minimize ghosting artifacts. Data were sampled for a period of about 3 minutes to rule out any respiratory effects. Data were reconstructed with retrospective electrocardiographic gating to provide 19 to 33 magnitude (anatomic) and velocity-encoded images per cardiac cycle. Blood flow velocity curves were measured in the left and right pulmonary arteries of the patients. The measurements of the left pulmonary artery were used for further analysis because of better depiction, especially in the TCPC group with their short distance from the cavopulmonary anastomosis to the origin of the right upper lobe artery. The right pulmonary artery was used only in 2 patients (1 with APC and 1 with TCPC) because of limited image quality in the left pulmonary artery.
26.3 ⫾ 6.0 (17–39)
SD ⫽ standard deviation;
In the control group, velocities were measured in the superior vena cava and the main pulmonary artery. Data analysis was performed off-line using commercially available software (MRI-Flow, Medis Medical Imaging Systems bv, Leiden, The Netherlands). Mean flow velocity across the entire cross section of the vessel was calculated for each of the reconstructed 19 to 33 phases.
Depiction of Blood Flow Patterns First, flow measurements were linearly interpolated from the variable number of 19 to 33 phases for every cardiac cycle to 100 phases in each patient. Therefore, each new phase represented 1% of the cardiac cycle length. Second, flow values at every single phase were normalized to the total flow in the whole cardiac cycle of that vessel. After these two steps the calculated values expressed the percentage of total blood flow that constituted that single phase. Finally, these values, interpolated to 100 phases and normalized to total flow, were averaged for several vessels and patient groups to outline typical peaks and troughs in that specific vessel for that specific patient group.
Results Fontan patients showed highly variable flow patterns in the pulmonary artery (Fig 1A). After averaging for the whole Fontan group, no typical peaks and troughs could be found except a slight flow acceleration at late diastole (Fig 2). Averaged pulmonary blood flow patterns resembled neither that in the superior vena cava of healthy volunteers, showing a clear systolic flow peak decelerating into early diastole (the diastolic peaks are also highly variable and disappeared after averaging), nor that in the normal pulmonary artery, with flow almost confined to a single systolic peak (Fig 2). Comparing Fontan subgroups, this late diastolic flow acceleration is only minimally enhanced in patients with AVC and APC compared with patients with TCPC (Fig 3).
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Fig 1. Comparison of blood flow patterns. The x-axis shows the phase of the cardiac cycle from phase 1 as the start of the systole to phase 100 (⫽ 0) as the end of diastole. The y-axis shows the flow normalized to the mean blood flow in that vessel, with 0 and 1 representing no and mean blood flows, respectively. The bar at the bottom outlines the period of systole estimated from the mean heart rate. (A) Pulmonary artery of 17 patients after Fontan surgery. (B) Superior vena cava of 12 healthy control subjects. (C) Pulmonary artery of 12 healthy control subjects.
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Fig 2. Averaged blood flow pattern, outlining the typical peaks and troughs, in the pulmonary artery of 17 patients after Fontan surgery (heavy solid line), compared with that in the superior vena cava (⫻) and in the pulmonary artery (Œ) of 12 healthy control subjects. The x-axis shows the phase of the cardiac cycle and the y-axis shows the normalized flow. The pulmonary artery of Fontan patients showed no typical patterns, except for a slight late diastolic peak, the superior vena cava of the control subjects showed a clear systolic flow peak decelerating into early diastole, and the pulmonary artery of control subjects showed flow almost confined to a single systolic peak.
Furthermore, there was also only a trivial enhancement of this diastolic flow acceleration in patients with no or trivial atrioventricular valve regurgitation (grade 0 and 1) compared with those with mild or moderate regurgitation (grade 2 and 3). None of our patients had severe regurgitation (grade 4). Comparative patterns are depicted in Figure 4.
Comment We reported averaged pulmonary blood flow patterns of patients with the Fontan circulation. With this method, we sought to outline peaks and troughs that are typical for that specific type of circulation after exclusion of respiratory effects. In the Fontan circulation almost none of them were present, except for a slight late diastolic flow acceleration. This acceleration is slightly enhanced in patients with the APC and AVC Fontan modifications and in patients with no or minimal atrioventricular valve regurgitation. Many Doppler and MRI studies showed that there is some pulsation in the pulmonary blood flow of Fontan
patients. Some authors described a biphasic pattern [9], some a monophasic pattern [10]. However, the timing of the peaks and troughs were not consistent. In our study with averaged blood flow patterns, this variability in presence and timing eliminated all peaks and troughs seen in the individual pattern. Therefore, a typical pulmonary blood flow pattern for the Fontan circulation could not be delineated. Second, our algorithm to normalize measured flows to flow patterns allowed us to calculate group patterns and to compare them directly. We found that patients after different types of Fontan operations showed almost the same flow patterns. The impact of the atrial contraction was rather small. Two MRI studies [9, 11] and many Doppler studies [12–15] identified the lack of pulsation and postulated the importance of respiration in that type of circulation in lateral tunnel TCPC, as it was the idea of this modification to achieve laminar flow inside the connection by accepting the loss of pulsation caused by atrial or infundibular contractions [2]. On the other hand in APC, a Doppler study had determined the importance of atrial contraction [16]. We found only minor differFig 3. Blood flow patterns in the pulmonary artery of 17 patients with various modifications of Fontan surgery. The x-axis shows the phase of the cardiac cycle and the y-axis the normalized flow. There was no significant difference in the patterns between the 3 patients with atrioventricular connection (‚), the 9 patients with atriopulmonary connection (Œ), and the 5 patients with total cavopulmonary connection (⫻).
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Fig 4. Blood flow patterns in the pulmonary artery of 17 patients after Fontan surgery with various degrees of atrioventricular valve regurgitation. The x-axis shows the phase of the cardiac cycle and the y-axis the normalized flow. There was no significant difference in the patterns between the 13 patients with trivial or no atrioventricular valve regurgitation () compared with the 4 patients with mild or moderate regurgitation (⫻).
ences among these groups, even in the AVC group in which at least some systolic flow from a ventricular contraction was expected. This might be attributable to a longer follow-up after surgery in our patients, especially in the AVC and APC groups. Dilatation and scarring of the atrial myocardium and calcification of the patch material might have contributed to the almost absent flow propagation owing to atrial contraction. Furthermore, methodological issues might have hampered the Doppler studies. Movements of the vessel in relation to the sample probe cannot be avoided in Doppler studies. The Doppler method measures peak velocities dependent on a small area inside the vessel, chosen by the investigator. This sample area can easily be shifted by cardiac movements directly transmitted to the investigated vessels. Postprocessing in cine MRI ensures that flow is integrated from velocities over the whole cross section of the vessel even if the vessel is moving. Finally, we want to speculate about the end-diastolic flow augmentation. If we had measured these patterns in the pulmonary veins, we would have diagnosed an atrial filling restriction as the diastolic peak exceeded the systolic peak [17]. However, it has to be assumed that this effect is transmitted to the pulmonary artery in the Fontan circulation with passive pulmonary blood flow only enhanced by a suctioning systemic ventricle. Ventricular filling restriction because of the lack of preload was also described in a recent tissue Doppler study [18]. The authors reported that this restrictive filling pattern is the normal pattern in Fontan patients with preserved ventricular function. The same group published a case report [19] of a patient with tricuspid atresia after TCPC and severe mitral regurgitation showing a (pseudo) normal diastolic function that switched to the restrictive pattern after mitral valve repair. This is also in accordance with our finding that patients with more than trivial atrioventricular regurgitation showed a lesspronounced end-diastolic flow acceleration (Fig 4). This regurgitation volume caused an early filling of the ven-
tricle in diastole and impaired the hemodynamically important suctioning mechanism. It is even more speculative to find an explanation of why patients with TCPC have less flow acceleration at the end of diastole than APC or AVC patients (Fig 3). Maybe in these patients the systemic ventricle has a reservoir (right atrium with or without a right infundibulum) to suction from in front of the pulmonary vascular bed, whereas the ventricle in TCPC patients has to suction from the systemic veins directly (enhancing systemic blood flow). Thus, TCPC, if necessary combined with an atrioventricular valve repair, should be the preferred surgical approach to the Fontan circulation to get an optimal smooth flow in the whole cardiac cycle, at both the venous and the arterial levels.
Thanks to Alexander Gratz for proofreading the manuscript.
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