Evaluation of the relationship between pulmonary artery volume and quantitative voxel based flow parameters in patients with and without pulmonary hypertension using 4D flow MRI

doi:10.21203/rs.3.rs-3952349/v1

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Research Article

Evaluation of the relationship between pulmonary artery volume and quantitative voxel based flow parameters in patients with and without pulmonary hypertension using 4D flow MRI

https://doi.org/10.21203/rs.3.rs-3952349/v1

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Purpose

Four-dimensional (4D) magnetic resonance imaging (MRI) is used to determine abnormal blood flow in patients with pulmonary hypertension (PH), but the relationship between abnormal blood flow and pulmonary artery volume is unclear. This study aimed to quantify pulmonary artery volume and flow parameters using 4D flow MRI, and to evaluate their relationship in patients with PH and in those without PH.

Methods

We retrospectively studied 177 patients at our institution who underwent cardiac contrast-enhanced MRI to investigate cardiomyopathy or cardiac dysfunction. The patients were divided into the non-PH group (n = 162) with systolic pulmonary artery pressure < 39 mmHg and the PH group (n = 15) with systolic pulmonary artery pressure > 40 mmHg. We performed 4D flow MRI to quantitively assess volume, energy loss (EL), vorticity (Vor), and helicity (Hel) in the pulmonary artery.

Results

Pulmonary artery volume, EL average, Vor average, Hel right screw average, and Hel left screw average were significantly lower in the non-PH group than in the PH group (all p < 0.05). The pulmonary artery volume was significantly correlated with EL average (R = 0.4140, p < 0.0001), Vor average (R = 0.7561, p < 0.0001), and Hel right and left screw averages in the non-PH group (R = 0.5105, p < 0.0001; R = −0.5349, p < 0.0001, respectively). The pulmonary artery volume was significantly correlated with Vor average in the PH group (R= 0.6152, p = 0.0146). However, the pulmonary artery volume was not correlated with EL average or Hel right and left screw averages in the PH group.

Conclusion

EL and Hel may reflect PH in voxel-based evaluation of blood flow in the pulmonary artery.

heart failure

4D flow magnetic resonance imaging

pulmonary hypertension

pulmonary artery

Pulmonary hypertension (PH) is considered a rare hemodynamic condition, with an estimated prevalence of 15–50 cases/million adults including primary PH and secondary PH [1,2]. However, PH can affect approximately 1% of the global population in up to 10% of individuals aged older than 65 years, and in at least 50% of patients with heart failure [3]. PH is defined as a mean pulmonary artery pressure of ≥ 20 mmHg by right-sided heart catheterization (RHC) [4]. RHC remains the gold standard for the diagnosis of PH. However, recently, three-dimensional (3D) phase-contrast magnetic resonance imaging (MRI) (4D flow MRI) has been developed as a noninvasive method to quantitatively evaluate blood flow in PH [5,6]. Several studies have reported the ability of 4D flow MRI to detect and quantify PH based on the wall shear stress (WSS) [7,8] and vortical flow in the pulmonary artery [9-13]. However, the method of quantification using this technique is complicated. Quantification of blood flow parameters in the whole pulmonary artery between the non-PH group and PH group would be more clinically useful. Many studies have reported that flow patterns change in dilated vessels compared with normal vessels [14,15].

Patients with PH often have dilation of the central pulmonary artery from the pulmonary artery trunk to both main pulmonary arteries [16]. Therefore, we hypothesize that the volume of the pulmonary artery affects quantitative parameters of blood flow in the whole pulmonary artery. In this study, we hypothesized that pulmonary blood flow parameters are correlated with whole pulmonary artery volume in patients without PH and in those with PH. As a result, if there are parameters that are not related to volume in patients with PH, they may reflect features other than a dilated pulmonary artery due to PH. Because pulmonary artery volume can be measured by computed tomography, we consider that quantitatively measuring parameters related to PH other than pulmonary artery volume would be clinically useful. Therefore, this study aimed to quantify pulmonary artery volume and flow parameters using 4D flow MRI in patients without PH and in those with PH, and to make a clear distinction between these patient groups. Moreover, we aimed to investigate the relationship between flow parameters and pulmonary artery volume.

Patient population

Our institutional review board approved this study and waived the need for written informed consent because the study design was retrospective. From April 2020 to September 2022, 185 patients (113 men [61.1%] and 72 women [38.9%]; mean age [SD]: 55.3 [16.9] years) underwent cardiac contrast-enhanced MRI to investigate cardiomyopathy or cardiac dysfunction, and 185 patients also underwent 4D flow MRI. Before the 4D flow MRI results were analyzed, the patients were divided into two groups (non-PH and PH groups) on the basis of their echocardiographic results. Seven patients without echo data and one patient with tetralogy of Fallot postoperation were excluded from the study cohort. Therefore, this study included 177 consecutive patients in the final cohort. The patient cohort included 162 patients without PH (96 [59.3%] men and 66 [40.7%] women; mean age [SD]: 55.0 [17.1] years) and 15 patients with PH (14 [93.3%] men and 1 [6.7%] woman; mean age [SD]: 58.0 [13.5] years) (Table 1).

There was no significant difference in age or body mass index between the two groups in this study (p = 0.6583 and p = 0.8886). In contrast, there was a greater proportion of men in the PH group than in the non-PH group (p < 0.0001). All of these patients were identified in a retrospective review of medical records conducted at a single medical institution.

Echocardiographic estimation of pulmonary artery pressure

Within 1 week of cardiac MRI, experienced cardiologists with more than 5 years of experience in cardiac echo in our hospital performed echocardiographic examinations using a Toshiba Artida ultrasound machine (Toshiba Medical Systems Corp., Tochigi, Japan) with 2.5-MHz transducers. The results were digitally recorded.

In the absence of pulmonary flow obstruction, tricuspid regurgitation (TR) peak velocity is correlated with systolic pulmonary artery pressure (sPAP) as assessed by RHC. The TR gradient was measured by continuous wave Doppler velocity across the tricuspid valve in line with regurgitation flow. The modified Bernoulli equation (4 × [velocity of TR]²) was used to convert this velocity into a pressure gradient [17]. This gradient shows the difference in pressure between the right ventricle and right atrium and can be used as an estimate of right ventricular systolic pressure [18] when right atrial pressure (normal: 5–10 mmHg) is added to the derived gradient. This estimated sPAP was used to evaluate the likelihood of a patient having PH. We used sPAP to divide our patients into the non-PH group with sPAP < 39 mmHg and the PH group with sPAP > 40 mmHg [19]. We classified patients into these two groups on the basis of echocardiographic sPAP recordings performed by cardiologists in our hospital.

MRI

All patients were scanned using a 3.0-T scanner (MAGNETOM Vida; Siemens, Healthcare, Germany) with a 32-channel cardiac phased-array coil. The scanning parameters were as follows: repetition time/echo time/flip angle = 43 ms/3.04 ms/15 degrees, voxel resolution = 1.8 × 1.8 × 2.0 mm, bandwidth = 1532 Hz/Px, velocity encoding = 150 cm/s, time resolution = 19–24 phases/cardiac cycle, and scan time = approximately 10 min (with compressed sensing).

All images were recorded under free-breathing conditions during the usual cardiac MRI sequence 30 s after gadolinium 0.10 mmol/kg was administered.

MRI analysis

Pulmonary artery blood flow parameters were calculated for arbitrary regions within data sets comprising multislice sagittal planes from phase contrast three-axis cine images, magnitude images, and steady-state free procession cine images obtained from measurements using iTFlow (Cardio Flow Design Inc., Tokyo, Japan). One radiologist with 12 years of experience in reading cardiac MRI analyzed the MRI scans. The radiologist was blinded to the patients’ clinical conditions and investigated. Using the procession 3D cine image, the pulmonary artery trunk just above the pulmonary valve to the first bifurcation of both pulmonary was manually drawn in each phase. Another radiologist (28 years of experience in reading cardiac MRI then rechecked the borders of the pulmonary artery to ensure their accuracy. The mean pulmonary artery volume (cm³) was automatically calculated, and flow parameters were also automatically measured. We then investigated this mean pulmonary artery volume and flow parameters.

Flow parameters

Energy loss (EL) is a numerical indicator of the energy efficiency within a region of interest, and a high EL results in an increased cardiac load. EL has attracted attention as an indicator for predicting cardiac load in valvular disease, cardiomyopathy, and congenital heart disease [20].

Using the 4D flow MRI data, the EL per voxel was calculated as follows:

where I and j are the coordinates of the 3D Euclidean space, and µ is blood viscosity. The spatial differential of the blood flow velocity was calculated by the central difference.

In this study, EL average was defined as the average value of all phases of EL in one cardiac cycle. EL maximum was defined as EL in the phase with the highest value among all phases in one cardiac cycle. EL minimum was defined as EL in the phase with the lowest value among all phases in one cardiac cycle.

The average, maximum, and minimum vorticity (Vor) and helicity (Hel) described below are also the average, maximum, and minimum values among all phases in one cardiac cycle.

Vor is an index that quantifies the strength of the swirl of the velocity vector. High Vor values may increase the stress on local blood vessel walls, promoting aneurysmal growth, and may also alter local vascular protective mechanisms, leading to a reduction in WSS [21,22].

Using the 4D flow voxel data, the Vor was calculated in this study as follows:

where x, y and z are the coordinate of 3D Eulerian and u, v and w are the blood flow velocity component in x, y and z direction.

Hel is an indicator of helical flow, which is corkscrew-like motion in the principal flow direction. Hel in the thoracic aorta may be exacerbated by common pathologies, such as aortic dilatation, aortic valve stenosis, and bicuspid aortic valve [14,23].

Using the 4D flow voxel data, the Hel was calculated in this study as follows:

where ω is the vorticity vector (𝑟𝑜𝑡(𝑼)), and 𝑼 is the blood flow velocity vector.

Right screw and left screw, average, maximum, and minimum values were calculated for Hel.

Statistical analysis

Prism for Windows (version 8.3.0; GraphPad, San Diego, CA) was used for all statistical analyses. We used the D’Agostino-Pearson test to assess the normality of the data, and non-normally distributed variables are shown as the median and range. Quantitative results are expressed as the mean ± the SD or the median and range.

The patients’ characteristics and 4D flow parameters were analyzed using the Mann–Whitney U test or the chi-square test, as appropriate. Spearman’s rank correlation coefficients were used to examine correlations between the mean pulmonary artery volume and blood flow parameters.

No statistical sample size calculations were conducted. However, because the number of patients in the PH group was relatively small, post hoc power analysis was performed by G*Power (version 3.1.9.7; Erdfelder, Faul & Buchner, 1996).

In all tests, a two-sided p value was used, and differences with a p value of < 0.05 were considered statistically significant.

Mean pulmonary artery volume

The mean pulmonary artery volume was significantly lower in the non-PH group (41.8 ± 13.6 cm³) than in the PH group (68.6 ± 21.8 cm³, p < 0.0001, Table 2).

The mean pulmonary artery volume was significantly higher in the male subgroup (47.2 ± 17.4 cm³) than in the female subgroup (38.9 ± 12.7, p = 0.0011, Table 3).

Flow parameters in patients without and with PH

EL average and minimum showed a significant difference between the two groups (p = 0.0015 and p = 0.0001, respectively) (Table 2). Vor average, maximum, and minimum showed a significant difference between the two groups (p < 0.0001, p = 0.0005, and p < 0.0001, respectively). Hel right screw average showed a significant difference between the two groups (p = 0.0217). Hel left screw average and maximum also showed a significant difference between the two groups (p = 0.0015 and p < 0.0001, respectively).

Correlations between mean pulmonary artery volume and flow parameters

The EL average and EL minimum were significantly positively correlated with the mean pulmonary artery volume in the non-PH group (R = 0.4140, p < 0.0001; R=0.4443, p < 0.0001, respectively). The EL maximum was significantly weakly positively correlated with the mean pulmonary artery volume in the non-PH group (R = 0.2662, p = 0.0006). In contrast, the EL average, EL maximum, and EL minimum were not significantly correlated with the mean pulmonary artery volume in the PH group (R = 0.0268, p = 0.9244; R = 0.0264, p = 0.9255; R=0.1347, p = 0.6321, respectively) (Fig. 1).

The Vor average, Vor maximum, and Vor minimum were significantly strongly positively correlated with the mean pulmonary artery volume in the non-PH group (R = 0.7561, p < 0.0001; R = 0.6969, p < 0.0001; R = 0.7012, p < 0.0001, respectively). Additionally, the Vor average, Vor maximum, and Vor minimum were significantly strongly positively correlated with the mean pulmonary artery volume in the PH group (R = 0.6152, p = 0.0146; R = 0.6292, p = 0.0120; R = 0.6120, p = 0.0153, respectively) (Fig. 2).

The Hel average and Hel maximum in the non-PH group, and the Hel minimum in the PH group were not significantly correlated with the mean pulmonary artery volume (R = −0.0943, p = 0.2326; R=0.0326, p = 0.6475; R = 0.1930, p = 0.4908, respectively). In contrast, the Hel minimum was weakly negatively correlated with the mean pulmonary artery volume in the non-PH group (R = −0.2071, p = 0.0082). The Hel average and Hel maximum were not significantly correlated with the mean pulmonary artery volume in the PH group (R = 0.4445, p = 0.0969; R=0.4746, p = 0.0738, respectively) (Fig. 3).

The Hel right screw average and Hel right screw minimum were significantly positively correlated with the mean pulmonary artery volume in the non-PH group (R = 0.5105, p < 0.0001; R=0.5815, p < 0.0001). Additionally the Hel right screw maximum was weakly positively correlated with the mean pulmonary artery volume in the non-PH group (R = 0.3544, p < 0.0001). In contrast, the Hel right screw average, Hel right screw maximum, and Hel right screw minimum were not significantly correlated with the mean pulmonary artery volume in the PH group (R = 0.2983, p = 0.2802; R = 0.3413, p = 0.2131; R=0.3425, p = 0.2115, respectively) (Fig. 4).

The Hel left screw average, Hel left screw maximum, and Hel left screw minimum was significantly negatively correlated with the mean pulmonary artery volume in the non-PH group (R = −0.5349, p < 0.0001; R = −0.5689, p < 0.0001; R = −0.4280, p < 0.0001, respectively). In contrast, The Hel left screw average, Hel left screw maximum, and Hel left screw minimum were not significantly correlated with the mean pulmonary artery volume in the PH group (R = −0.2116, p = 0.4489; R = −0.2375, p = 0.3939; R = −0.3222, p = 0.2415, respectively) (Fig. 5).

Fig. 6 shows 4D flow map imaging in a representative case in the non-PH group. Fig. 7 shows 4D flow map imaging in a representative case in the PH group.

In this study, pulmonary artery volume was significantly higher in the PH group than in the non-PH group. The most likely reason for this difference is dilation of the pulmonary artery associated with PH. Although there are other possible causes for this difference in pulmonary artery volume, there was no difference in age or body mass index between the two groups. However, there was a higher proportion of male sex in the PH group than in the non-PH group. The mean pulmonary artery volume was also significantly higher in men than in women. These findings suggested that the difference in the male-female ratio affected the difference in pulmonary artery volume between the non-PH and PH groups. A previous study reported that 4D flow MRI can show age-related differences in pulmonary hemodynamics [24]. However, there was no significant difference in age between the non-PH and PH groups in this study.

Four-dimensional flow MRI can provide various types of blood flow parameters, such as EL, Hel, Vor, and WSS [25]. In this study, there were significant differences in the Vor average, maximum, and minimum between the non-PH and PH groups. Vor is an indicator of spatial velocity gradients that may show complex hemodynamic phenomena, and reflects distal resistance, proximal compliance, and right ventricular contraction [26]. Vor has been well studied in patients with PH. The appearance of vortical flow in the main pulmonary artery has been shown in PH [8, 27-30]. Moreover, the duration of vortical blood flow in 4D flow MRI has been suggested as an indicator for the accurate estimation of elevated mean pulmonary artery pressure [12, 13, 31]. Our results regarding Vor are in good agreement with these previous studies. Moreover, the Vor average, maximum, and minimum were significantly positively correlated with the mean pulmonary artery volume in the PH and non-PH groups. In this study, flow parameters were calculated by the integration of voxel volume in the pulmonary artery. Therefore, Vor may have been strongly influenced not only by PH, but also by the pulmonary artery volume.

In this study, there was no significant difference in the Hel between the non-PH and PH groups. However, there were significant differences in the Hel right screw average, Hel left screw average, and Hel left screw maximum between the two groups. Hel is an indicator of helical flow. Hel is a corkscrew-like motion in the principal flow direction and is considered to be a normal feature in healthy subjects [32-34]. Helical flow increases owing to a change in aortic blood flow resulting from aortic valve disease [23, 35, 36]. However, in a previous study, Hel was considerably lower in patients with PH than in healthy controls in the main pulmonary and right pulmonary arteries [37]. Although Hel in this previous study is considered to be consistent with Hel in our study, our results are not consistent with those in this previous report. The reason for this discrepancy between studies is unclear, but it may be related to the fact that our study included the left main pulmonary artery and the difference in pulmonary artery volume. However, our results suggested that Hel in the PH group was not large compared with that in the non-PH group. This finding is probably due to the fact that the right and left screws were similar in the PH and non-PH groups. However, the Hel right screw and left screw were larger in the PH group than in the non-PH group, which may indicate the heterogeneity of the Hel screw for each voxel due to PH. The Hel right and left screw averages, maximum, and minimum in the non-PH group were significantly positively correlated with the mean pulmonary artery volume. In contrast, the Hel right and left screw averages, maximum, and minimum in the PH group were not correlated with the mean pulmonary artery volume. Hel was calculated by integration of the voxel-based absolute value of Vor × velocity in the pulmonary artery. Because Vor was correlated with the pulmonary artery volume in the PH group, velocity may have been affected by PH other than pulmonary artery volume. A previous study reported that velocity was significantly lower in patients with PH than in controls at the left pulmonary and right pulmonary arteries [38]. Interestingly, the results between our study and this previous study appear to be the opposite. It suggests that pulmonary artery blood flow velocity decreases, but voxel-based helical flow velocity increases in patients with PH.

There were significant differences in the EL average and minimum between the non-PH and PH groups. Kinetic energy is the energy contained in the flow of the bloodstream due to motion, and EL is the kinetic energy that is lost owing to frictional forces induced by fluid viscosity within the blood flow [39]. Schäfer et al reported that the EL average was higher in patients with PH than in healthy adults in the pulmonary artery trunk and both main pulmonary arteries because of the size and nature of observed Vor/Hel [40]. Han et al reported that percent EL in the pulmonary artery was small in healthy subjects, but was almost an order of magnitude greater in subjects with PH [41]. Additionally, the increase in pulmonary artery EL in subjects with PH due to vortex formation resulted in a decrease in mechanical energy available for the system. Our result in this study showed that EL average was significantly higher in the PH group than in the non-PH group, and this is in good agreement with these previous studies. Moreover, in this study, the EL average, maximum, and minimum were significantly positively correlated with the mean pulmonary artery volume in the non-PH group. In contrast, the EL average, maximum, and minimum were not significantly correlated with the mean pulmonary artery volume in the PH group. In this study, flow parameters were calculated by the integration of voxel volume in the pulmonary artery. EL indicates energy efficiency in the region, not just blood flow. Therefore, EL may more sensitively reflect the status of PH than pulmonary artery volume. Moreover, EL minimum was significantly higher in the PH group than in the non-PH group. This finding may have occurred because the PH group showed a higher EL even during the diastolic phase owing to increased pulmonary peripheral vascular resistance and stiffness of the proximal pulmonary artery compared with the non-PH group.

The use of 4D flow MRI is less invasive than RHC. With 4D flow MRI, blood flow can be quantitatively evaluated in the pulmonary artery. To the best of our best knowledge, there have been no reports on the correlation between pulmonary artery volume and voxel-based blood flow parameters in the non-PH group and the PH group. The results of this study should be clinically useful, because with noninvasive quantitative evaluation of blood flow parameters, we may be able to diagnose patients with PH and monitor the response to treatment.

This study has several limitations. First, this study was retrospective and included a small number of patients with PH from a single institution, and they were included in the study on the basis of echocardiographic results. Therefore, the study lacked an external validation cohort. Second, many patients in this study underwent cardiac MRI with a 4D flow sequence because of suspected heart disease. Therefore, the results generated in this population subset cannot be generalized to the entire population.

This study shows that there are significant differences in EL, Vor, and Hel right screw and left screw between patients without PH and those with PH as shown by 4D flow MRI. EL, Vor, and Hel in patients without PH and Vor in patients with PH are correlated with pulmonary artery volume. However, EL and Hel right screw and left screw are not correlated with pulmonary artery volume in patients with PH, and they may reflect features of PH other than volume. EL and Hel may sensitively reflect PH in voxel-based evaluation of blood flow in the pulmonary artery.

pulmonary hypertension

RHC

right-sided heart catheterization

four-dimensional

MRI

magnetic resonance imaging

WSS

wall shear stress

tricuspid regurgitation

sPAP

systolic pulmonary artery pressure

energy loss

Vor

vorticity

Hel

helicity

Author information

Authors and Affiliations

Hirofumi Koike, M.D.^a (e-mail: [email protected])

Eijun Sueyoshi, M.D.^a (e-mail: [email protected])

Takamasa Nishimura, M.D.^a (e-mail: [email protected])

Minoru Morikawa, M.D.^a (e-mail: [email protected])

Shohei Miyazaki, M.D.^b(e-mail: [email protected])

^aDepartment of Radiology, Nagasaki University Graduate School of Biomedical Sciences, Nagasaki University School of Medicine, 1-7-1 Sakamoto, Nagasaki 852-8501, Japan

^bCardio Flow Design Inc, 22-3 Ichiban-cho Chiyoda-ku, Tokyo 102-0082, Japan

Corresponding author:

H. Koike

Department of Radiology, Nagasaki University School of Medicine, 1-7-1 Sakamoto, Nagasaki 852-8501, Japan

Tel: +81-95-819-7354; fax: +81-95-819-7357

E-mail: [email protected]

Acknowledgments

We thank Ellen Knapp, PhD, from Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.

Funding

This study was supported by JSPS KAKENHI Grant Number 21K07733.

Declarations of interest: none.

Ethical approval

The institutional review board of Nagasaki University Hospital approved this study. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

Consent to participate

Not applicable.

Consent to publish

Not applicable.

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Table 1

Patients’ demographic and clinical characteristics
Parameter	Non-PH group (n = 162)	PH group (n = 15)	p value
Age, years	55.0 ± 17.1	58.0 ± 13.5	0.6583
Male sex, n (%)	96 (59.3)	14 (93.3)	< 0.0001
BMI (kg/m²)	23.2 ± 4.8	23.4 ± 4.7	0.8886
sPAP (mmHg)	26.6 ± 6.5	48.9 ± 7.0	< 0.0001
History of PH, n	0	1	NS
Final diagnosis, n	No specific findings, 7 DCM, 47 HCM, 29 HHD, 4 MI, 10 Nonspecific myocarditis, 31 Radiation myocarditis, 5 Arrhythmia, 13 Cardiac sarcoidosis, 4 Cardiac amyloidosis, 6 LVNC, 6	DCM, 7 HCM, 1 RCM, 1 Nonspecific myocarditis, 2 Cardiac amyloidosis, 4	NS
Data are expressed as n, n (%), or the mean ± standard deviation. PH, pulmonary hypertension; sPAP, systolic pulmonary artery pressure; DCM, dilated cardiomyopathy; HCM, hypertrophic cardiomyopathy; HHD, hypertensive heart disease; MI, myocardial infarction; LVNC, left ventricular noncompaction; RCM, restrictive cardiomyopathy; NS, not significant.

Table 2

Pulmonary artery volume and flow parameters in patients without and with PH
Parameter	Non-PH group (n = 162)	PH group (n = 15)	p value	Post hoc power (%)
Mean pulmonary artery volume (cm³)	41.8 ± 13.6	68.6 ± 21.8	< 0.0001*	99.9
Energy loss average (mW)	1.12 ± 0.97	2.17 ± 2.64	0.0015*	49.4
Energy loss max (mW)	2.32 ± 2.10	3.32 ± 4.27	0.1225	19.5
Energy loss min (mW)	0.64 ± 0.63	1.40 ± 1.26	0.0001*	80.3
Vorticity average (m^3s^-1)	0.0020 ± 0.0008	0.0034 ± 0.0014	< 0.0001*	99.5
Vorticity max (m^3s^-1)	0.0031 ± 0.0012	0.0094 ± 0.0018	0.0005*	100
Vorticity min (m^3s^-1)	0.0015 ± 0.0007	0.0029 ± 0.0012	< 0.0001*	99.9
Helicity average (m^4s^-2)	−0.00000034 ± 0.000024	−0.0000056 ± 0.000024	0.4090	5.0
Helicity max (m^4s^-2)	0.000063 ± 0.000062	0.000039 ± 0.000033	0.1267	42.9
Helicity min (m^4s^-2)	−0.000084 ± 0.000080	-0.000058 ± 0.000068	0.2304	25.2
Helicity right screw average (m^4s^-2)	0.00010 ± 0.00005	0.00014 ± 0.00012	0.0217*	36.1
Helicity right screw max (m^4s^-2)	0.00027 ± 0.00015	0.00029 ± 0.00024	0.7193	6.6
Helicity right screw min (m^4s^-2)	0.00004 ± 0.00008	0.00007 ± 0.00007	0.1155	31.3
Helicity left screw average (m^4s^-2)	−0.00010± 0.00006	−0.00015± 0.00014	0.0015*	40.1
Helicity left screw max (m^4s^-2)	−0.00003± 0.00003	−0.00008± 0.00008	< 0.0001*	86.2
Helicity left screw min (m^4s^-2)	−0.00030± 0.00016	−0.00029± 0.00025	0.8448	5.4
Data are expressed as the mean ± standard deviation. PH, pulmonary hypertension; max, maximum; min, minimum.

Table 3

Pulmonary artery volume in men and women
Parameter	Men (n = 110)	Women (n = 67)	p value
Mean pulmonary artery volume (cm³)	47.2 ± 17.4	38.9 ± 12.7	0.0011
Data are expressed as the mean ± standard deviation.

No competing interests reported.

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Evaluation of the relationship between pulmonary artery volume and quantitative voxel based flow parameters in patients with and without pulmonary hypertension using 4D flow MRI

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