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Evaluation of blood flow distribution asymmetry and vascular geometry in patients with Fontan circulation using 4-D flow MRI

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Abstract

Background

Asymmetrical caval to pulmonary blood flow is suspected to cause complications in patients with Fontan circulation. The aim of this study was to test the feasibility of 4-D flow MRI for characterizing the relationship between 3-D blood flow distribution and vascular geometry.

Objective

We hypothesized that both flow distribution and geometry can be calculated with low interobserver variability and will detect a direct relationship between flow distribution and Fontan geometry.

Materials and methods

Four-dimensional flow MRI was acquired in 10 Fontan patients (age: 16 ± 4 years [mean ± standard deviation], range: 9–21 years). The Fontan connection was isolated by 3-D segmentation to evaluate flow distribution from the inferior vena cava (IVC) and superior vena cava (SVC) to the left and right pulmonary arteries (LPA, RPA) and to characterize geometry (cross-sectional area, caval offset, vessel angle).

Results

Flow distribution results indicated SVC flow tended toward the RPA while IVC flow was more evenly distributed (SVC to RPA: 78% ± 28 [9–100], IVC to LPA: 54% ± 28 [4–98]). There was a significant relationship between pulmonary artery cross-sectional area and flow distribution (IVC to RPA: R2=0.50, P=0.02; SVC to LPA: R2=0.81, P=0.0004). Good agreement was found between observers and for flow distribution when compared to net flow values.

Conclusion

Four-dimensional flow MRI was able to detect relationships between flow distribution and vessel geometry. Future studies are warranted to investigate the potential of patient specific hemodynamic analysis to improve diagnostic capability.

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References

  1. Fontan F, Baudet E (1971) Surgical repair of tricuspid atresia. Thorax 26:240–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Gewillig M (2005) The Fontan circulation. Heart 91:839–846

    Article  PubMed  PubMed Central  Google Scholar 

  3. Marelli A, Mackie A, Ionescu-Ittu R et al (2007) Congenital heart disease in the general population: changing prevalence and age distribution. Circulation 115:163–172

    Article  PubMed  Google Scholar 

  4. Larsson ES, Eriksson BO, Sixt R (2003) Decreased lung function and exercise capacity in Fontan patients. A long-term follow-up. Scand Cardiovasc J 37:58–63

    Article  CAS  PubMed  Google Scholar 

  5. Kim S-J, Kim W-H, Lim H-G et al (2008) Outcome of 200 patients after an extracardiac Fontan procedure. J Thorac Cardiovasc Surg 136:108–116

    Article  PubMed  Google Scholar 

  6. Shah MJ, Rychik J, Fogel MA et al (1997) Pulmonary AV malformations after superior cavopulmonary connection: resolution after inclusion of hepatic veins in the pulmonary circulation. Ann Thorac Surg 63:960–963

    Article  CAS  PubMed  Google Scholar 

  7. Shinohara T, Yokoyama T (2001) Pulmonary arteriovenous malformation in patients with total cavopulmonary shunt: what role does lack of hepatic venous blood flow to the lungs play? Pediatr Cardiol 22:343–346

    Article  CAS  PubMed  Google Scholar 

  8. Hiramatsu T, Komori S, Nishimura Y et al (2008) Conversion from total cavopulmonary shunt to Fontan circulation: improved cyanosis with an 11-year interval. Ann Thorac Cardiovasc Surg 14:29–31

    PubMed  Google Scholar 

  9. Sernich S, Ross-Ascuitto N, Dorotan J et al (2009) Surgical improvement of hepatic venous mixing to resolve systemic arterial hypoxemia associated with post-Fontan pulmonary arteriovenous fistulae. Tex Heart Inst J 36:480–482

    PubMed  PubMed Central  Google Scholar 

  10. Be’eri E, Maier SE, Landzberg MJ et al (1998) In vivo evaluation of Fontan pathway flow dynamics by multidimensional phase-velocity magnetic resonance imaging. Circulation 98:2873–2882

    Article  PubMed  Google Scholar 

  11. Tayama M, Hirata N, Matsushita T et al (1999) Pulmonary blood flow distribution after the total cavopulmonary connection for complex cardiac anomalies. Heart Vessels 14:154–160

    Article  CAS  PubMed  Google Scholar 

  12. Fogel MA, Weinberg PM, Rychik J et al (1999) Caval contribution to flow in the branch pulmonary arteries of Fontan patients with a novel application of magnetic resonance presaturation pulse. Circulation 99:1215–1221

    Article  CAS  PubMed  Google Scholar 

  13. Gutberlet M, Hosten N, Abdul-Khaliq H et al (1999) The value of magnetic resonance tomography (MRT) for evaluating ventricular and anastomotic functions in patients with an extra- or intracardiac total cavopulmonary connection (TCPC)-modified Fontan operation. Röfo 171:431–441

    CAS  PubMed  Google Scholar 

  14. Fratz S, Hess J, Schwaiger M et al (2002) More accurate quantification of pulmonary blood flow by magnetic resonance imaging than by lung perfusion scintigraphy in patients with fontan circulation. Circulation 106:1510–1513

    Article  PubMed  Google Scholar 

  15. Whitehead KK, Sundareswaran KS, Parks WJ et al (2009) Blood flow distribution in a large series of patients having the Fontan operation: a cardiac magnetic resonance velocity mapping study. J Thorac Cardiovasc Surg 138:96–102

    Article  PubMed  PubMed Central  Google Scholar 

  16. Brix L, Ringgaard S, Rasmusson A et al (2009) Three dimensional three component whole heart cardiovascular magnetic resonance velocity mapping: comparison of flow measurements from 3D and 2D acquisitions. J Cardiovasc Magn Reson 11:3

    Article  PubMed  PubMed Central  Google Scholar 

  17. Uribe S, Beerbaum P, Sorensen TS et al (2009) Four-dimensional (4D) flow of the whole heart and great vessels using real-time respiratory self-gating. Magn Reson Med 62:984–992

    Article  PubMed  Google Scholar 

  18. Markl M, Geiger J, Kilner PJ et al (2011) Time-resolved three-dimensional magnetic resonance velocity mapping of cardiovascular flow paths in volunteers and patients with Fontan circulation. Eur J Cardiothorac Surg 39:206–212

    Article  PubMed  Google Scholar 

  19. Valverde I, Nordmeyer S, Uribe S et al (2012) Systemic-to-pulmonary collateral flow in patients with palliated univentricular heart physiology: measurement using cardiovascular magnetic resonance 4D velocity acquisition. J Cardiovasc Magn Reson 14:25

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bachler P, Valverde I, Pinochet N et al (2013) Caval blood flow distribution in patients with Fontan circulation: quantification by using particle traces from 4D flow MR imaging. Radiology 267:67–75

    Article  PubMed  Google Scholar 

  21. Vasanawala SS, Hanneman K, Alley MT et al (2015) Congenital heart disease assessment with 4D flow MRI. J Magn Reson Imaging 42:870–886

    Article  PubMed  Google Scholar 

  22. Walker PG, Howe TT, Davies RL et al (2000) Distribution of hepatic venous blood in the total cavo-pulmonary connection: an in vitro study. Eur J Cardiothorac Surg 17:658–665

    Article  CAS  PubMed  Google Scholar 

  23. DeGroff CG, Carlton JD, Weinberg CE et al (2002) Effect of vessel size on the flow efficiency of the total cavopulmonary connection: in vitro studies. Pediatr Cardiol 23:171–177

    Article  CAS  PubMed  Google Scholar 

  24. Migliavacca F, Kilner PJ, Pennati G et al (1999) Computational fluid dynamic and magnetic resonance analyses of flow distribution between the lungs after total cavopulmonary connection. IEEE Trans Biomed Eng 46:393–399

    Article  CAS  PubMed  Google Scholar 

  25. Dasi LP, KrishnankuttyRema R, Kitajima HD et al (2009) Fontan hemodynamics: importance of pulmonary artery diameter. J Thorac Cardiovasc Surg 137:560–564

    Article  PubMed  PubMed Central  Google Scholar 

  26. Marsden AL, Bernstein AJ, Reddy M et al (2009) Evaluation of a novel Y-shaped extracardiac Fontan baffle using computational fluid dynamics. J Thorac Cardiovasc Surg 137:394–403

    Article  PubMed  Google Scholar 

  27. Dasi LP, Whitehead K, Pekkan K et al (2011) Pulmonary hepatic flow distribution in total cavopulmonary connections: extracardiac versus intracardiac. J Thorac Cardiovasc Surg 141:207–214

    Article  PubMed  PubMed Central  Google Scholar 

  28. Tang E, Restrepo M, Haggerty CM et al (2014) Geometric characterization of patient-specific total cavopulmonary connections and its relationship to hemodynamics. JACC Cardiovasc Imaging 7:215–224

    Article  PubMed  PubMed Central  Google Scholar 

  29. Slesnick TC, Yoganathan AP (2014) Computational modeling of Fontan physiology: at the crossroads of pediatric cardiology and biomedical engineering. Int J Cardiovasc Imaging 30:1073–1084

    Article  PubMed  Google Scholar 

  30. Markl M, Harloff A, Bley TA et al (2007) Time-resolved 3D MR velocity mapping at 3T: improved navigator-gated assessment of vascular anatomy and blood flow. J Magn Reson Imaging 25:824–831

    Article  PubMed  Google Scholar 

  31. Griswold MA, Jakob PM, Heidemann RM et al (2002) Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47:1202–1210

    Article  PubMed  Google Scholar 

  32. Schnell S, Markl M, Entezari P et al (2014) k-t GRAPPA accelerated four-dimensional flow MRI in the aorta: effect on scan time, image quality, and quantification of flow and wall shear stress. Magn Reson Med 72:522–533

    Article  PubMed  Google Scholar 

  33. Bernstein MA, Zhou XJ, Polzin JA et al (1998) Concomitant gradient terms in phase contrast MR: analysis and correction. Magn Reson Med 39:300–308

    Article  CAS  PubMed  Google Scholar 

  34. Walker PG, Cranney GB, Scheidegger MB et al (1993) Semiautomated method for noise reduction and background phase error correction in MR phase velocity data. J Magn Reson Imaging 3:521–530

    Article  CAS  PubMed  Google Scholar 

  35. Bock J, Kreher BW, Hennig J et al (2007) Optimized pre-processing of time-resolved 2D and 3D Phase Contrast MRI data. 15th Annual Meeting of ISMRM. Abstract 3138, Berlin, Germany

  36. Van Uitert R, Bitter I (2007) Subvoxel precise skeletons of volumetric data based on fast marching methods. Med Phys 34:627–638

    Article  PubMed  Google Scholar 

  37. Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:307–310

    Article  CAS  PubMed  Google Scholar 

  38. Friman O, Hennemuth A, Harloff A et al (2011) Probabilistic 4D blood flow tracking and uncertainty estimation. Med Image Anal 15:720–728

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge Maya Gabbour, M.D., Samantha E. Schoeneman, B.A., and Ryan Kuhn, B.S., from the Department of Medical Imaging, Ann & Robert H. Lurie Children’s Hospital of Chicago, for their contributions in data management and patient recruitment. We received grant support from the National Institutes of Health (R01HL115828) and American Heart Association (14PRE18620016).

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Correspondence to Kelly Jarvis.

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Three-dimensional blood flow visualization in a patient with Fontan circulation (patient 5, a 16-year-old boy status post extracardiac Fontan). (MPG 45906 kb)

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Jarvis, K., Schnell, S., Barker, A.J. et al. Evaluation of blood flow distribution asymmetry and vascular geometry in patients with Fontan circulation using 4-D flow MRI. Pediatr Radiol 46, 1507–1519 (2016). https://doi.org/10.1007/s00247-016-3654-3

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  • DOI: https://doi.org/10.1007/s00247-016-3654-3

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