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Abstract

 
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OBJECTIVES

This study aimed to explore the flow dynamics factors affecting turbulence formation in the false lumen (FL) of aortic dissection using four-dimensional flow magnetic resonance imaging (4D flow MRI). This study also aimed to uncover risk factors affecting late complications of aortic dissection.

METHODS

Thirty-three aortic dissection patients were examined using 4D flow MRI for quantitative flow dynamics (gross flow, velocity and regurgitant fraction) and turbulence visualization (helix and vortex with three-point visual grading) in the FL. The incidence of late complications (rupture or prophylactic intervention) was also obtained prospectively.

RESULTS

The helix grade was correlated with FL gross flow (rS = 0.55, P < 0.001) and FL velocity (rS = 0.45, P = 0.008). The vortex grade was also correlated with FL gross flow (rS = 0.70, P < 0.001) and FL velocity (rS = 0.67, P < 0.001). Comparative analysis of patients with complications and stable patients revealed that patients with complications exhibited higher FL gross flow [41.7 (interquartile range, IQR 29.1–59.7) vs 17.7 (IQR 9.0–42.0) ml/s; P = 0.01], higher helix grade [2 (IQR 1.25–2) vs 0 (IQR 0–1); P = 0.001] and higher vortex grade [2 (IQR 1–2) vs 0 (IQR 0–2); P = 0.01].

CONCLUSIONS

Using 4D flow MRI analysis, we showed that turbulence formation depends on flow volume and velocity in the FL. Patients with high-volume turbulent flow in their FL are at higher risk of late complications; therefore, close follow-up and aggressive prophylactic intervention may improve their survival.

Clinical trial registration number

Nippon Medical School Hospital Institutional Review Board approved this observational study in September 2018 (No. 30-08-986).

Thoracic aorta, Aortic dissection, False lumen, Magnetic resonance imaging, Four-dimensional flow magnetic resonance imaging, Haemodynamic alteration

INTRODUCTION

Despite successful emergency surgical treatment for type A aortic dissection, the distal aorta can remain dissected and at risk of aneurysmal degeneration [1]. Similarly, patients with type B aortic dissection (TBAD) exhibit delayed aortic growth, which can lead to late complications [2]. Prognostic outcomes of chronic aortic dissection are affected by thrombosis status inside the false lumen (FL): patients with FL perfusion, especially partially thrombosed FL, are at higher risk of late complications compared to patients with a completely occluded FL [1–4]. This crucial finding indicates that haemodynamic conditions in the FL can cause an aneurysmal change in the dissected aorta, ultimately determining late outcomes [3, 5]. Accordingly, there has been an ongoing debate regarding the feasibility to identify patients at risk of dissection-related complications with imaging technology and improve their survival by timely prophylactic intervention [2].

Four-dimensional flow magnetic resonance imaging (4D flow MRI) was developed to assess aortic flow dynamics by accurately quantifying flow volume and velocity, as well as visualization of velocity-encoded three-dimensional pathlines [6]. Recent 4D flow studies have reported several flow dynamics in the FL including volume, direction, velocity, and turbulence formation, as contributing factors for aortic growth [7, 8]. In addition, turbulent flow was identified as a risk factor for aortic degeneration mediated by endothelial reaction to changes in local wall shear stress, as well as by relative hypoxia due to reduced blood circulation [7, 9]. Turbulence formation in the FL presents itself as a potential predictor of complication in the dissected aorta; however, the mechanism by which turbulence is generated in the FL remains unclear.

The objective of this observational study was to uncover the flow dynamic mechanism of turbulence formation inside the FL by investigating the correlation between quantitative haemodynamic parameters and their impact on turbulence formation using 4D flow MRI. This study also performed comparison analysis regarding complications.

MATERIALS AND METHODS

Study cohort

Between April 2018 and March 2020, a total of 33 chronic aortic dissection patients were enrolled and underwent a single 4D flow MRI evaluation. The cohort included 20 (61%) patients with repaired type A aortic dissection (rTAAD) and 13 (39%) patients of TBAD. Patients were excluded for (i) completely thrombosed FL, (ii) a history of endovascular aortic repair or (iii) known contraindications to MRI with gadolinium-based contrast media.

Nippon Medical School Hospital Institutional Review Board approved this observational study (No. 30-08-986). Written consent was obtained from all subjects.

4D flow MRI acquisition techniques

Achieva 3.0 T (Philips) with flow patch (GyroTools, Winterthur, Switzerland) was used [10]. To maintain a high signal–noise ratio in the target vessel, we used triphasic protocol with 0.1 mmol/kg gadobutrol injection (Gadovist, Bayer Healthcare, Osaka, Japan). We administered a half-dose bolus injection of contrast agent (2 ml/s) followed by a saline flush (2 ml/s) to acquire time-resolved contrast-enhanced magnetic resonance angiography, with a scan time of 2 min. Following the scan, 4D flow MRI was initiated with a slow flow infusion (0.02–0.04 ml/s) of the remaining half dose of contrast agent followed by a slow flow saline flush injection (0.02–0.04 ml/s). The scan parameters were as follows: echo time = 4.4 ms; repetition time = 2.5 ms; flip angle = 11°; resolution = 1.7 × 1.7 × 2.0 mm3; triple-velocity encoding (VENC) acquisition = 50–100–300 cm/s; k-t principle component analysis (acceleration factor = 5–7); free breath acquisition; and acquisition time = 8–15 min depending on heart rate [11, 12]. Triple-VENC acquisition was applied to widen the dynamic range of the velocity quantification and accurately capture slow flow in the FL [10, 13].

4D flow MRI quantification and visualization

The following parameters were obtained separately in the true lumen (TL) and FL (Fig. 1):

  • Gross flow (ml/s) = forward flow (ml/s) + backward flow (ml/s)

  • Average velocity (cm/s) = gross flow (ml/s)/cross-sectional area (mm2)

  • Regurgitant fraction (%) = backward flow (ml/s)/gross flow (ml/s)

A case example of quantification of flow dynamics in the true and false lumen. (A) Three-dimensional segmentation of a thoracic aorta. (B) Pathline visualization, and slice placement at the cross-section containing the largest aortic diameter perpendicular to the estimated centreline. (C) The flow analysis region of interest is placed separately on the true and false lumen. (D) Forward and backward flow volume is obtained separately through 1 cardiac cycle.
Figure 1:

A case example of quantification of flow dynamics in the true and false lumen. (A) Three-dimensional segmentation of a thoracic aorta. (B) Pathline visualization, and slice placement at the cross-section containing the largest aortic diameter perpendicular to the estimated centreline. (C) The flow analysis region of interest is placed separately on the true and false lumen. (D) Forward and backward flow volume is obtained separately through 1 cardiac cycle.

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Also, three-dimensional flow patterns inside the FL were visualized. Figure 2 and Video 1 shows representative pathline images with helices, vortices and laminar flow. A turbulent flow pattern includes helices which are defined as a blood column moving spirally in the main flow direction (Fig. 2A) and vortices which are defined as recirculating blood deviating from main flow direction (Fig. 2B) [9]. Helices and vortices were visualized and graded (grades 0–2) using the following scale: no helices or vortices (laminar flow) = grade 0; mild/moderate helices or vortices (<360° of rotation) = grade 1; and severe helices or vortices (≥360° of rotation) = grade 2, as previously described [14]. All reported helix and vortex grades are averages from 3 independent and blinded observers. Figure 3 shows visualized pathlines of helices at 5 time points in the cardiac cycle. Flow analyses were performed using GT Flow software (GyroTools).

Representative pathline images of flow dynamics in the false lumen. (A) Helices occur in the distal arch near the intimal tear of type B aortic dissection. (B) Vortices are depicted in a patient with type A aortic dissection after total arch replacement and descending aortic replacement. (C) Antegrade low-volume laminar flow is observed in the false lumen of a repaired type A aortic dissection. (D) Antegrade high-volume laminar flow is observed in the false lumen of a repaired type A aortic dissection with total arch replacement distally anastomosed in a double barrel fashion.
Figure 2:

Representative pathline images of flow dynamics in the false lumen. (A) Helices occur in the distal arch near the intimal tear of type B aortic dissection. (B) Vortices are depicted in a patient with type A aortic dissection after total arch replacement and descending aortic replacement. (C) Antegrade low-volume laminar flow is observed in the false lumen of a repaired type A aortic dissection. (D) Antegrade high-volume laminar flow is observed in the false lumen of a repaired type A aortic dissection with total arch replacement distally anastomosed in a double barrel fashion.

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Helix visualization at 5 time points in the cardiac cycle. (A) Horizontally rotated view of a three-dimensional pathline image shows helices in the false lumen of the distal arch. Helices in the false lumen occur in the systole and disappears in the diastole. (B) Magnified images depict a high-velocity flow jet passing through the entry tear in the systole (arrow).
Figure 3:

Helix visualization at 5 time points in the cardiac cycle. (A) Horizontally rotated view of a three-dimensional pathline image shows helices in the false lumen of the distal arch. Helices in the false lumen occur in the systole and disappears in the diastole. (B) Magnified images depict a high-velocity flow jet passing through the entry tear in the systole (arrow).

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Baseline morphological information

Computed tomography (CT) angiography was used to measure the following morphological parameters during 4D flow MRI evaluation; (i) maximal aortic diameter, (ii) FL diameter, (iii) dominant entry diameter, (iv) the localization of the entry tear (inner/outer curvature), and (v) FL thrombosis status (patent/partially thrombosed). Sizing of maximal aortic diameter was performed at the largest short-axial diameter, perpendicular to the estimated centreline. Sizing of FL diameter was performed at the same contour. FL thrombosis status was classified as patent if flow was present in the absence of thrombus, or as partially thrombosed if both flow and thrombus were present [3, 4].

Patient clinical outcomes

After 4D flow MRI evaluation, follow-up information including complications (aortic rupture or prophylactic intervention) and imaging data (yearly CT) was prospectively obtained until February 2021. Aortic growth rate (mm/year) was calculated as the difference between the maximal aortic diameter on baseline CT scan and the latest CT scan. A group comparison between patients with and without complications was performed.

Statistical analysis

Considering skewness and kurtosis of continuous variables due to small size of the cohort, continuous variables are listed as median (interquartile range, IQR) and compared with the non-parametric Mann–Whitney U-test. The Fisher’s exact test was used to evaluate differences in the frequency of categorical variables. Visual grades of turbulent flow (grades 0–2) were compared using the non-parametric Mann–Whitney U-test. A P-value of <0.05 was considered statistically significant.

To explore correlation of the grades of helix and vortex with haemodynamic and morphological parameters, Spearman’s (rS) correlation coefficient was calculated as appropriate.

Statistical analyses were performed with EZR (Saitama Medical Centre, Jichi Medical University, Saitama, Japan) [15], which is a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria).

RESULTS

Patient characteristics

Patient characteristics are summarized in Table 1. The median patient age was 64 (IQR 51–70, range 39–84) years, and 21 (64%) patients were male. The majority (20/33, 61%) had FL ranging from the thoracic aorta to the abdominal aorta. Localized FL within the thoracic aorta were mostly observed in TBAD patients (6/7, 86%), while localized FL within the abdominal aorta was only observed in rTAAD patients. Partially thrombosed FL were observed in 14 (42%) patients and the rate was not significantly different between rTAAD and TBAD. The median time interval from diagnosis of aortic dissection to 4D flow MRI scan was 9 (IQR 4–20, range 1–86) months.

Table 1:
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Demographics and clinical patient characteristics

VariablesDissection type
P-valueFL thrombosis status
P-value
rTAAD (n = 20)TBAD (n = 13)Patent (n = 21)Partially thrombosed (n = 12)
Age (years), median (IQR)55 (47–67)68 (65–74)0.0158 (51–68)68 (59–74)0.18
Male gender, n (%)13 (65)8 (62)>0.9912 (57)9 (75)0.46
Connective tissue disease, n (%)2 (10)0 (0)0.511 (5)1 (8)>0.99
Range of FL, n (%)
 Thoracic and abdominal aorta13 (65)7 (54)14 (67)6 (50)
 Thoracic aorta1 (5)6 (46)5 (24)2 (17)
 Abdominal aorta6 (30)0 (0)0.044 (19)4 (33)0.62
Baseline CT morphological information
 Maximum aortic diameter (mm), median (IQR)41.3 (33.7–49.8)40.0 (35.9–44.9)0.8338.1 (34.0–45.0)42.6 (37.5–55.3)0.12
 FL diameter (mm), median (IQR)24.1 (19.2–35.7)20.0 (15.6–27.0)0.2121.0 (16.1–31.0)23.1 (20.0–41.0)0.29
 Dominant entry diameter (mm), median (IQR)6.1 (4.5–10.4)8.0 (6.5–12.0)0.387.0 (4.7–11.0)6.8 (4.5–9.8)0.64
 Entry site at inner curvature, n (%)8 (40)8 (62)0.2911 (52)5 (42)0.72
 Partially thrombosed FL, n (%)5 (25)7 (54)0.14
Clinical outcomes after 4D flow MRI evaluation
 Rupture, n (%)1 (5)1 (8)>0.991 (5)1 (8)>0.99
 Prophylactic intervention, n (%)5 (25)4 (31)>0.994 (19)5 (42)0.23
 Aortic growth rate (mm/year), median (IQR)1.5 (0.9–3.7)1.0 (0–4.0)0.331.5 (1.0–3.2)1.2 (0–4.3)0.49
 Follow-up duration (months), median (IQR)31 (25–32)27 (20–37)0.0830 (25–32)28 (22–31)0.35
VariablesDissection type
P-valueFL thrombosis status
P-value
rTAAD (n = 20)TBAD (n = 13)Patent (n = 21)Partially thrombosed (n = 12)
Age (years), median (IQR)55 (47–67)68 (65–74)0.0158 (51–68)68 (59–74)0.18
Male gender, n (%)13 (65)8 (62)>0.9912 (57)9 (75)0.46
Connective tissue disease, n (%)2 (10)0 (0)0.511 (5)1 (8)>0.99
Range of FL, n (%)
 Thoracic and abdominal aorta13 (65)7 (54)14 (67)6 (50)
 Thoracic aorta1 (5)6 (46)5 (24)2 (17)
 Abdominal aorta6 (30)0 (0)0.044 (19)4 (33)0.62
Baseline CT morphological information
 Maximum aortic diameter (mm), median (IQR)41.3 (33.7–49.8)40.0 (35.9–44.9)0.8338.1 (34.0–45.0)42.6 (37.5–55.3)0.12
 FL diameter (mm), median (IQR)24.1 (19.2–35.7)20.0 (15.6–27.0)0.2121.0 (16.1–31.0)23.1 (20.0–41.0)0.29
 Dominant entry diameter (mm), median (IQR)6.1 (4.5–10.4)8.0 (6.5–12.0)0.387.0 (4.7–11.0)6.8 (4.5–9.8)0.64
 Entry site at inner curvature, n (%)8 (40)8 (62)0.2911 (52)5 (42)0.72
 Partially thrombosed FL, n (%)5 (25)7 (54)0.14
Clinical outcomes after 4D flow MRI evaluation
 Rupture, n (%)1 (5)1 (8)>0.991 (5)1 (8)>0.99
 Prophylactic intervention, n (%)5 (25)4 (31)>0.994 (19)5 (42)0.23
 Aortic growth rate (mm/year), median (IQR)1.5 (0.9–3.7)1.0 (0–4.0)0.331.5 (1.0–3.2)1.2 (0–4.3)0.49
 Follow-up duration (months), median (IQR)31 (25–32)27 (20–37)0.0830 (25–32)28 (22–31)0.35

4D flow MRI: four-dimensional flow magnetic resonance imaging; CT: computed tomography; FL: false lumen; IQR: interquartile range; rTAAD: repaired type A aortic dissection; TBAD: type B aortic dissection.

Table 1:
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Demographics and clinical patient characteristics

VariablesDissection type
P-valueFL thrombosis status
P-value
rTAAD (n = 20)TBAD (n = 13)Patent (n = 21)Partially thrombosed (n = 12)
Age (years), median (IQR)55 (47–67)68 (65–74)0.0158 (51–68)68 (59–74)0.18
Male gender, n (%)13 (65)8 (62)>0.9912 (57)9 (75)0.46
Connective tissue disease, n (%)2 (10)0 (0)0.511 (5)1 (8)>0.99
Range of FL, n (%)
 Thoracic and abdominal aorta13 (65)7 (54)14 (67)6 (50)
 Thoracic aorta1 (5)6 (46)5 (24)2 (17)
 Abdominal aorta6 (30)0 (0)0.044 (19)4 (33)0.62
Baseline CT morphological information
 Maximum aortic diameter (mm), median (IQR)41.3 (33.7–49.8)40.0 (35.9–44.9)0.8338.1 (34.0–45.0)42.6 (37.5–55.3)0.12
 FL diameter (mm), median (IQR)24.1 (19.2–35.7)20.0 (15.6–27.0)0.2121.0 (16.1–31.0)23.1 (20.0–41.0)0.29
 Dominant entry diameter (mm), median (IQR)6.1 (4.5–10.4)8.0 (6.5–12.0)0.387.0 (4.7–11.0)6.8 (4.5–9.8)0.64
 Entry site at inner curvature, n (%)8 (40)8 (62)0.2911 (52)5 (42)0.72
 Partially thrombosed FL, n (%)5 (25)7 (54)0.14
Clinical outcomes after 4D flow MRI evaluation
 Rupture, n (%)1 (5)1 (8)>0.991 (5)1 (8)>0.99
 Prophylactic intervention, n (%)5 (25)4 (31)>0.994 (19)5 (42)0.23
 Aortic growth rate (mm/year), median (IQR)1.5 (0.9–3.7)1.0 (0–4.0)0.331.5 (1.0–3.2)1.2 (0–4.3)0.49
 Follow-up duration (months), median (IQR)31 (25–32)27 (20–37)0.0830 (25–32)28 (22–31)0.35
VariablesDissection type
P-valueFL thrombosis status
P-value
rTAAD (n = 20)TBAD (n = 13)Patent (n = 21)Partially thrombosed (n = 12)
Age (years), median (IQR)55 (47–67)68 (65–74)0.0158 (51–68)68 (59–74)0.18
Male gender, n (%)13 (65)8 (62)>0.9912 (57)9 (75)0.46
Connective tissue disease, n (%)2 (10)0 (0)0.511 (5)1 (8)>0.99
Range of FL, n (%)
 Thoracic and abdominal aorta13 (65)7 (54)14 (67)6 (50)
 Thoracic aorta1 (5)6 (46)5 (24)2 (17)
 Abdominal aorta6 (30)0 (0)0.044 (19)4 (33)0.62
Baseline CT morphological information
 Maximum aortic diameter (mm), median (IQR)41.3 (33.7–49.8)40.0 (35.9–44.9)0.8338.1 (34.0–45.0)42.6 (37.5–55.3)0.12
 FL diameter (mm), median (IQR)24.1 (19.2–35.7)20.0 (15.6–27.0)0.2121.0 (16.1–31.0)23.1 (20.0–41.0)0.29
 Dominant entry diameter (mm), median (IQR)6.1 (4.5–10.4)8.0 (6.5–12.0)0.387.0 (4.7–11.0)6.8 (4.5–9.8)0.64
 Entry site at inner curvature, n (%)8 (40)8 (62)0.2911 (52)5 (42)0.72
 Partially thrombosed FL, n (%)5 (25)7 (54)0.14
Clinical outcomes after 4D flow MRI evaluation
 Rupture, n (%)1 (5)1 (8)>0.991 (5)1 (8)>0.99
 Prophylactic intervention, n (%)5 (25)4 (31)>0.994 (19)5 (42)0.23
 Aortic growth rate (mm/year), median (IQR)1.5 (0.9–3.7)1.0 (0–4.0)0.331.5 (1.0–3.2)1.2 (0–4.3)0.49
 Follow-up duration (months), median (IQR)31 (25–32)27 (20–37)0.0830 (25–32)28 (22–31)0.35

4D flow MRI: four-dimensional flow magnetic resonance imaging; CT: computed tomography; FL: false lumen; IQR: interquartile range; rTAAD: repaired type A aortic dissection; TBAD: type B aortic dissection.

The median prospective follow-up duration after 4D flow MRI scan was 29 (IQR 24–32, range 11–37) months. During the follow-up, 2 (6%) patients died from aortic rupture and 9 (27%) patients underwent prophylactic intervention because of aortic growth or refractory symptoms.

Quantitative haemodynamic analysis

Haemodynamic parameters in 4D flow MRI are summarized in Table 2. Overall median gross flow, average velocity and regurgitant fraction in the TL were 39.8 (IQR 25.5–54.1, range 9.7–97.5) ml/s, 8.8 (IQR 6.8–12.7, range 4.2–21.2) cm/s and 15.8 (IQR 8.8–22.3%, range 3.1–40.9%), while those in the FL were 25.5 (IQR 10.4–47.2, range 4.4–117.5) ml/s, 4.2 (IQR 2.7–5.7, range 0.9–9.9) cm/s and 64.1 (IQR 49.0–81.4%, range 18.2–96.3%), respectively. These data illustrate that fast forward flow was dominant in the TL, while slow backward flow was common in the FL. A comparison analysis revealed that rTAAD showed a higher TL average velocity relative to TBAD [12.7 (IQR 7.1–21.2) vs 8.1 (IQR 6.5–10.9) cm/s; P = 0.04]. Patent FL exhibited a higher FL average velocity relative to partially thrombosed FL [4.7 (IQR 3.3–5.9) vs 3.0 (IQR 2.2–4.8) cm/s; P = 0.03].

Table 2:
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Haemodynamic comparison in 4D flow MRI

VariablesDissection type
P-valueFL thrombosis status
P-value
rTAAD (n = 20)TBAD (n = 13)Patent (n = 21)Partially thrombosed (n = 12)
Quantitative haemodynamics of the TL, median (IQR)
 TL gross flow (ml/s)48.7 (19.3–55.5)35.4 (34.0–46.2)0.8147.4 (23.3–59.5)39.5 (32.7–47.4)0.57
 TL average velocity (cm/s)12.7 (7.1–21.2)8.1 (6.5–10.9)0.049.0 (7.2–13.8)8.4 (6.5–11.1)0.39
 TL regurgitant fraction (%)17.5 (8.6–22.2)15.6 (9.1–22.3)0.6017.5 (9.1–25.8)11.7 (8.1–16.1)0.08
Quantitative haemodynamics of the FL, median (IQR)
 FL gross flow (ml/s)30.1 (13.8–66.7)19.1 (10.4–31.4)0.1925.5 (15.4–65.2)22.7 (9.7–31.9)0.26
 FL average velocity (cm/s)4.4 (3.2–5.7)3.3 (2.3–5.4)0.354.7 (3.3–5.9)3.0 (2.2–4.8)0.03
 FL regurgitant fraction (%)61.2 (48.8–68.4)75.8 (52.5–86.4)0.2762.4 (46.6–79.8)72.4 (59.6–82.6)0.18
Visual grading of turbulent flow in the FL
 Helix grade = 0, n (%)10 (50)5 (39)12 (57)3 (25)
 Helix grade = 1, n (%)3 (15)3 (23)1 (5)5 (42)
 Helix grade = 2, n (%)7 (35)5 (39)0.738 (38)4 (33)0.03
 Helix grade (0–2), median (IQR)0.5 (0–2)1.0 (0–2)0.650 (0–2)1 (0.75–2)0.37
 Vortex grade = 0, n (%)10 (50)5 (39)10 (48)5 (42)
 Vortex grade = 1, n (%)2 (10)2 (15)0 (0)4 (33)
 Vortex grade = 2, n (%)8 (40)6 (46)0.7911 (52)3 (25)0.02
 Vortex grade (0–2), median (IQR)0.5 (0–2)1.0 (0–2)0.612 (0–2)1 (0–1.25)0.57
VariablesDissection type
P-valueFL thrombosis status
P-value
rTAAD (n = 20)TBAD (n = 13)Patent (n = 21)Partially thrombosed (n = 12)
Quantitative haemodynamics of the TL, median (IQR)
 TL gross flow (ml/s)48.7 (19.3–55.5)35.4 (34.0–46.2)0.8147.4 (23.3–59.5)39.5 (32.7–47.4)0.57
 TL average velocity (cm/s)12.7 (7.1–21.2)8.1 (6.5–10.9)0.049.0 (7.2–13.8)8.4 (6.5–11.1)0.39
 TL regurgitant fraction (%)17.5 (8.6–22.2)15.6 (9.1–22.3)0.6017.5 (9.1–25.8)11.7 (8.1–16.1)0.08
Quantitative haemodynamics of the FL, median (IQR)
 FL gross flow (ml/s)30.1 (13.8–66.7)19.1 (10.4–31.4)0.1925.5 (15.4–65.2)22.7 (9.7–31.9)0.26
 FL average velocity (cm/s)4.4 (3.2–5.7)3.3 (2.3–5.4)0.354.7 (3.3–5.9)3.0 (2.2–4.8)0.03
 FL regurgitant fraction (%)61.2 (48.8–68.4)75.8 (52.5–86.4)0.2762.4 (46.6–79.8)72.4 (59.6–82.6)0.18
Visual grading of turbulent flow in the FL
 Helix grade = 0, n (%)10 (50)5 (39)12 (57)3 (25)
 Helix grade = 1, n (%)3 (15)3 (23)1 (5)5 (42)
 Helix grade = 2, n (%)7 (35)5 (39)0.738 (38)4 (33)0.03
 Helix grade (0–2), median (IQR)0.5 (0–2)1.0 (0–2)0.650 (0–2)1 (0.75–2)0.37
 Vortex grade = 0, n (%)10 (50)5 (39)10 (48)5 (42)
 Vortex grade = 1, n (%)2 (10)2 (15)0 (0)4 (33)
 Vortex grade = 2, n (%)8 (40)6 (46)0.7911 (52)3 (25)0.02
 Vortex grade (0–2), median (IQR)0.5 (0–2)1.0 (0–2)0.612 (0–2)1 (0–1.25)0.57

4D flow MRI: four-dimensional flow magnetic resonance imaging; FL: false lumen; IQR: interquartile range; rTAAD: repaired type A aortic dissection; TBAD: type B aortic dissection; TL: true lumen.

Table 2:
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Haemodynamic comparison in 4D flow MRI

VariablesDissection type
P-valueFL thrombosis status
P-value
rTAAD (n = 20)TBAD (n = 13)Patent (n = 21)Partially thrombosed (n = 12)
Quantitative haemodynamics of the TL, median (IQR)
 TL gross flow (ml/s)48.7 (19.3–55.5)35.4 (34.0–46.2)0.8147.4 (23.3–59.5)39.5 (32.7–47.4)0.57
 TL average velocity (cm/s)12.7 (7.1–21.2)8.1 (6.5–10.9)0.049.0 (7.2–13.8)8.4 (6.5–11.1)0.39
 TL regurgitant fraction (%)17.5 (8.6–22.2)15.6 (9.1–22.3)0.6017.5 (9.1–25.8)11.7 (8.1–16.1)0.08
Quantitative haemodynamics of the FL, median (IQR)
 FL gross flow (ml/s)30.1 (13.8–66.7)19.1 (10.4–31.4)0.1925.5 (15.4–65.2)22.7 (9.7–31.9)0.26
 FL average velocity (cm/s)4.4 (3.2–5.7)3.3 (2.3–5.4)0.354.7 (3.3–5.9)3.0 (2.2–4.8)0.03
 FL regurgitant fraction (%)61.2 (48.8–68.4)75.8 (52.5–86.4)0.2762.4 (46.6–79.8)72.4 (59.6–82.6)0.18
Visual grading of turbulent flow in the FL
 Helix grade = 0, n (%)10 (50)5 (39)12 (57)3 (25)
 Helix grade = 1, n (%)3 (15)3 (23)1 (5)5 (42)
 Helix grade = 2, n (%)7 (35)5 (39)0.738 (38)4 (33)0.03
 Helix grade (0–2), median (IQR)0.5 (0–2)1.0 (0–2)0.650 (0–2)1 (0.75–2)0.37
 Vortex grade = 0, n (%)10 (50)5 (39)10 (48)5 (42)
 Vortex grade = 1, n (%)2 (10)2 (15)0 (0)4 (33)
 Vortex grade = 2, n (%)8 (40)6 (46)0.7911 (52)3 (25)0.02
 Vortex grade (0–2), median (IQR)0.5 (0–2)1.0 (0–2)0.612 (0–2)1 (0–1.25)0.57
VariablesDissection type
P-valueFL thrombosis status
P-value
rTAAD (n = 20)TBAD (n = 13)Patent (n = 21)Partially thrombosed (n = 12)
Quantitative haemodynamics of the TL, median (IQR)
 TL gross flow (ml/s)48.7 (19.3–55.5)35.4 (34.0–46.2)0.8147.4 (23.3–59.5)39.5 (32.7–47.4)0.57
 TL average velocity (cm/s)12.7 (7.1–21.2)8.1 (6.5–10.9)0.049.0 (7.2–13.8)8.4 (6.5–11.1)0.39
 TL regurgitant fraction (%)17.5 (8.6–22.2)15.6 (9.1–22.3)0.6017.5 (9.1–25.8)11.7 (8.1–16.1)0.08
Quantitative haemodynamics of the FL, median (IQR)
 FL gross flow (ml/s)30.1 (13.8–66.7)19.1 (10.4–31.4)0.1925.5 (15.4–65.2)22.7 (9.7–31.9)0.26
 FL average velocity (cm/s)4.4 (3.2–5.7)3.3 (2.3–5.4)0.354.7 (3.3–5.9)3.0 (2.2–4.8)0.03
 FL regurgitant fraction (%)61.2 (48.8–68.4)75.8 (52.5–86.4)0.2762.4 (46.6–79.8)72.4 (59.6–82.6)0.18
Visual grading of turbulent flow in the FL
 Helix grade = 0, n (%)10 (50)5 (39)12 (57)3 (25)
 Helix grade = 1, n (%)3 (15)3 (23)1 (5)5 (42)
 Helix grade = 2, n (%)7 (35)5 (39)0.738 (38)4 (33)0.03
 Helix grade (0–2), median (IQR)0.5 (0–2)1.0 (0–2)0.650 (0–2)1 (0.75–2)0.37
 Vortex grade = 0, n (%)10 (50)5 (39)10 (48)5 (42)
 Vortex grade = 1, n (%)2 (10)2 (15)0 (0)4 (33)
 Vortex grade = 2, n (%)8 (40)6 (46)0.7911 (52)3 (25)0.02
 Vortex grade (0–2), median (IQR)0.5 (0–2)1.0 (0–2)0.612 (0–2)1 (0–1.25)0.57

4D flow MRI: four-dimensional flow magnetic resonance imaging; FL: false lumen; IQR: interquartile range; rTAAD: repaired type A aortic dissection; TBAD: type B aortic dissection; TL: true lumen.

Turbulence visualization analysis

Helices were observed in 18 (55%) patients. Specifically, grade 1 helices were observed in 6 (18%) patients and grade 2 helices were observed in 12 (36%) patients. Vortices were observed in 18 (55%) patients. Grade 1 vortices were observed in 4 (12%) patients and grade 2 vortices 14 (42%) patients. In the group comparison analysis, the median grades of both helix and vortex were not significantly different according to dissection type or FL thrombosis status.

Correlation of flow turbulence with haemodynamic and morphological factors

Figure 4 shows box plots of the haemodynamic and morphological parameters within each helix or vortex grade in the FL. Helix grade shows a significant correlation with FL gross flow (rS = 0.55, P < 0.001), FL average velocity (rS = 0.45, P = 0.008), FL diameter (rS = 0.50, P = 0.003) and dominant entry diameter (rS = 0.37, P = 0.03). Similarly, vortex grade shows a significant correlation with FL gross flow (rS = 0.70, P < 0.001), FL average velocity (rS = 0.67, P < 0.001), FL diameter (rS = 0.43, P = 0.01) and dominant entry diameter (rS = 0.50, P = 0.003). There was no significant correlation between flow turbulence with FL regurgitant fraction or aortic growth rate.

Box plots of haemodynamic and morphological parameters of (A) each helix grade and (B) each vortex grade. The centreline denotes the median value (50th percentile), while the box contains the 25th to 75th percentiles of dataset. The whiskers mark the 10th and 90th percentiles, and values beyond these upper and lower bounds are considered outliers, marked with dots. FL: false lumen; rS: Spearman correlation coefficient.
Figure 4:

Box plots of haemodynamic and morphological parameters of (A) each helix grade and (B) each vortex grade. The centreline denotes the median value (50th percentile), while the box contains the 25th to 75th percentiles of dataset. The whiskers mark the 10th and 90th percentiles, and values beyond these upper and lower bounds are considered outliers, marked with dots. FL: false lumen; rS: Spearman correlation coefficient.

Open in new tabDownload slide

Video 1:

Representative pathline images of flow dynamics in the false lumen with helices, vortices, low-volume laminar flow and high-volume laminar flow.

Morphological and haemodynamic factors affecting complications

Comparison analysis regarding complications is summarized in Table 3. Patients with complications exhibited greater maximal aortic diameter [54.7 (IQR 46.0–55.8) vs 37.6 (IQR 34.0–44.1) mm; P < 0.001], FL diameter [40.4 (IQR 28.7–44.0) vs 20.0 (IQR 15.9–37.8) mm; P < 0.001] and dominant entry diameter [11.5 (IQR 8.9–12.6) vs 5.7 (IQR 4.1–7.3) mm; P < 0.001]. In haemodynamic comparison, patients with complications showed higher FL gross flow [41.7 (IQR 29.1–59.7) vs 17.7 (IQR 9.0–42.0) ml/s; P = 0.01], helix grade [2 (IQR 1.25–2) vs 0 (IQR 0–1); P = 0.001] and vortex grade [2 (IQR 1–2) vs 0 (IQR 0–2); P = 0.01]. Partially thrombosed FL was more frequently observed in patients with complications (6/10, 60%) compared to patients without complication (6/22, 27%), but it was not statistically significant (P = 0.11).

Table 3:
Open in new tab

Comparison analysis regarding complications

VariablesRupture or intervention (n = 11)No complication (n = 22)P-value
Morphological factors in baseline CT
 Maximal aortic diameter (mm), median (IQR)54.7 (46.0–55.8)37.6 (34.0–44.1)<0.001
 FL diameter (mm), median (IQR)40.4 (28.7–44.0)20.0 (15.9–37.8)<0.001
 Dominant entry diameter (mm), median (IQR)11.5 (8.9–12.6)5.7 (4.1–7.3)<0.001
 Entry site at inner curvature, n (%)3 (30)13 (59)0.26
 Partially thrombosed FL, n (%)6 (60)6 (27)0.11
 Aortic growth rate (mm/year), median (IQR)4.8 (3.1–5.8)1.0 (0.0–1.5)0.002
Haemodynamic factors in 4D flow MRI
 TL gross flow (ml/s), median (IQR)40.8 (26.9–49.3)35.4 (26.1–54.3)0.86
 TL average velocity (cm/s), median (IQR)8.8 (5.8–12.0)8.8 (6.8–13.5)0.52
 TL regurgitant fraction (%), median (IQR)11.7 (8.9–15.6)17.5 (8.7–24.3)0.22
 FL gross flow (ml/s), median (IQR)41.7 (29.1–59.7)17.7 (9.0–42.0)0.01
 FL average velocity (cm/s), median (IQR)5.1 (3.6–5.7)3.8 (2.4–5.4)0.29
 FL regurgitant fraction (%), median (IQR)56.3 (46.6–67.8)64.5 (51.9–84.0)0.18
 Helix grade in the FL (0–2), median (IQR)2 (1.25–2)0 (0–1)0.001
 Vortex grade in the FL (0–2), median (IQR)2 (1–2)0 (0–2)0.01
VariablesRupture or intervention (n = 11)No complication (n = 22)P-value
Morphological factors in baseline CT
 Maximal aortic diameter (mm), median (IQR)54.7 (46.0–55.8)37.6 (34.0–44.1)<0.001
 FL diameter (mm), median (IQR)40.4 (28.7–44.0)20.0 (15.9–37.8)<0.001
 Dominant entry diameter (mm), median (IQR)11.5 (8.9–12.6)5.7 (4.1–7.3)<0.001
 Entry site at inner curvature, n (%)3 (30)13 (59)0.26
 Partially thrombosed FL, n (%)6 (60)6 (27)0.11
 Aortic growth rate (mm/year), median (IQR)4.8 (3.1–5.8)1.0 (0.0–1.5)0.002
Haemodynamic factors in 4D flow MRI
 TL gross flow (ml/s), median (IQR)40.8 (26.9–49.3)35.4 (26.1–54.3)0.86
 TL average velocity (cm/s), median (IQR)8.8 (5.8–12.0)8.8 (6.8–13.5)0.52
 TL regurgitant fraction (%), median (IQR)11.7 (8.9–15.6)17.5 (8.7–24.3)0.22
 FL gross flow (ml/s), median (IQR)41.7 (29.1–59.7)17.7 (9.0–42.0)0.01
 FL average velocity (cm/s), median (IQR)5.1 (3.6–5.7)3.8 (2.4–5.4)0.29
 FL regurgitant fraction (%), median (IQR)56.3 (46.6–67.8)64.5 (51.9–84.0)0.18
 Helix grade in the FL (0–2), median (IQR)2 (1.25–2)0 (0–1)0.001
 Vortex grade in the FL (0–2), median (IQR)2 (1–2)0 (0–2)0.01

4D flow MRI: four-dimensional flow magnetic resonance imaging; CT: computed tomography; FL: false lumen; IQR: interquartile range; TL: true lumen.

Table 3:
Open in new tab

Comparison analysis regarding complications

VariablesRupture or intervention (n = 11)No complication (n = 22)P-value
Morphological factors in baseline CT
 Maximal aortic diameter (mm), median (IQR)54.7 (46.0–55.8)37.6 (34.0–44.1)<0.001
 FL diameter (mm), median (IQR)40.4 (28.7–44.0)20.0 (15.9–37.8)<0.001
 Dominant entry diameter (mm), median (IQR)11.5 (8.9–12.6)5.7 (4.1–7.3)<0.001
 Entry site at inner curvature, n (%)3 (30)13 (59)0.26
 Partially thrombosed FL, n (%)6 (60)6 (27)0.11
 Aortic growth rate (mm/year), median (IQR)4.8 (3.1–5.8)1.0 (0.0–1.5)0.002
Haemodynamic factors in 4D flow MRI
 TL gross flow (ml/s), median (IQR)40.8 (26.9–49.3)35.4 (26.1–54.3)0.86
 TL average velocity (cm/s), median (IQR)8.8 (5.8–12.0)8.8 (6.8–13.5)0.52
 TL regurgitant fraction (%), median (IQR)11.7 (8.9–15.6)17.5 (8.7–24.3)0.22
 FL gross flow (ml/s), median (IQR)41.7 (29.1–59.7)17.7 (9.0–42.0)0.01
 FL average velocity (cm/s), median (IQR)5.1 (3.6–5.7)3.8 (2.4–5.4)0.29
 FL regurgitant fraction (%), median (IQR)56.3 (46.6–67.8)64.5 (51.9–84.0)0.18
 Helix grade in the FL (0–2), median (IQR)2 (1.25–2)0 (0–1)0.001
 Vortex grade in the FL (0–2), median (IQR)2 (1–2)0 (0–2)0.01
VariablesRupture or intervention (n = 11)No complication (n = 22)P-value
Morphological factors in baseline CT
 Maximal aortic diameter (mm), median (IQR)54.7 (46.0–55.8)37.6 (34.0–44.1)<0.001
 FL diameter (mm), median (IQR)40.4 (28.7–44.0)20.0 (15.9–37.8)<0.001
 Dominant entry diameter (mm), median (IQR)11.5 (8.9–12.6)5.7 (4.1–7.3)<0.001
 Entry site at inner curvature, n (%)3 (30)13 (59)0.26
 Partially thrombosed FL, n (%)6 (60)6 (27)0.11
 Aortic growth rate (mm/year), median (IQR)4.8 (3.1–5.8)1.0 (0.0–1.5)0.002
Haemodynamic factors in 4D flow MRI
 TL gross flow (ml/s), median (IQR)40.8 (26.9–49.3)35.4 (26.1–54.3)0.86
 TL average velocity (cm/s), median (IQR)8.8 (5.8–12.0)8.8 (6.8–13.5)0.52
 TL regurgitant fraction (%), median (IQR)11.7 (8.9–15.6)17.5 (8.7–24.3)0.22
 FL gross flow (ml/s), median (IQR)41.7 (29.1–59.7)17.7 (9.0–42.0)0.01
 FL average velocity (cm/s), median (IQR)5.1 (3.6–5.7)3.8 (2.4–5.4)0.29
 FL regurgitant fraction (%), median (IQR)56.3 (46.6–67.8)64.5 (51.9–84.0)0.18
 Helix grade in the FL (0–2), median (IQR)2 (1.25–2)0 (0–1)0.001
 Vortex grade in the FL (0–2), median (IQR)2 (1–2)0 (0–2)0.01

4D flow MRI: four-dimensional flow magnetic resonance imaging; CT: computed tomography; FL: false lumen; IQR: interquartile range; TL: true lumen.

DISCUSSION

This study utilized multi-VENC 4D flow MRI to investigate the relationship between haemodynamics factors and their impact on turbulence formation in the FL. We report that visual grades of turbulence showed a significant correlation with flow volume and velocity. A comparison analysis regarding complications revealed that patients with late complications exhibited higher-volume flow and higher-grades of turbulence in their FL.

The flow dynamic mechanism of turbulence formation in the FL

Haemodynamic characteristics inside the FL are patient-specific, differing according to the location and size of the intimal tears [5, 16]. In the FL of these patients, certain flow dynamic conditions generate turbulent flow, which is known to cause negative remodelling [6, 7, 17]. Based upon the current results, flow volume and velocity are responsible for turbulence formation in the FL, which may cause negative remodelling of the dissected aorta. Previous flow analyses reported that helices are likely secondary to an asymmetric high-velocity flow jet associated with bicuspid aortic valve [17] or obstructed left ventricular outflow [14]. The mechanism of helix formation is thought to result from an asymmetric high-flow jet impinging the vessel wall of the proximal aorta and folding spirally on the endo-luminal surfaces [18]. In addition, this flow abnormality was reported to cause altered wall shear stress, which may trigger maladaptive vascular remodelling [17, 19]. Using the pathline visualization analysis, similar flow abnormalities were observed at the entry tear and the subsequent FL. An asymmetric high-flow jet passing through the entry tear was depicted and followed by helices folding spirally along the endo-luminal surface of the FL (Fig. 3). This finding suggests that flow alterations at the entry tear, with secondary turbulence in the FL, may cause negative remodelling by a similar mechanism as the proximal aorta affected by the bicuspid aortic valve.

Anatomical factors affecting turbulence formation in the FL

Another potential mechanism for turbulence formation was revealed by our novel analysis. Pathline visualization revealed that both helices and vortices arise from the dominant entry tear in the FL and change to low-velocity flow towards the ends (Fig. 2A and B). Gulan et al. [20] indicated that vortices are developed because of flow separation due to a sudden increase in diameter. Their study also reported that a sudden diameter increase is responsible for the irreversible energy loss and wall tension. The aforementioned mechanism is considered to be applicable to the FL. According to the current evaluation, the median dominant entry diameter was 7.0 (IQR 4.7–11.0) mm while the median FL diameter was 22.0 (IQR 16.9–31.0) mm, which indicates that blood flow passing through the entry tear induces flow separation with a sudden increase in diameter, therefore turbulence was observed near the entry tear in the FL. In addition, the current results showed significant correlation of turbulence grades with FL diameter and dominant entry diameter. We speculate that the large entry tear may contribute to high-volume inflow to the FL, flow turbulence is generated by the sudden diameter increase, and subsequently the elevated wall tension cause FL dilation. Conversely, turbulence does not occur when the entry tear is as large as the FL cross-section without diameter increase. Figure 2D depicts a case of laminar flow inside the FL without any turbulence. This patient underwent total arch replacement distally anastomosed in a double barrel fashion. During the surgery, the dissection flap of the descending aorta was longitudinally incised with a longer distance than the length of the FL cross-section. As a caveat for this technique, it should be indicated only in cases where both the TL and FL are responsible for critical aortic branch flow downstream. Generally, the large entry tear may cause high-volume inflow and elevated wall tension of the FL when the outflow is impaired due to small re-entry or partial thrombosis [16]. If the downstream perfusion of the FL is highly demanded like the case of Fig. 2D, FL flow pattern becomes TL-like laminar flow.

Risk factors affecting complication

Comparison analysis regarding complications (Table 3) indicates that altered haemodynamics was not the only reason for poor outcomes. Aortic diameter, FL diameter and dominant entry diameter were significantly higher in patients with complications, as described previously [2, 8, 21]. Though the cause-and-effect relationship between FL dilation and altered haemodynamics still remains controversial, the current results brought us to the hypothesis that altered haemodynamics may cause the FL pressurization which is regarded as the trigger of post-dissection aneurysm formation [3, 16]. Among the 11 patients who developed late complications, all (100%) subjects exhibited both helices and vortices in their FL in 4D flow MRI analysis, while 4 (36%) patients presented normal aortic diameter (<50 mm) at the baseline CT. A previous flow study also suggested that the altered flow pattern is not secondary to a dilated aorta and may be implicated in the pathogenesis of aneurysmal formation [19]. These findings indicate that altered flow pattern potentially predicts aneurysmal formation more sensitively than morphological parameters such as baseline aortic diameter.

Flow characteristics of the surgically repaired aorta

Most rTAAD patients presented flow acceleration in their replaced graft (Fig. 2B–D), which was not observed in TBAD (Fig. 2A). It is assumed that non-compliant graft, graft kink, or using an inner felt strip at the anastomosis site are the main cause of the distal flow acceleration, resulting in the faster TL flow observed in rTAAD. Jarvis et al. [22] presented a similar hypothesis, as they suspected the elevated flow parameters are the result of prior surgery. They also indicated that the elevated flow metrics will lead to higher rates of aneurysm, however, a detailed investigation will be required to solidify these claims.

Limitations

Our study has several limitations. First, validity of comparing rTAAD and TBAD as an equal cohort is a limitation. rTAAD patients underwent primary entry resection while TBAD patients did not, therefore the haemodynamic conditions in the FL might be different between them. Interestingly, the present cohort showed similar flow dynamic profiles between rTAAD and TBAD. The recruited rTAAD patients showed patent FL ranging from the thoracic to abdominal aorta due to multiple remnant intimal tears located distally to the replaced graft, and exhibited similar flow dynamic profiles to TBAD. Thus, we concluded that the recruited rTAAD and TBAD cohorts could be analysed equally. Second, the interval from diagnosis to 4D flow MRI scan varied with the median interval of 9 (IQR 4–20, range 1–86) months. Several patients had already exhibited an enlarging aorta at the time of 4D flow MRI evaluation, and underwent prophylactic intervention in their early phase of the follow-up period. The variance in timing of MRI scan prevented exploring the correlation between flow turbulence and aortic growth rate (mm/year). Lastly, the semi-quantitative grading system of helices and vortices is an observer-dependent subjective evaluation method which is not ideal. Development of an automated quantitative flow evaluation of helices and vortices will be the subject of future efforts. Automating the process will remove user bias, user variability and provide more precise diagnostic groups for treatment.

CONCLUSION

In patients with chronic aortic dissection, multi-VENC 4D flow MRI analysis revealed that flow turbulence depends on volume and velocity in the FL. In addition, higher flow volume and higher turbulence grade in the FL had been observed in patients who suffered from aortic rupture or who underwent prophylactic intervention. Patients with high-volume flow in their FL may be at higher risk of late complications resulting from turbulence-related negative remodelling, therefore close follow-up and aggressive prophylactic intervention may improve their survival.

Funding

This work was supported by the JSPS KAKENHI [17K18160, 19K17151 and 19K08186], research grants from Fukuda Foundation for Medical Technology and Terumo Foundation for Life Sciences and Arts.

Conflict of interest: none declared.

Author contributions

Kenichiro Takahashi: Conceptualization; Data curation; Methodology; Project administration; Visualization; Writing—original draft. Tetsuro Sekine: Conceptualization; Data curation; Funding acquisition; Investigation; Methodology; Supervision; Validation; Visualization; Writing—review & editing. Yasuo Miyagi: Supervision; Validation; Writing—review & editing. Sayaka Shirai: Data curation; Validation; Visualization. Toshiaki Otsuka: Formal analysis. Shinichiro Kumita: Supervision. Yosuke Ishii: Conceptualization; Supervision; Writing—review & editing.

Reviewer information

European Journal of Cardio-Thoracic Surgery thanks Luca Bertoglio, Mario Lescan, Gabriele Piffaretti and the other, anonymous reviewer(s) for their contribution to the peer review process of this article.

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ABBREVIATIONS

     
  • 4D flow MRI

    Four-dimensional flow magnetic resonance imaging

    •  
  • CT

    Computed tomography

    •  
  • FL

    False lumen

    •  
  • IQR

    Interquartile range

    •  
  • TBAD

    Type B aortic dissection

    •  
  • TL

    True lumen

    •  
  • rTAAD

    Repaired type A aortic dissection

    •  
  • VENC

    Velocity encoding

© The Author(s) 2021. Published by Oxford University Press on behalf of the European Association for Cardio-Thoracic Surgery. All rights reserved.
This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://dbpia.nl.go.kr/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
Topic:
Subject
Aortic Disorders
Issue Section:
CONVENTIONAL AORTIC SURGERY
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