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Interact CardioVasc Thorac Surg 2009;9:155-158. doi:10.1510/icvts.2008.195859
© 2009 European Association of Cardio-Thoracic Surgery

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Work in progress report - Vascular thoracic

Preliminary results by flow-sensitive magnetic resonance imaging after Tiron David I procedure with an anatomically shaped ascending aortic graft{star}

Alex Frydrychowicz*, Alexander Berger, Aurélien F. Stalder and Michael Markl

Department of Diagnostic Radiology and Medical Physics, University Hospital Freiburg, Germany

Received 6 October 2008; received in revised form 2 April 2009; accepted 3 April 2009

{star} The authors have no relevant financial disclosures. Dr Markl receives governmental funding from "Deutsche Forschungsgemeinschaft" (DFG) Grant # MA 2383/4-1 and "Bundesministerium für Bildung und Forschung" Grant # 01EV0706.

*Corresponding author. University Hospital Freiburg, Department of Diagnostic Radiology, Hugstetter Str. 55, 79106 Freiburg, Germany. Tel.: +49-761-270-2401; fax: +49-761-270-3831. E-mail address: alex.frydrychowicz{at}uniklinik-freiburg.de (A. Frydrychowicz).


    Abstract
 Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Acknowledgements
 References
 
We present preliminary data of the vascular hemodynamics in a novel, anatomically shaped ascending aortic graft in comparison to non-operated individuals by use of 3D magnetic resonance (MR) flow measurements. We examined a 72-year-old male patient after Tiron David I valve sparing aortic root reconstruction and replacement of the ascending aorta (AAo) with an anatomically curved prosthesis. Results from flow-sensitive MR at 3T were compared to 12 age-matched individuals with comparable diameters of the AAo. For 3D flow visualization, streamlines and time-resolved particle traces were applied. A visual analysis of hemodynamic properties including blood flow helicity, vorticity and retrograde flow was performed. In contrast to reported highly disturbed flow of straight aortic grafts in the literature, the patient analysis revealed smooth blood flow through the graft which gave rise to a right-handed helical flow in the reconstructed aorta. In comparison to non-operated volunteers, blood flow helicity was more pronounced. Flow jets or vortices were not encountered. While physiological retrograde flow was seen in the volunteers, it was absent in the patient which may be explained by the altered aortic compliance and thus reduced Windkessel effect. This promising finding will have to prove its validity in further comparative studies.

Key Words: Velocity mapping; Time-resolved MRA; Phase contrast MRI; Anatomically shaped aortic graft; Aortic aneurysm


    1. Introduction
 Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Acknowledgements
 References
 
There have been various reports about the significance of hemodynamic considerations in aortic surgery analyzed either directly by magnetic resonance (MR) imaging [1] or with the aid of computer models and computational fluid dynamics (CFD) [2]. However, the in-vivo accuracy of those models might be questionable and in-vivo validation remains a challenge.

Replacing parts of the aorta as a standard procedure, e.g. in aortic aneurysm, dissection, or rupture has been shown to induce overt changes in the associated hemodynamics. Long-term effects related to the altered conductance of flow may be important for clinical management but can nowadays only be hypothesized (see Table 1). However, hemodynamic research offers proof of vascular remodeling in the presence of altered blood flow conditions and therefore, points towards an optimization of hemodynamic outcome in aortic surgery especially in the young.


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Table 1 Summary of hemodynamic findings in straight aortic grafts investigated by flow sensitive magnetic resonance imaging

 
Previously published works have aimed at a comparison of aortic valve surgery to normal controls [3], presented initial insights into the effect of straight aortic grafts in the descending and ascending aorta (AAo) [1, 4–6], and valve prosthesis [7]. Since its first description in 1996 [8], modern 4-dimensional qualitative blood flow analysis has been shown to be able to detect alterations in hemodynamics in comparison to normal controls [5] and has been optimized in terms of patient comfort and feasibility [9].

An anatomically shaped aortic graft for replacement of the AAo may result in hemodynamically improved conductance of the blood flow. Thereby it may offer improved outcome for the individual patient since vascular remodeling and related complication such as thrombosis or aneurysm formation proximal or distal to the graft may be avoided. This may be of special note since the hemodynamic contribution to secondary complications, e.g. as the mediating mechanism in situations where steep gradients along the vascular wall are induced by sutures and implanted grafts are present, is not known at all. However, it is beyond doubt that implanted fabric grafts are at risk for secondary geometrical changes [10] which may be mediated by largely altered hemodynamics.

In this preliminary study we aimed at the analysis of blood flow in a single patient after replacement of the AAo with an anatomically shaped vascular tube graft in comparison to blood flow properties in 12 age-matched healthy volunteers with a comparable size of the AAo.


    2. Materials and methods
 Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Acknowledgements
 References
 
2.1. Graft and operative procedure

A 72-year-old male was operated because of an ascending aortic aneurysm six months prior to the MR flow study receiving a novel anatomically shaped 31 mm vascular tube graft (Uni-graft® W, Braun, Aesculap, Tuttlingen, Germany) and a typical Tiron David I operation.

Preoperative echocardiography revealed aortic diameters of 55 mm in the AAo, 40 mm at the aortic sinus, and 35 mm at the annulus. Left ventricular (LV) function was reported to be normal, and except from mild sclerosis there were no signs of an aortic valve pathology. The operative procedure was performed by Prof. Hans-H. Sievers at Lübeck University Hospital, Department of Cardiovascular Surgery. In brief, the David I operation consisted of replacement of the wall of the aortic root with a 31-mm Dacron tube graft with re-implantation of the coronary artery ostia. The aortic valve leaflets were preserved. The recovery was uneventful and the patient was discharged 10 days postoperatively. Postoperative echocardiography revealed a visually normal LVEF. Aortic valve function remained unsuspicious.

2.2. MR flow analysis

Flow experiments were performed in a 72-year-old male (107 kg) six months after replacement of the aortic arch with an anatomically shaped vascular tube graft (diameter 31 mm). Findings were compared to hemodynamic analyses in 12 age-matched individuals (64±10 years, 72.3±10.8 kg, 7 females, 5 males) with comparable diameters of the AAo of 3.1±0.2 mm. The volunteer data were taken from a collective of 62 individuals previously examined by MR flow acquisitions for analysis of thoracic aortic hemodynamics at the Freiburg University Cardiovascular Imaging Group [11]. Black-blood HASTE acquisitions were performed in all three spatial directions and the aortic diameter was measured at the level of the pulmonary artery bifurcation.

All examinations were previously approved by the Local Ethics Committee and were performed after written informed consent on a 3T MR system (Magnetom TRIO, Siemens, Germany, maximum gradient strength=40 mT/m, rise time=200 µs, 8-channel receiver coil). We applied a rf-spoiled gradient echo sequence using interleaved 3-directional velocity encoding during free breathing and prospective ECG gating. Examinations were carefully adapted to each individual's anatomy and data were collected with {alpha}=15°, venc=150 cm/s, TE=3.67 ms, TR=5.6 ms, bandwidth 480 Hz/pixel, temporal resolution=48.8 ms and a spatial resolution of 3.0x1.7x3.2 mm3. To minimize breathing artifacts and image blurring, respiration control was performed based on combined adaptive k-space reordering and navigator gating [9].

2.3. Visualization and qualitative evaluation

All blood flow analyses were performed using a homebuilt software tool based on MatLab (The MathWorks Inc, Natick, MA, USA). 4D flow visualization included time-resolved, color-encoded visualization of flow characteristics (EnSight 8.2, CEI, Apex, NC, USA) based on 3D streamlines and particle traces. The visual evaluation of datasets was performed by two experienced readers in a consensus reading with the surgeon (A.F. and M.M.) screening for general hemodynamics, blood flow helicity, development, size and direction of vortices, and degree of physiological retrograde flow in the AAo, the aortic arch (arch), and the descending aorta (DAo).


    3. Results
 Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Acknowledgements
 References
 
3.1. MR acquisitions and post-processing

All blood flow acquisitions in the patient and the individuals were successfully performed and the resulting data sets were of sufficient quality for the subsequent pre-processing and visualization strategy.

3.2. Analysis of control individuals

In agreement with previously published analyses [12] and pictorial data [5, 6, 9], the control individuals presented with straight or pre-dominantly right helical blood flow in the AAo and transverse arch (right=5, none=6, left=1). No local accelerations or decelerations of the overall blood flow were detected. We encountered a total of 24 vortices in the thoracic aorta with a median of two vortices (0–4 vortices, 7 individuals showed 2 vortices). Most of the vortices were seen in the ascending and proximal DAo (AAo=10, DAo=10, arch=4). In all volunteers, late-systolic retrograde flow was encountered in the AAo (n=11) and arch (n=10) whereas in the DAo, the number of individuals without retrograde flow markedly decreased (n=4). Its pre-dominant localization was found at the inner curvature pointing to the left body half and changed slightly to the inner and outer right.

3.3. Patient analysis

As shown in Figs. 1 and 2, there were three major findings indicating near-physiological aortic blood flow conditions after implantation of the anatomically shaped ascending aortic graft:
  1. Preserved right helical flow which was slightly accelerated at the larger curvature of the AAo and the right body half. No local blood flow accelerations or attenuations were observed. The helix was markedly accentuated especially in the proximal AAo with an absence of re-circulating flow or vortices at the proximal or distal graft orifice.
  2. Throughout the measured 2/3 of the cardiac cycle, no relevant retrograde flow was seen. This may be attributed to a prolonged cardiac output phase or, most likely, to the decreased compliance of the graft material.
  3. From the hemodynamic images the exact localization of the graft could not be determined (e.g. no localized blood flow alterations at the site of the proximal and distal anastomosis were detectable) which hints toward optimized conditions with respect to anastomosis, suture, and conduction of blood flow.


Figure 1
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Fig. 1. 3D streamline visualization during peak systole. Color-coding corresponded to absolute velocity measurements as indicated in the right upper corner. Accelerated blood flow in the left ventricular outflow tract (LVOT) can be appreciated which transitioned smoothly into a pronounced right helix through the ascending aorta and arch. According to physiology, accelerated flow also appeared at the outer curvature (white arrowheads). The asterisk indicates aberrant streamlines related to noise within the acquired images. The incomplete depiction of the supraaortic arteries and the aberrant streamlines can be attributed to the limited spatiotemporal resolution and noise level within the images. No vortices can be observed.

 

Figure 2
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Fig. 2. Time-integrated 3D particle traces allow an overview over the blood flow traces over time. Clearly, the pronounced helical flow in the proximal graft and the smooth right helical flow through the ascending aorta and aortic arch can be appreciated.

 

    4. Discussion
 Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Acknowledgements
 References
 
Our preliminary results demonstrated blood flow in the anatomically shaped ascending aortic graft of a single patient that was in most respects similar to findings in a collective of normal volunteers with comparable sizes of the AAo. In contrast to findings in grafts by Bogren et al. [4] and Frydrychowicz and co-workers [6] for which highly disturbed flow and small re-circulating vortices adjacent to the straight graft wall were reported (see also Table 1), near-physiological blood flow in the anatomically shaped graft was observed. In most respects, the observed blood flow properties were in agreement with earlier results from 2D and 3D analyses of blood flow as presented by Kilner et al. [12] and Bogren and co-workers [13]. The interpretation and conclusions are based on the assumption that an increased number of vortices and disturbed flow resemble a loss of kinetic energy of the blood flow and bury potentially negative effects for the vasculature whereas laminar-like flow properties are optimal with respect to the derived forces of the blood flow on the vascular wall especially distal to the graft.

The loss of retrograde flow in our patient may most likely be attributed to the altered material of the graft and the loss of the elastic properties that usually allows for the Windkessel effect. General atherosclerotic stiffening of the vessel wall of the entire aorta, such as in cardiovascular disease, results in earlier and more pronounced reflection of the aortic pressure wave from the peripheral vessels which leads to increased retrograde flow [12, 13]. In contrast, the altered compliance of the graft in the patient introduced a highly localized increased stiffness in the AAo. The normal AAo exhibits a very pronounced Windkessel effect which supports normal diastolic retrograde flow assisting the filling of the coronary arteries. We hypothesized that the lesser elasticity of the graft compromised this effect and reduced retrograde flow.

It has to be noted though that the imaging sequence allowed acquiring only approximately two-thirds of the cardiac cycle. Therefore, parts of late diastole were not depicted. However, there is evidence toward the fact that normal retrograde flow is early-diastolic [12]. Although the flow-sensitive measurements used in this study did not cover the entire cardiac cycle, the early-diastolic blood flow has been covered and acquired. This potential limitation can be overcome by the integration of retrograde ECG-triggering which was not available at the time of the study. Further, a potential drawback may be seen in the lack of a gold standard of comparison. Yet, neither ultrasound, contrast-enhanced ultrasound, nor computed tomography, digital subtraction angiography, or computational fluid design can provide the detailed information gained with the presented 3D flow-sensitive MR examinations.

The analysis performed in this study was limited to the blood flow of the aorta thereby disregarding blood flow kinetics induced by the left ventricle that can supposedly vary significantly. This may be seen as a potential drawback of the study which may be overcome by additional complex 4D blood flow analysis of the entire LV system. Despite the fact that initial LV studies have been presented [14] a comprehensive acquisition and evaluation strategy for the combined investigation of LV and aortic blood flow was not available at the time of this study. It has to be further noted that the data acquisition scheme relies on a temporal averaging of data and thus cyclic variations in blood flow dynamics over multiple cardiac cycles cannot be resolved. Effectively, minor variations in blood flow properties such as small turbulences and instabilities may remain undetected. Last, the limited spatiotemporal resolution and thus noise level within the images is the cause of the incomplete depiction of the supraaortic arteries and the aberrant streamlines. Further methodological improvements will in future help to overcome these shortcomings.

The method used for this analysis has successfully detected hemodynamic alterations in various cardiovascular situations and geometrically alterations before. In addition to this qualitative analysis, future studies can also include the analysis of the resulting wall shear stress and shear indices. Although the method is limited by its spatial and temporal resolution, it enables to generate intrinsically consistent values [15] and may therefore be used to detect alterations of related vessel wall parameters also.

The preliminary data presented here are based on observations in a single patient only. Therefore, a powerful study, e.g. of different commonly used prostheses may thus be conducted by expanding this preliminary setting to overcome limiting issues of a small sample size and a purely qualitative data analysis strategy.

Nevertheless, the presented 3D visualization of flow characteristics in an optimized aortic graft demonstrated the potential of the analysis methodology. With respect to the future analysis of hemodynamics in aortic grafts, this implies the potential to analyze the conduction of blood flow which may help to overcome difficulties imposed by implanting a prosthetic tube in the human vasculature.


    Acknowledgements
 Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Acknowledgements
 References
 
We would like to thank Prof. Hans-H. Sievers and his colleagues from the Department of Cardiovascular Surgery at Lübeck University Hospital, Germany for the co-operation and our co-workers Adriana Komancsek, Manuela Keckeis, and Maximilian F. Russe for their valuable contribution and continuous support.


    References
 Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Acknowledgements
 References
 

  1. Bogren HG, Buonocore MH, Follette DM. Four-dimensional aortic blood flow patterns in thoracic aortic grafts. J Cardiovasc Magn Reson 2000;2:201–208.[Medline]
  2. Lei M, Archie JP, Kleinstreuer C. Computational design of a bypass graft that minimizes wall shear stress gradients in the region of the distal anastomosis. J Vasc Surg 1997;25:637–646.[CrossRef][Medline]
  3. Markl M, Draney MT, Miller DC, Levin JM, Williamson EE, Pelc NJ, Liang DH, Herfkens RJ. Time-resolved three-dimensional magnetic resonance velocity mapping of aortic flow in healthy volunteers and patients after valve-sparing aortic root replacement. J Thorac Cardiovasc Surg 2005;130:456–463.[Abstract/Free Full Text]
  4. Bogren HG, Mohiaddin RH, Yang GZ, Kilner PJ, Firmin DN. Magnetic resonance velocity vector mapping of blood flow in thoracic aortic aneurysms and grafts. J Thorac Cardiovasc Surg 1995;110:704–714.[Abstract/Free Full Text]
  5. Frydrychowicz A, Harloff A, Jung B, Zaitsev M, Weigang E, Bley TA, Langer M, Hennig J, Markl M. Time-resolved, 3-dimensional magnetic resonance flow analysis at 3T: visualization of normal and pathological aortic vascular hemodynamics. J Comput Assist Tomogr 2007;31:9–15.[CrossRef][Medline]
  6. Frydrychowicz A, Weigang E, Langer M, Markl M. Flow-sensitive 3D magnetic resonance imaging reveals complex blood flow alterations in aortic Dacron graft repair. Interact CardioVasc Thorac Surg 2006;5:340–342.[Abstract/Free Full Text]
  7. Kozerke S, Hasenkam JM, Pedersen EM, Boesiger P. Visualization of flow patterns distal to aortic valve prostheses in humans using a fast approach for cine 3D velocity mapping. J Magn Reson Imaging 2001;13:690–698.[CrossRef][Medline]
  8. Wigstrom L, Sjoqvist L, Wranne B. Temporally resolved 3D phase-contrast imaging. Magn Reson Med 1996;36:800–803.[Medline]
  9. Markl M, Harloff A, Bley TA, Zaitsev M, Jung B, Weigang E, Langer M, Hennig J, Frydrychowicz A. Time-resolved 3D MR velocity mapping at 3T: improved navigator-gated assessment of vascular anatomy and blood flow. J Magn Reson Imaging 2007;25:824–831.[CrossRef][Medline]
  10. Bromberg BI, Beekman RH, Rocchini AP, Snider AR, Bank ER, Heidelberger K, Rosenthal A. Aortic aneurysm after patch aortoplasty repair of coarctation: a prospective analysis of prevalence, screening tests and risks. J Am Coll Cardiol 1989;14:734–741.[Abstract]
  11. Frydrychowicz A, Stalder AF, Harloff A, Berger A, Russe MF, Hennig J, Langer M, Markl M. Initial results from diameter dependence of thoracic aortic hemodynamics acquired by 4D flow-sensitive MRI at 3T. Proc Intl Soc Mag Reson Med 2007.
  12. Kilner PJ, Yang GZ, Mohiaddin RH, Firmin DN, Longmore DB. Helical and retrograde secondary flow patterns in the aortic arch studied by three-directional magnetic resonance velocity mapping. Circulation 1993;88:2235–2247.[Abstract/Free Full Text]
  13. Bogren HG, Buonocore MH, Valente RJ. Four-dimensional magnetic resonance velocity mapping of blood flow patterns in the aorta in patients with atherosclerotic coronary artery disease compared to age-matched normal subjects. J Magn Reson Imaging 2004;19:417–427.[CrossRef][Medline]
  14. Bolger AF, Heiberg E, Karlsson M, Wigstrom L, Engvall J, Sigfridsson A, Ebbers T, Kvitting JP, Carlhall CJ, Wranne B. Transit of blood flow through the human left ventricle mapped by cardiovascular magnetic resonance. J Cardiovasc Magn Reson 2007;9:741–747.[CrossRef][Medline]
  15. Stalder AF, Russe MF, Frydrychowicz A, Bock J, Hennig J, Markl M. Quantitative 2D and 3D phase contrast MRI: optimized analysis of blood flow and vessel wall parameters. Magn Reson Med 2008;60:1218–1231.[CrossRef][Medline]




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