Int J Cardiovasc Imaging DOI 10.1007/s10554-014-0580-z


Pulmonary vascular remodeling before and after pulmonary endarterectomy in patients with chronic thromboembolic pulmonary hypertension: a cardiac magnetic resonance study Andreas Rolf • Johannes Rixe • Won K. Kim • Stefan Guth • Nils Ko¨rlings • Helge Mo¨llmann • Holger M. Nef • Christoph Liebetrau • Gabriele Krombach Thorsten Kramm • Eckhard Mayer • Christian W. Hamm

Received: 6 October 2014 / Accepted: 12 December 2014 Ó Springer Science+Business Media Dordrecht 2014

Abstract Phase-contrast magnetic resonance imaging (PC-MRI) offers a range of surrogate markers to quantify the hemodynamic changes associated with chronic thromboembolic pulmonary hypertension (CTEPH). Our aim was to noninvasively monitor effects of pulmonary vascular remodeling before and after endarterectomy (PEA) in patients with CTEPH by using PC-MRI. Fifty-seven consecutive patients (mean age 56.7 ± 16, 28 female) underwent PC-MRI before and after PEA as part of their perioperative routine workup. Pulmonary artery (PA) maximum flow velocity (maxV), acceleration time/ejection time (AT/ET), distensibility [(PA maximum area - PA minimum area)/PA minimum area], mid-systolic flow deceleration (notch), and the timing of deceleration (notch ratio) were recorded. Mean PA pressure was obtained from standard right heart catheter procedures. maxV and AT/ET

Electronic supplementary material The online version of this article (doi:10.1007/s10554-014-0580-z) contains supplementary material, which is available to authorized users. A. Rolf (&)  W. K. Kim  H. Mo¨llmann  C. Liebetrau  C. W. Hamm Department of Cardiology, Kerckhoff Heart and Lung Centre, Benekestrasse 2-8, 61231 Bad Nauheim, Germany e-mail: [email protected]; [email protected] A. Rolf  J. Rixe  N. Ko¨rlings  H. M. Nef  C. W. Hamm Department of Cardiology, University of Giessen, Giessen, Germany S. Guth  T. Kramm  E. Mayer Department of Thoracic Surgery, Kerckhoff Heart and Lung Centre, Bad Nauheim, Germany G. Krombach Department of Radiology, University of Giessen, Giessen, Germany

were decreased before PEA and significantly improved afterwards (60.8 ± 16 vs. 73.8 ± 19 cm/s, p = 0.007; 0.32 ± 0.06 vs. 0.36 ± 0.09, p = 0.0015). Surprisingly, distensibility did not change significantly (30 ± 19 vs. 26 ± 12 %, p = 0.11). Forty-five patients (78 %) had a systolic notch before PEA that persisted in only 10 (18 %; p = 0.00001). Among patients with a persisting notch, the notch ratio did not significantly increase (1.3 ± 0.2 vs. 1.6 ± 1.5, p = 0.32). Our data show early PA reverse remodeling after PEA. Flow velocities increase while PA flow wave reflections represented by mid-systolic flow deceleration are abolished. In some patients a mid-systolic notch persists, suggesting increased downstream resistance as a consequence of small vessel arteriopathy. Keywords Cardiac MRI  Chronic thromboembolic pulmonary hypertension  Pulmonary endarterectomy  Vascular remodeling

Introduction Chronic thromboembolic pulmonary hypertension (CTEPH) is an important and frequently encountered type of pulmonary hypertension that has been acknowledged as an independent entity in the Dana Point and renewed Nice Classification [1]. Its incidence is estimated to be between 0.5 and 3.8 % following acute pulmonary embolism [2–4]. In contrast to pulmonary hypertension of other etiologies, CTEPH is potentially curable by pulmonary endarterectomy (PEA) with excellent long-term results [5, 6]. The changes found in the pulmonary vasculature are a consequence of incomplete thrombus resolution, remodeling of the thrombus, and neoangiogenesis mediated by inflammatory processes [7]. As a consequence, the intimal


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layer of the central and segmental vessels are encased by fibrous tissue, and the thrombus itself is reorganized by neochannels and pouches lined with endothelium, creating the characteristic pattern of webs and bands [8]. In later stages of the disease vascular remodeling extends beyond the central vessels and also involves the vascular bed primarily not affected by thromboemboli. At this stage the histopathology of the vasculature resembles that found in idiopathic pulmonary arterial hypertension [9]. The sequelae of thrombus remodeling result in decreased vessel distensibility, increased pressure and resistance, and reduced flow. The resistive forces in the pulmonary bed can be further partitioned into upstream and downstream components [10]. Depending on the degree of small vessel arteriopathy, patients present with more or less pronounced downstream resistance. It has been shown that CTEPH patients that have\60 % of the downstream component of the pulmonary resistance have a better outcome after PEA [11]. Cardiac magnetic resonance imaging (MRI) can be used to monitor some of the aforementioned changes to the vascular bed. Phase-contrast MRI (PC-MRI) allows visualization of changing vessel diameters as well as measurement of blood velocity (cm/s) over the cardiac cycle. From these measurements a range of surrogate markers of pulmonary vascular remodeling can be derived. As a consequence of increased pressure and resistance absolute flow velocity is reduced and the acceleration time (AT) or acceleration time over ejection time (AT/ET) of the flow curve is shortened [12–15]. The central pulmonary vessels are enlarged because of increased pressures, and at the same time their distensibility decreases due to fibrous remodeling. Distensibility correlates well with PVR and has been shown to have prognostic value [16–18]. The term distensibility is used in various contexts in the literature; here it is defined as ðPA maximum area  PA minimum areaÞ PA minimum area Wave reflections in the pulmonary bed contribute greatly to overall pulmonary resistance [14]. Recently, Hardziyenka et al. [19] proposed a new echocardiographic marker that differentiates between upstream and downstream resistance. The so-called mid- or late systolic notch, which mirrors deceleration of pulmonary flow caused by wave reflections, reflects the degree by which downstream resistance contributes to overall resistance. The further the notch is shifted to late systole, the larger the downstream resistance. Klok et al. [20] applied the same parameter to PC-MRI measurements of flow in follow-up examinations of patients with acute pulmonary embolism and found the notch only in one patient, who had developed CTEPH. All parameters can be derived from a single PC-MRI measurement in the pulmonary artery (PA). We utilized this technique with a cohort of CTEPH patients to monitor


pulmonary vascular remodeling and reverse remodeling completely noninvasively before and shortly after PEA. As CTEPH before and after surgery behaves like an on/ off phenomenon of pulmonary hypertension, it is an ideal setting to study the feasibility of PC-MRI as a follow up marker of pulmonary hypertension. All parameters derived from these measurements reflect changes in pressure and resistance. While no single parameter has clearly defined advantages over the others, the notch ratio has at least the potential to reflect changes in the partioning of up- and downstream resistive forces. It was therefore the aim of our study to demonstrate the feasibility of PCI-MRI to follow up patients with pulmonary hypertension, especially CTEPH, and to detect increasing downstream resistance.

Methods Patients and ethics Sixty-five consecutive patients who were referred for PEA and completed cardiac MRI as part of their peri-operative routine workup were initially enrolled in this study. Contraindications for MRI were renal failure with GFR below 30 ml/min/1.73 m2, incompatible metallic implants, known intolerance to gadolinium, and claustrophobia. All patients gave written informed consent. The study was approved by the ethics committee of the University of Giessen. Cardiac PC-MRI All patients were examined on a 1.5 T MR scanner (Sonata, Siemens, Erlangen, Germany) in the head-first, supine position using a six-channel phased array surface coil. Image acquisition was performed perpendicular to the main PA about 1–2 cm above the pulmonary valve in a double oblique plane to assure orthogonal flow measurements. Typical sequence parameters of the retrograde ECG-gated phase contrast gradient echo sequence were as follows: TE 2.8 ms, TR 11 ms, flip angle 30°, receiver bandwidth 1,220 Hz/px, in-plane resolution 1.5 9 2 mm, with three signal averages, and VENC 150 cm/s yielding a temporal resolution of 22 ms. Patients were encouraged to use shallow breathing during signal acquisition. Depending on the patient´s heart rate, between 30 and 60 time frames were reconstructed. Image analysis All images were analyzed on an off-line workstation (Argus, Siemens, Erlangen, Germany). Regions of interest

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(ROI) were traced manually in the PA on magnitude images and transferred to the phase images. Peak velocity and maximum/minimum area of the PA were computed automatically from the ROIs, and PA area distensibility was calculated as described in the Introduction (Fig. 1). AT, ET, and notch ratio were recorded manually from flow/time curves. The notch ratio was computed as systolic time before deceleration (t1) divided by systolic time after deceleration (t2) (Fig. 2). Right heart catheterization Pre- and post-operative pulmonary pressures were obtained from routine right heart catheterization measurements during the pre-operative workup and in the intensive care unit after PEA. Statistics The Shapiro–Wilk test was used to test the data for normality. Values are presented as mean ± SD, and counts are presented as absolute frequencies and percentages. Student´s t test for paired data was used to test for significant differences between pre- and post-operative values.

McNemar´s test for paired data was used to compare count variables. In cases of non-Gaussian distribution the Wilcoxon signed rank test for paired data was used. Nonparametric ROC analysis was performed and Youden’s J index was applied to define cut-off values for prediction of binary events. An alpha error of \0.05 was accepted as significant. All tests were performed using STATA11 (StataCorp, College Station, Texas, USA).

Results Of the 65 consecutive patients who were enrolled in the study, 57 had good-quality, diagnostic PC-MRI images and 8 had to be excluded because of motion artifacts. Twentyeight were female, and the mean age was 56.7 ± 16 years. Median time between preoperative MR and surgery was 1 day (IQR 1–3), median time between postoperative RHC and postoperative MR was 11 days (IQR 10–11). Mean PA pressure (mPAP) was markedly elevated before PEA and dropped significantly afterwards (47 ± 12 vs. 25 ± 9 mmHg, p = 0.0001). PVR data were completely available pre and post PEA for only 16 patients of the cohort, in those PVR decreased significantly from 531 ± 176 to 331 ± 279, p = 0.01.

Fig. 1 Magnitude image of the pulmonary trunk. The left panel shows PA max area at systole; the right panel shows PA min area

Fig. 2 Flow time curves. The left-hand panel shows a typical flow time curve before PEA with mid-systolic deceleration (notch). The right-hand panel shows flow time curves after PEA; notch is no longer present. Acceleration time (AT), ejection time (ET), systolic time before (t1) and after (t2) notch


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Fig. 3 Peak velocity, AT/ET, and distensibility before and after PEA. Peak velocity and AT/ET were significantly higher following PEA

Table 1 Patient characteristics and PC-MRI-derived parameters of vascular remodeling Mean age (years)

56.7 ± 16

Female gender (%)

28 (43) Before PEA

The improvement in pressure and resistance is reflected by the CMR parameters. PA peak velocity significantly increased after PEA from 60.8 ± 16 to 73.8 ± 19 cm/s (p = 0.007), and AT/ET changed accordingly from 0.32 ± 0.06 to 0.36 ± 0.09 (p = 0.0015). PA max area significantly decreased from 11.5 ± 3.3 to 8.8 ± 2.5 cm2 (p = 0.00001). The PA distensibility decreased from 30 ± 19 to 26 ± 12 %; however this change was not significant (p = 0.11) (Fig. 3; Compare Tables 1 and 2 for results). Forty-five patients (78 %) showed a systolic notch before PEA, which persisted in ten patients (18 %) after PEA (p = 0.00001) (Fig. 4). In the group of patients that showed a systolic notch before and after PEA, the notch ratio increased from 1.3 ± 0.2 to 1.6 ± 1.5, but this was not significant (p = 0.32). Figure 2 shows the different flow curve patterns before and after PEA. None of the patients who did not show a notch before PEA developed one afterwards. Patients in whom the systolic notch persisted showed a tendency for a lower peak velocity (57.6 ± 10 vs.


p value

mPAP (mmHg)

47 ± 12

25 ± 9


PA peak velocity (cm/s)

60.8 ± 16

73.8 ± 19



0.32 ± 0.06

0.36 ± 0.09



Fig. 4 The frequency of notch before and after PEA. The decrease in the frequency of notch after PEA was significant

After PEA

PA max area (cm )

11.5 ± 3.3

8.8 ± 2.5


PA distensibility (%)

30 ± 19

26 ± 12


Presence of systolic notch (%)

45 (78)

10 (18)


Notch ratio (n = 10)

1.3 ± 0.2

1.6 ± 1.5


AT acceleration time, ET ejection time, mPAP mean pulmonary arterial pressure, PA pulmonary artery, PEA pulmonary endarterectomy Table 2 Comparison of pre-operative PC-MRI parameters in patients with persisting notch Notch-free after PEA

Persisting notch after PEA

p value

PA peak velocity (cm/s)

62.5 ± 17

57.6 ± 10




0.32 ± 0.07

0.31 ± 0.03

PA distensibility (%)

30 ± 19

30 ± 19


Notch ratio (n = 10)

1.2 ± 0.39

1.3 ± 0.23


AT acceleration time, ET ejection time, PA pulmonary artery, PEA pulmonary endarterectomy

62.5 ± 17 cm/s, p = 0.38) and AT/ET (0.31 ± 0.03 vs. 0.32 ± 0.07, p = 0.62) before PEA and a higher notch ratio (1.3 ± 0.23 vs. 1.2 ± 0.39) before PEA than patients without a persisting notch. PVR was higher in patients with persisting notch (698 ± 328 vs. 549 ± 237, p = 0.15). However, all of these results failed to reach statistical significance.

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AT/ET and notch ratio were well correlated (r = 0.75, p = 0.0001). Non-parametric ROC analysis and Youden´s J index identified a notch ratio of 1.25 as a predictor of persisting notch with a sensitivity of 66 % and a specificity of 69 %.

Discussion The current view on the pathogenesis of CTEPH is that it is a vascular repair process mediated by monocytes entailing incomplete thrombus resolution, inflammation, fibrosis and neoangiogenesis [7]. In some patients the process of vascular remodeling extends beyond the vessels primarily affected by thromboembolism and evolves into small vessel arteriopathy similar to that seen in idiopathic pulmonary hypertension [9]. PEA offers a potential cure by removing any organized thrombus material and performing an endarterectomy down to the sub-segmental level [4, 5]. More distal parts of the pulmonary vascular tree are beyond the reach of the surgeon. Once small vessel arteriopathy has ensued, the prognosis of the patients is worse [19, 21]. Cardiac MRI is part of the routine workup for CTEPH patients at our institution because it yields a plethora of diagnostic information ranging from PA angiography and perfusion to right ventricular function and the analysis of flow in the PA. We hypothesized that a single PC-MRI sequence of the PH protocol in the PA trunk yields several parameters, that reflect vascular remodeling and reverse remodeling with special respect to upstream and downstream forces. In the present study we found that (1) peak velocity and AT/ET were reduced before PEA and significantly increased afterwards. (2) the maximum PA area was enlarged before PEA and was significantly reduced afterwards, while PA distensibility was limited before surgery and remained unchanged by PEA. (3) The majority of patients, 45, expressed a systolic notch before PEA, while only 10 patients were found to have a systolic notch after surgery. In those patients with persisting notch, the notch ratio increased—albeit not significantly. In any fluid-dynamic system, increased resistance leads to decreased flow. It was therefore to be expected that PA peak velocity and AT/ET would increase after PEA. Our data are in good agreement with reports from Kreitner et al. and Ley et al. [22, 23] comparing flow velocity before and after PEA; these authors also found significant increases post-PEA. The values we report here are higher than those found by Kreitner and Ley, but they were measured at the pulmonary trunk, whereas Kreitner and Ley measured flow

in the right and left PA. However, the absolute values compare well with data from Sanz et al. measured at the pulmonary trunk in pulmonary hypertensive patients of different etiology. Castelain et al. have shown, that due to the very proximal remodeling of the PA in CTEPH, pressure rises more instantly and steeply in CTEPH compared to PH of other etiologies. This instant pressure rise is the basis for the short AT/ET found in our cohort. The increasing AT/ET after PEA therefore reflects the removal of the fibrous endoluminal layer of the proximal PA very well. PA distensibility is a completely non-invasive parameter that correlates well with PA resistance and stiffness [16–18, 24–26]. Reduced distensibility of the PA was even found in patients with only mild pulmonary hypertension and was shown to be predictive of mortality [27]. Increased stiffness of the vascular system can be both cause and effect of increased vascular pressure [18]. Interestingly, in a rat model of pulmonary hypertension an excess of collagen in the large pulmonary vessels was associated with reduced PA elastance. It is therefore not surprising that distensibility was severely reduced in our patients before PEA, as a thick endoluminal fibrous layer is the hallmark of the disease. We expected a considerable improvement of distensibility after PEA; conversely, the values were even further decreased. A likely explanation for this result is the surgical technique used. The most proximal part of the pulmonary trunk is spared from endarterectomy, hence its elastic properties do not change. However, it is there that we made the measurements. The decreased distensibility at the proximal trunk is probably a consequence of the improved downstream elasticity of the segmental pulmonary arteries faced by the proximal trunk. The increasing flow finds a vent in the now much more elastic distal parts of the segmental pulmonary arteries, which act like a windkessel for the fibrous proximal PA. During the course of the disease CTEPH can evolve into small vessel arteriopathy [9], and this is associated with adverse outcome even after PEA [21]. Small vessel arteriopathy, however, is a histological diagnosis. Therefore, clinical parameters are required that suggest the presence of small vessel remodeling. By use of a right heart catheter pulmonary arterial occlusion technique it is possible to partition overall resistance into upstream (proximal) and downstream (pre-capillary small arteries) resistance [11]. Wave reflections cause mid- to late systolic decelerations in the PA flow [28]. It was shown that distal obstructions of the pulmonary bed were associated with later decelerations in the flow curve in comparison with proximal obstructions [28, 29]. Based on these findings Hardziyenka et al. [19] developed novel echocardiographic markers, the systolic notch and notch ratio, to identify CTEPH patients with


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higher likelihood of small vessel arteriopathy and thus higher likelihood of adverse outcome after PEA. We applied the same technique as described by Hardziyenka et al. [19] to pulmonary flow curves from PC-MRI measurements. Klok et al. [20] already showed that the systolic notch can also be found in pulmonary flow curves of CTEPH patients. A systolic notch was observed in 45 of the 57 patients (78 %) that persisted in 10 patients. Patients not exhibiting a notch before PEA did not develop one afterwards. Of note, in the group of 10 patients with persisting notch the notch ratio showed a tendency to increase, albeit not significantly. This is particularly interesting as it shows that after resection of the proximal obstruction the wave reflection shifts further downstream and is most likely caused by small vessel arteriopathy, which of course persists after PEA. Also, the baseline notch ratio was slightly larger among patients with persisting notch, although the difference failed to reach significance. These findings agree well with the data from Hardziyenka et al. [19] who also found increasing notch ratios after PEA and larger notch ratios in patients with persisting notch . The notch ratios reported here are larger compared with those reported by Hardziyenka et al. [19]. This can be explained by differences in the temporal resolution of flow measurements, which is lower in MRI compared with echocardiography. True partioning of up- and downstream resistive forces is only possible by pulmonary occlusion pressure tracing wave form analysis. In the absence of this gold standard we used CTEPH as an on/off model of pulmonary hypertension. As is the nature of the disease, the site of wave reflection will shift downstream once the proximal obstruction is removed. In the healthy pulmonary bed wave reflections occur in diastole and can therefore not be detected in pressure or flow tracings [30]. However in case of CTEPH wave reflections will still be visible if either small vessel arteriopathy is present or subsegmental obstruction persists. The results found in our study are exactly as hypothesized. So in the light of other studies using either ultrasound or direct flow measurements [19, 28, 30] we think it justified to assume that PC-CMR flow measurements reflect changes in up- and downstream resistance accurately. To further strengthen this theory we compared norch ratio and AT/ET. The proximal fibrous encasement of the pulmonary vasculature affects AT/ET and notch ratio in a similar way, because for this reason the PA pressure rise is more instant and steeper and wave reflections occur earlier in the systolic phase of the cardiac cycle [30, 31]. Even though both parameters are independent, they were well correlated, which supports our hypothesis of a downstream shift of resistance. To the best of our knowledge our study reports the largest series of patients with CTEPH undergoing PC-MRI to mirror


PA vascular remodeling before and after PEA. All parameters reported here have been validated against hemodynamic measurements [15–19, 24]. The data reflecting vascular remodeling before PEA consist of decreased flow velocities and AT/ET with decreased distensibility and the presence of wave reflections. After PEA, wave reflections in pulmonary flow ceased in the majority of patients. In the small group of patients in which wave reflections persisted, the notch ratio increased, suggesting small vessel arteriopathy beyond the reach of the surgeon. The proximal trunk of the PA, spared from endarterectomy, is even less distensible as elastance of the peripheral vessels increases. As a consequence of these changes velocity and AT/ET are improved.

Limitations The parameters presented here are surrogate markers of vascular remodelling. They have not been validated against hemodynamics within the study, because all hemodynamic data have been collected retrospectively. However the changes of these surrogate markers over time (before and after surgery) are very plausible, given that CTEPH before and after surgery is like an on and off phenomenon. We therefore think it is reasonable to conclude, that phase contrast MRI is a well suited tool to study intraindividual changes of the pulmonary vasculature. Conflict of interest The authors declare, that they have no conflict of interest related to this work.

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Pulmonary vascular remodeling before and after pulmonary endarterectomy in patients with chronic thromboembolic pulmonary hypertension: a cardiac magnetic resonance study.

Phase-contrast magnetic resonance imaging (PC-MRI) offers a range of surrogate markers to quantify the hemodynamic changes associated with chronic thr...
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