Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 https://doi.org/10.1186/s12968-022-00852-6 RESEARCH Open Access False lumen rotational flow and aortic stiffness are associated with aortic growth rate in patients with chronic aortic dissection of the descending aorta: a 4D flow cardiovascular magnetic resonance study Aroa Ruiz‑Muñoz1,2,3,4†, Andrea Guala1,2*†, Lydia Dux‑Santoy1, Gisela Teixidó‑Turà1,2,3, Maria Luz Servato3, Filipa Valente3, Juan Garrido‑Oliver1, Laura Galian‑Gay3, Laura Gutiérrez3, Rubén Fernandez‑Galera3, Guillem Casas3, Teresa González‑Alujas3, Hug Cuéllar‑Calabria1,4,6, Kevin M. Johnson7, Oliver Wieben7, Ignacio Ferreira‑Gonzalez1,3,4,5, Arturo Evangelista1,2,3,4,8 and Jose Rodriguez‑Palomares1,2,3,4* Abstract Background: Patency of the false lumen in chronic aortic dissection (AD) is associated with aortic dilation and long- term aortic events. However, predictors of adverse outcomes in this population are limited. The aim of this study was to evaluate the relationship between aortic growth rate and false lumen flow dynamics and biomechanics in patients with chronic, patent AD. Methods: Patients with a chronic AD with patent false lumen in the descending aorta and no genetic connective tis‑ sue disorder underwent an imaging follow-up including a contrast-enhanced 4D flow cardiovascular magnetic reso‑ nance (CMR) protocol and two consecutive computed tomography angiograms (CTA) acquired at least 1 year apart. A comprehensive analysis of anatomical features (including thrombus quantification), and false lumen flow dynamics and biomechanics (pulse wave velocity) was performed. Results: Fifty-four consecutive patients with a chronic, patent false lumen in the descending aorta were included (35 surgically-treated type A AD with residual tear and 19 medically-treated type B AD). Median follow-up was 40 months. The in-plane rotational flow, pulse wave velocity and the percentage of thrombus in the false lumen were positively related to aortic growth rate (p = 0.006, 0.017, and 0.037, respectively), whereas wall shear stress showed a trend for a positive association (p = 0.060). These results were found irrespectively of the type of AD. Conclusions: In patients with chronic AD and patent false lumen of the descending aorta, rotational flow, pulse wave velocity and wall shear stress are positively related to aortic growth rate, and should be implemented in the follow-up algorithm of these patients. Further prospective studies are needed to confirm if the assessment of these parameters helps to identify patients at higher risk of adverse clinical events. *Correspondence: andrea.guala@yahoo.com; jfrodriguezpalomares@gmail.com † Aroa Ruiz Muñoz and Andrea Guala equally contributed 1 Vall d’Hebron Institut de Recerca (VHIR), Barcelona, Spain Full list of author information is available at the end of the article © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​ mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 2 of 13 Keywords: Aortic dissection, 4D flow CMR, Magnetic resonance imaging, Aortic stiffness Background potential role of wall shear stress (WSS) and the biome- Aortic dissection (AD) is one of the most devastating chanical properties of the aortic wall (aortic stiffness) complications of the thoracic aorta and is associated in patients with a chronic, patent false lumen in the with high morbidity and mortality [1]. In the recent descending aorta after an AD still remain unexplored. years, outcomes in the acute phase have improved due This study aimed to test whether false lumen flow to earlier detection, and advances in diagnostic imaging dynamics and biomechanics may predict aortic growth techniques and surgical and endovascular interventions rate in a cohort of patients with a chronic, patent false [2]. Consequently, acute aortic syndromes are increas- lumen in the descending aorta. ingly converting to chronic aortic diseases that require a close monitoring to avoid future complications. Methods Type A AD is more prevalent and requires a more Study population aggressive management, most often replacement of Between November 2015 and June 2019, consecutive the diseased part of the aorta containing the dominant patients with a chronic AD and a patent false lumen in entry tear, whereas for type B AD, pharmacological the descending aorta followed at the Aortic Unit of Vall treatment or endovascular repair in case of complica- Hebron Hospital underwent a 4D flow CMR. In January tions [1] is conventionally used. Although emergent 2021, patients with at least two computed tomography surgery for acute type A AD has significantly improved angiograms (CTA) acquired at least 1 year apart and after survival, most patients persist with a residual dissec- the CMR protocol, were identified and included. Exclu- tion of the descending aorta (surgically-treated type A sion criteria were age < 18 years, bicuspid aortic valve, with residual descending AD) [3], thereby increasing genetic connective tissue disorders, previous endovascu- the number of patients with a chronic type B AD. lar or surgical repair of the descending aorta, main entry Survival rate in chronic type B AD has been estab- tear located in the descending aorta below the level of lished around 50–80% at 5 years and 30–60% at the pulmonary artery bifurcation, complete false lumen 10 years [4–7]. Thus, frequent clinical and imaging thrombosis, baseline CTA study acquired < 3 months follow-up is recommended to evaluate the progression after the acute event, follow-up duration < 1 year and of aortic dilation [8] since endovascular aortic repair contraindication for CMR (Fig. 1). The study was or open surgery is indicated in case of either fast pro- approved by the institutional Ethics Committee and writ- gressive thoracic aortic enlargement (> 10 mm/year) ten informed consent was obtained from all participants. or aortic diameter > 60 mm [8, 9]. Predictors of aortic dilation or adverse events in patients with a patent false Computed tomography protocol lumen in the descending aorta after an AD have mostly CTAs were acquired on a 128-slice CT scanner (Defini- been focused on morphological or anatomical variables tie AS + , Siemens, Forchheim, Germany). Arterial- such as the baseline aortic diameter and entry tear size phase non-electrocardiographic (ECG) gated CTA was and its location [10]. Additionally, partial false lumen obtained after intravenous bolus injection of 100 mL thrombosis has been related to a higher aortic enlarge- of non-ionic iodinated contrast material at a flow rate ment at follow-up [11, 12]. of 4 mL/s and using an automated bolus-tracking tech- Although a patent false lumen in the descending nique. Contiguous axial 1 mm sections were acquired aorta has been associated with aortic enlargement [13], from the thoracic inlet to the pubic symphysis. need of aortic intervention/repair or late mortality [14], studies quantifying flow in the false lumen and its rela- Cardiovascular magnetic resonance protocol tionship with aortic growth rate are still limited. Studies CMR studies were performed on a 1.5 T scanner (Signa, based on 4-dimensional (4D) phase-contrast cardio- General Electric Healthcare, Waukesha, Wisconsin, vascular magnetic resonance (4D flow CMR) analysing USA). The protocol included a contrast-enhanced CMR flow dynamics in the true and false lumen have been angiogram to obtain the 3D volumes of the true and false published [15–19]. However, these studies reported lumina and two 4D flow CMR studies, one acquired with qualitative or semi-quantitative analysis of flow data a velocity encoding (VENC) of 70 cm/s to allow accu- [16, 17], included a limited number of patients (≤ 20), rate assessment of low velocities in the false lumen [20] and mixed individuals with and without genetic con- and the other with a higher VENC of 150 cm/s to assess nective tissue disorders [15–19]. Additionally, the regions of high velocity flow. Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 3 of 13 Fig. 1 Flow chart. CMR cardiovascular magnetic resonance, FL false lumen, MRA magnetic resonance angiography, CTA​ Computed tomography angiography A radially-undersampled acquisition (PC-VIPR [phase- were corrected for background phase from concomitant contrast vastly undersampled isotropic projection]) with gradients, eddy currents and trajectory errors of the 3D 5-point balanced velocity encoding [21] and retrospec- radial acquired k-space [21]. Brachial systolic and dias- tive-ECG gating during free-breathing was used for 4D tolic blood pressures were registered immediately after flow CMR imaging of the entire thoracic aorta, using the the CMR study. following parameters: field of view 400 × 400 × 400 mm, acquisition matrix 160 × 160 × 160, voxel size Aortic growth rate and anatomical features 2.5 × 2.5 × 2.5 mm and flip angle 8 ◦ . The dataset was The aortic growth rate was calculated as the differ- reconstructed according to the nominal temporal reso- ence in the diameter between the last and first available lution of each patient, ranging from 23 to 46 ms. Data CTA divided by the time interval between them, at the Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 4 of 13 level of the largest diameter on the final CTA and using The end of systole and the start of diastole was deter- the double-oblique approach. The maximum descend- mined when the flow rate-time curve at the level of the ing aortic diameter, the location and area of the domi- sinotubular junction had reached the first 0 mL/s after nant entry tear as well as the distance from the dominant the maximum peak of flow rate. Retrograde systolic and entry tear to the surgical anastomosis in type A or to the diastolic flow were calculated as the time-integral of third supraortic vessel in type B AD were defined on the backward through-plane flow rate curve over systolic baseline CTA by an experienced radiologist [22]. The or diastolic phases, respectively. False lumen retrograde dominant entry tear was defined as the largest proximal flow fraction was calculated as the ratio of retrograde communication between the true and false lumen [23]. In diastolic flow rate over the anterograde systolic flow patients with a patent false lumen in the descending aorta rate, as proposed [18]. IRF, a parameter used to quan- after a surgically-treated type A AD, in which a primary tify flow rotation within a plane, was calculated as the entry tear had been closed at surgery, the largest proxi- integral of vorticity with respect to cross-sectional area mal communication between both lumina was consid- at the systolic peak [24, 25] (Fig. 2D). Peak-systolic WSS ered to be the residual dominant entry tear. vectors were calculated at 64 points equally-distributed The percentage of thrombus in the false lumen was cal- along each false lumen contour by fitting the 3D veloc- culated as the percentage of volume with thrombus with ity data and computing velocity derivatives on the ves- respect to the total volume of the false lumen on a con- sel lumen [24, 26, 27]. Maximum systolic kinetic energy trast enhanced CMR angiography (MRA) (Fig. 2A, B). (KE), maximum systolic deceleration rate (MSDR) and flow stasis were quantified in a volume covering the false lumen from the level of the pulmonary bifurcation to the Flow dynamics and biomechanics in the false lumen by 4D diaphragmatic level. The KE was computed as the maxi- flow CMR mum value over the cardiac cycle of the sum of the KE Patent and thrombosed regions in the false lumen were in all the voxels inside the volume of interest. MSDR was semi-automatically segmented in the CMR angiogram computed as the maximum minus the minimum systolic (Fig. 2A, B) and six anatomical landmarks (sinotubular acceleration divided by the time interval between these junction, first and third supra-aortic vessels, pulmonary two acceleration peaks [28]. Flow stasis was calculated as artery bifurcation, diaphragmatic level, and dominant the percentage of cardiac time phases with a mean veloc- entry tear) were manually located using ITK-SNAP. ity < 5 cm/s, as suggested [29]. Details about the assess- These anatomical landmarks, and centreline and segmen- ment of each flow descriptor and their inter-observer and tation of both lumina were mapped to 4D flow CMR data intra-observer reproducibility are included in Additional by applying a rigid transformation. To optimize the regis- file 1 (Table S1, Figures S2-S7). tration, the surroundings of the transformed 3D volumes Regional aortic pulse wave velocity (PWV) was com- were explored with translations in the three directions puted from 4D flow CMR data in the false lumen as pre- after excluding the pulmonary artery, and the final loca- viously described [30]. Transit time was calculated with tion was selected as the one maximizing lumina blood the wavelet-based method, the most robust technique flow. Then, 4D flow CMR velocity data inside the true [31] (Fig. 2E). and false lumina were extracted. Flow dynamics in the false lumen were assessed on the Statistical analysis low VENC 4D flow CMR study by means of a custom- Continuous variables are expressed as mean ± standard designed Matlab code (Mathworks, Natick, Massachu- deviation if normally distributed and as median [1st-3rd] setts, USA). quartiles otherwise. Categorical variables are presented Flow rate, retrograde systolic and diastolic flow, ret- as frequency (percentage). The Kolmogorov–Smirnov rograde flow fraction, in-plane rotational flow (IRF) and test was used to assess distribution normality. Differences WSS were obtained in eight equidistant planes located among groups for continuous parameters were assessed perpendicular to the aortic centreline in the false lumen by Student’s t-test if normally distributed and Mann– from the level of the pulmonary artery bifurcation to Whitney U test otherwise. Chi-square test was used for the level of the diaphragm (Fig. 2C). Only those planes categorical variables. Multivariate linear regression with at > 3 cm distal to the dominant entry tear were consid- a backward selection procedure was used to identify sta- ered to avoid flow disturbances induced by the direct tistically-significant independent associations with aortic influence of the proximal entry tear. Then, for each growth rate. Independent variables entered the model descriptor of aortic flow dynamics the average of its val- if p < 0.2 on univariate analysis and were progressively ues in these planes of the descending aorta was retained excluded if p > 0.1. The inter-observer and intra-observer for the analysis. reproducibility for flow descriptors were evaluated using Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 5 of 13 Fig. 2 Pre-processing of imaging data: contrast-enhanced cardiovascular magnetic resonance angiography (A), its segmentation (B) and the extraction of the regions of interests in 4D flow data (C), and examples of rotational flow (D) and pulse wave velocity (E). CMR cardiovascular magnetic resonance, CMRA cardiovascular magnetic resonance angiography, PWV pulse wave velocity Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 6 of 13 correlation and Bland–Altman plots, Pearson correla- bias in aortic dilation due to genetic disease. Demograph- tion coefficient (R) and intra-class correlation coeffi- ics and clinical variables were similar in type A and type cients (ICC) (average measures, two-way mixed, absolute B AD, however, mechanical aortic valve and antiplatelet agreement) (Supplementary Materials). A two-tailed therapy were more prevalent in surgically-treated type A p-value < 0.05 was considered statistically significant. than in type B AD (p = 0.058 and 0.051, respectively). The SPSS (version 21.0, Statistical Package for the Social Sci- median time interval between the acute AD and the 4D ences, International Business Machines, Inc., Armonk, flow CMR study was 51 [15; 128] months. New York, USA) was used for the analysis. Over a median follow-up duration of 40 months, inter- quartile range (IQR) [24; 44] months, the median aortic Results growth rate was 1.2 [0.6; 2.7] mm/year. Demographic and clinical data From a total cohort of 97 patients with a chronic AD of Predictors of aortic growth rate the descending aorta, 54 patients met the inclusion crite- Anatomical features, flow dynamics and biomechan- ria and were included in the analysis (Fig. 1). The demo- ics in the false lumen stratified by AD type are shown in graphic and clinical characteristics stratified by AD type Table 2. Bivariate and multivariate relationships between are shown in Table 1. The cohort comprised 35 (65%) the investigated descriptors and aortic growth rate are surgically-treated type A AD and 19 (35%) medically- reported in Table 3. treated type B AD all with a patent false lumen in the descending aorta. Mean age of the overall population was 66 ± 11 years and most patients were male (44/54, 81%). Clinical and anatomical features Ten (19%) patients had a mechanical prosthetic aortic Demographic (age, sex and body surface area (BSA)) and valve. Twenty-four (44%) patients received anticoagula- clinical characteristics (blood pressure and treatment tion and/or statin therapy, and 14 (26%) were treated with with anticoagulants, antiplatelet agents and/or statins), antiplatelet agents. Most patients had a history of hyper- comorbidities (hypertension, diabetes mellitus and dys- tension (34/54, 65%) while few had a history of diabetes lipidaemia), the presence of a mechanical prosthetic aor- (5/54, 10%) or dyslipidaemia (12/54, 23%). No subject tic valve, and the type of AD were not related to aortic had a genetic connective tissue disorders, thus avoiding growth rate in bivariate analysis (Table 3). Table 1 Demographics and clinical data Characteristics Overall (n = 54) Surgically-treated type A AD Medically-treated type P-value with residual tear (n = 35) B AD (n = 19) Age [years] 66 ± 11 68 ± 11 64 ± 10 0.174 Sex [male] 44 (81%) 27 (77%) 17 (89%) 0.265 BSA ­[m2] 1.9 ± 0.2 1.9 ± 0.2 1.9 ± 0.2 0.701 SBP [mmHg] 138 ± 20 140 ± 21 134 ± 20 0.278 DBP [mmHg] 79 ± 13 76 ± 12 84 ± 15 0.128 Stroke volume [mL] 55 ± 19 53 ± 19 57 ± 20 0.488 Active smoker 10 (19%) 6 (18%) 4 (21%) 0.800 Hypertension 34 (65%) 21 (64%) 13 (68%) 0.727 Diabetes mellitus 5 (10%) 3 (9%) 2 (10%) 0.866 Dyslipidaemia 12 (23%) 7 (21%) 5 (26%) 0.674 Mechanical prosthetic aortic valve 10 (19%) 9 (26%) 1 (5%) 0.058 Anticoagulation therapy 24 (44%) 18 (51%) 6 (32%) 0.163 Antiplatelet therapy 14 (26%) 12 (35%) 2 (10%) 0.051 Statin therapy 22 (44%) 14 (45%) 8 (42%) 0.833 Heart rate [bpm] 63 ± 10 65 ± 10 61 ± 9 0.330 Follow-up duration between baseline and final CTAs 35 ± 11 33 ± 11 34 ± 12 0.878 [months] Time between acute AD and 4D flow [months] 78 ± 81 95 ± 92 47 ± 43 0.099 Aortic growth rate [mm/year] 1.8 ± 1.6 1.7 ± 1.6 1.9 ± 1.6 0.550 Values are mean ± standard deviation or n (%) AD aortic dissection, BSA body surface area, CTA​ computed tomography angiogram, SBP and DBP systolic and diastolic blood pressure, respectively Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 7 of 13 Table 2 Anatomical features, flow dynamics and biomechanics in the false lumen Overall (n = 54) Surgically-treated type A AD with Medically-treated type P-value residual tear (n = 35) B AD (n = 19) Anatomical features Maximum DAo diameter [mm] 48 ± 10 48 ± 11 49 ± 8 0.368 Dominant entry tear area ­[cm2] 1.2 ± 0.8 1.1 ± 0.8 1.3 ± 0.9 0.326 Local distance of the dominant entry tear 28 ± 28 30 ± 26 26 ± 33 0.370 [mm] Thrombus in the false lumen [%] 11 ± 14 11 ± 14 12 ± 16 0.636 Flow dynamics in the false lumen Retrograde systolic flow [mL] 1.6 ± 1.3 1.6 ± 1.1 1.6 ± 1.5 0.867 Retrograde diastolic flow [mL] 9.7 ± 5.0 9.8 ± 4.5 9.5 ± 6.0 0.553 Retrograde flow fraction [%] 82 ± 42 92 ± 42 66 ± 38 0.109 IRF ­[cm2/s] 1.25 ± 5.79 1.04 ± 4.55 1.63 ± 7.72 0.923 WSS [N/m2] 0.26 ± 0.10 0.26 ± 0.10 0.24 ± 0.10 0.475 KE [mJ] 0.62 ± 0.48 0.54 ± 0.34 0.47 ± 0.30 0.523 MSDR [cm/s3] 2996 ± 2552 3448 ± 2531 2193 ± 2453 0.055 Flow stasis [%] 52 ± 18 54 ± 18 47 ± 18 0.200 Biomechanics in the false lumen PWV [m/s] 7.7 ± 3.7 7.7 ± 3.7 7.6 ± 3.6 0.808 Values are mean ± standard deviation DAo descending aorta, IRF in-plane rotational flow, KE kinetic energy, MSDR maximum systolic deceleration rate, PWV pulse wave velocity, WSS wall shear stress The median of the maximum descending aortic diame- growth rate (R = 0.279, p = 0.060) (Fig. 3E). Median IRF ter at baseline was 45 [40; 54] and 46 [43; 54] mm in type was non-significantly lower in type A than in type B A and B AD, respectively (Table 2). In the whole cohort it AD (1.60 [− 1.80; 4.09] vs. 0.76 [− 4.30; 7.17]). It was was significantly and positively related to aortic growth 1.3 [− 1.9; 4.2] c­ m2/s in the whole population and was rate (R = 0.280, p = 0.042) (Fig. 3A). Median dominant positively related to aortic enlargement rate (R = 0.393, entry tear area was non-significantly higher in type A p = 0.006) (Fig. 3D). Thus, a larger rotational component compared to type B AD (1.0 [0.5; 1.6] vs. 0.8 [0.6; 1.9], of blood flow and an increased stress conveyed by blood respectively). In the whole population, it was 0.9 c­m2, flow to the aortic wall were associated with faster growth. ranging from 0.12 to 10 ­cm2 (Table 2), and was positively Regarding local stiffness, median PWV was 6.8 [4.5; but not significantly associated with aortic growth rate 10.9] m/s in type A AD, 7.7 [4.8; 10.0] m/s in type B (R = 0.257, p = 0.096) (Fig. 3B). The location of the domi- AD and 7.4 [4.8; 10.5] m/s in the entire cohort. It was nant entry tear was similar in both types of AD. Throm- positively related to growth rate (R = 0.370, p = 0.017) bus was present in 49% of the population, occupying (Fig. 3F). Therefore, a stiffer false lumen was associated between 1 and 42% of the false lumen volume, it was sim- with faster local growth. ilar in type A and type B AD and was positively related to aortic enlargement rate (R = 0.336, p = 0.037) (Fig. 3C). Multivariate analysis In a multivariate model corrected for dominant entry Flow dynamics and biomechanics in the false lumen tear area and the percentage of false lumen occupied by Flow dynamics was not distinct in type A and type B AD, thrombus, both IRF and PWV were independently and only MSDR was increased in type A compared to type positively related to aortic growth rate (p = 0.008 and B AD (3123 [1081; 4999] vs. 1576 [950; 2722]) (Table 2). p = 0.017, respectively) (Table 3). Systolic and diastolic retrograde flow, retrograde flow fraction, KE, MSDR and flow stasis in the false lumen Impact of aortic dissection type were not related to aortic growth rate (Table 3). Median As prognosis for surgically-treated type A AD or medi- WSS was 0.25 [0.18; 0.34] and 0.23 [0.15; 0.34] N/m2 in cally treated type B AD is different; anatomical fea- type A and type B AD, respectively, and 0.25 [0.16; 0.34] tures, and false lumen flow dynamics and biomechanics N/m2 in the whole population. It showed a positive, were analyzed, separately, according to the type of AD nearly statistically-significant association with aortic (Table 2). No differences were found between both types Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 8 of 13 Table 3 Bivariate and multivariate correlation of demographics, anatomical features, and flow dynamics and biomechanics in the false lumen with aortic growth rate Bivariate Multivariate R P-value Beta P-value 95% CI Demographics and clinical data Age [years] 0.018 0.899 Sex (male) 0.398 Body surface area 0.101 0.494 Systolic blood pressure [mmHg] 0.086 0.566 Diastolic blood pressure [mmHg] 0.071 0.637 Smoking 0.390 Hypertension 0.386 Diabetes mellitus 0.391 Dyslipidaemia 0.396 Mechanical prosthetic aortic valve 0.397 Anticoagulation therapy 0.396 Antiplatelet therapy 0.394 Statin therapy 0.394 Type of aortic dissection 0.481 Anatomical features Maximum DAo diameter [mm] 0.280 0.042 Dominant entry tear area ­[cm2] 0.257 0.096 0.371 0.018 [0.130; 1.251] Local distance of the dominant entry tear [mm] -0.094 0.513 Thrombus in the false lumen [%] 0.336 0.037 0.293 0.049 [0.000; 0.065] Flow dynamics in the false lumen Retrograde systolic flow [mL] 0.165 0.237 Retrograde diastolic flow [mL] 0.102 0.465 Retrograde flow fraction [%] 0.060 0.708 IRF ­[cm2/s] 0.393 0.006 0.433 0.008 [0.034; 0.202] WSS [N/m2] 0.279 0.060 KE [mJ] 0.015 0.919 MSDR [cm/s3] -0.214 0.136 Flow stasis [%] 0.106 0.457 Biomechanics in the false lumen PWV [m/s] 0.370 0.017 0.360 0.017 [0.031; 0.281] DAo descending aorta, IRF in-plane rotational flow, KE kinetic energy, MSDR maximum systolic deceleration rate, PWV pulse wave velocity, WSS wall shear stress of AD in terms of growth rate, dominant entry tear area, diastolic flow and flow stasis (ICC > 0.90). MSDR thrombus in the false lumen, IRF, WSS and PWV. More- showed good inter-observer and excellent intra-observer over, the inclusion of the type of AD into the multivariate agreement. model reported in Table 3 did not provide any added pre- dictive value for growth rate (p = 0.864). Discussion This study reported a comprehensive analysis of the rela- Reproducibility of flow descriptors tionship between anatomical features, flow dynamics Details of inter-observer and intra-observer variability for and biomechanical descriptors in the false lumen with flow descriptors are shown in Additional file 1 (Table S1, aortic growth rate in a cohort of patients with a patent Figures S2-S7). Inter-observer and intra-observer repro- false lumen in the descending aorta after a surgically- ducibilities were good for maximum velocity, retrograde treated type A or medically-treated type B AD. The main systolic flow, retrograde flow fraction, IRF, WSS and KE findings of this work were that in-plane rotational flow, (ICC between 0.75 and 0.90) and excellent for retrograde false lumen stiffness and the proportion of false lumen Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 9 of 13 Fig. 3 Scatter plots showing correlations between aortic growth rate and maximum diameter of the descending aorta at baseline (A), dominant entry tear area (B), thrombus (C), in-plane rotational flow (D) wall shear stress (E), and pulse wave velocity (F) in the false lumen. AD aortic dissection, FL false lumen Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 10 of 13 occupied by thrombus were positively and independently investigated its potential role in chronic descending related to aortic growth rate. Additionally, wall shear AD. A pathological wall shear stress in the false lumen stress showed a positively nearly-significant association may play a similar role to that found in the other with aortic growth rate. This is the largest 4D flow CMR pathologies confined to the ascending aorta [35, 36]. study aiming at the assessment of predictors of progres- In this study a positive, nearly-statistical significant sive dilation for chronic descending AD. association was found between WSS and aortic growth rate (p = 0.060), but this relationship was not sustained Anatomical features in multivariate analysis. However, the in-plane rota- Imaging studies suggested that complete thrombosis tional flow, which is a measurement of rotational flow of the false lumen has beneficial prognostic value [32], similar to circumferential WSS [34], was found to be whereas a patent false lumen predicts poor outcome independently and positively related to aortic growth and progressive aortic dilation [6, 10, 11, 13, 33]. On the rate (p = 0.008). As commented above, we hypoth- other hand, there are discrepancies with respect to the esized that the presence of rotational flow in the false role of partial thrombosis for aortic adverse events and lumen may be related to the difficulty of the flow to growth rate in type B AD. In most previous studies, the move forward the false lumen and the limited drainage existence and distribution of thrombus was determined at the exit tear/s, which may lead to higher pressuri- semi-quantitatively. This is the first study to perform a zation in the false lumen and thus may contribute to volumetric quantification of the presence of thrombus in aortic dilation. Further prospective studies including a the false lumen and to evaluate its role in aortic dilation. larger number of patients are needed to confirm these Our study is in line with a previous study which dem- hypothesis. onstrated that new or increased false lumen thrombo- The relationship of KE and flow stasis in the false sis area during follow-up was strongly associated with a lumen with aortic growth rate had not been previously faster aortic growth and late adverse events [12]. analysed in patients with chronic descending AD. This study reported that KE, flow stasis and MSDR were not Flow dynamics and biomechanics in the false lumen associated with aortic growth rate. Our results concur The potential role of rotational flow in promoting aor- with those of Marlevi et al. who found the MSDR to tic enlargement has been suggested in previous studies be equal between stable and enlarging growth groups based on other aortic conditions such as in the pres- [37]. We speculate that a larger cohort may be needed ence of bicuspid aortic valve and Marfan syndrome [24, to unveil the possible role of KE and flow stasis in the 27, 34]. To the best of our knowledge, this is also the prediction of growth rate in descending AD. first quantitative study assessing rotational flow pat- Confirming findings in other conditions [38, 39], terns and WSS in the false lumen of chronic AD of the this study showed that PWV is an excellent predic- descending aorta. Qualitatively-assessed, marked systolic tor for aortic dilation. In chronic descending AD, an helical flow in the false lumen was reported [16] and was increased PWV, indicating an increased stiffness of the related to the rate of aortic growth rate in bivariate analy- false lumen wall, could furthermore induce resistance sis [17]. These preliminary qualitative results were here in flow progression. Indeed, for a given volume of blood confirmed with quantitative data, since IRF was inde- filling the false lumen, higher stiffness would result in pendently associated with aortic growth. Present results higher false lumen pressure. This finding would be in further specify the independent predictive value of rota- line with the observations of Burris et al. [37] in which tional flow on top of established predictors, such as entry a higher false lumen ejection fraction (associated with tear area [10], whose role was confirmed in the present lack of flow progression due to greater false lumen cohort. We speculate that a large rotational flow may pressure) is associated with a greater aortic dilation. result in increased stress to the aortic wall that would Although long-term outcomes of patients with surgi- induce a greater aortic growth (similarly to other aortic cally-treated type A and medically-treated type B AD diseases). Additionally, it may also indicate a limited flow are distinct [10], the increased helicity of flow and aor- progression within the false lumen, possibly associated tic stiffness are conditions observed independently of with higher local pressure. Therefore, these two factors the type of AD for predicting faster growth rate. This (higher pressure and increased wall shear stress) could confirms the role and strength of the predictors deter- jointly induce aortic dilation. This hypothesis should be mined in the present study. demonstrated in larger scaled studies. Limitations Although wall shear stress has been shown to affect aortic dilation in bicuspid aortic valve and Marfan Despite being the largest study to date testing aor- syndrome patients [24, 27, 34, 35], no previous study tic flow dynamics and stiffness as predictors of aortic Ruiz‑Muñoz et al. Journal of Cardiovascular Magnetic Resonance (2022) 24:20 Page 11 of 13 dilation in chronic non-complicated descending AD, (SEC/FEC-INV-CLI 20/015 and SEC/FEC-INV-CLI 21/030) and the Biomedical Research Networking Center on Cardiovascular Diseases (CIBERCV). Guala the size of the cohort is still only modest. This was A. has received funding from Spanish Ministry of Science, Innovation and partially due to the exclusion of patients with genetic Universities (IJC2018-037349-I). connective tissue disorders, whose evolution may sub- Availability of data and materials stantially differ. Another limitation was the variability The datasets used and/or analysed during the current study are available from of the time interval between the acute event and the 4D the corresponding author on reasonable request. flow CMR study. However, all CMR studies have been performed in the chronic phase to ensure the stability Declarations of flow variables that may be more variable in the acute Ethics approval and consent to participate or subacute phase. Larger prospective studies initiated Institutional Review Board approval was obtained and written informed systematically after the acute event are needed to con- consent was obtained from all subjects (patients) in this study. firm present findings. Finally, the use of time-resolved Consent for publication segmentations of the false lumen may entail a more Not applicable. accurate wall shear stress quantification by addressing the effect of intimal flap motion, which is nonetheless Competing interests K.M. Johnson and O. Wieben have received significant research grants from GE limited in chronic dissections [8]. Healthcare through The University of Wisconsin-Madison (no personal com‑ pensation). The other authors declare that they have no competing interests. Author details Conclusions 1 Vall d’Hebron Institut de Recerca (VHIR), Barcelona, Spain. 2 CIBER-CV, Instituto Increased rotational flow, aortic stiffness and wall shear de Salud Carlos III, Madrid, Spain. 3 Department of Cardiology, Hospital Univer‑ stress are related to aortic growth rate in patients with sitari Vall d´Hebron, Barcelona, Spain. 4 Department of Medicine, Universitat Autònoma de Barcelona, Bellaterra, Spain. 5 CIBERESP, Instituto de Salud an uncomplicated chronic descending AD with no Carlos III, Madrid, Spain. 6 Department of Radiology, Hospital Universitari Vall genetic connective tissue disorders. Clinical follow-up d’Hebron, Barcelona, Spain. 7 Departments of Medical Physics & Radiology, of these variables may help to identify patients at major University of Wisconsin, Madison, WI, USA. 8 Instituto del Corazón. Quirónsalud- Teknon, Barcelona, Spain. risk of late adverse events or in need of further inter- ventions or more frequent monitoring. Received: 15 October 2021 Accepted: 14 March 2022 Abbreviations AD: Aortic dissection; BSA: Body surface area; CMR: Cardiovascular magnetic resonance; CMRA: Cardiovascular magnetic resonance angiography; CTA​: References Computed tomography angiogram; DAo: Descending aorta; ECG: Electrocar‑ 1. Evangelista A, Isselbacher EM, Bossone E, Gleason TG, Di Eusanio M, diogram; FL: False lumen; IRF: In-plane rotational flow; KE: Maximum systolic Sechtem U, Ehrlich MP, Trimarchi S, Braverman A, Myrmel T, et al. Insights kinetic energy; MSDR: Maximum systolic deceleration rate; PWV: Pulse wave From the International Registry of Acute Aortic: A 20-year experience of velocity; VENC: Velocity encoding; WSS: Wall shear stress. collaborative clinical research. Circulation. 2018. https://​doi.​org/​10.​1161/​ CIRCU​LATIO​NAHA.​105.​000620. 2. Pape LA, Awais M, Woznicki EM, Suzuki T, Trimarchi S, Evangelista A, Supplementary Information Myrmel T, Larsen M, Harris KM, Greason K, et al. 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