Pulmonary flow assessment by phase-contrast MRI can predict short-term mortality of fibrosing interstitial lung diseases

Abstract

Background

Phase-contrast magnetic resonance imaging (PC-MRI) can determine pulmonary hemodynamics non-invasively. Pulmonary hypertension causes changes in pulmonary hemodynamics and is a factor for acute exacerbation and death in interstitial lung diseases (ILD).

Purpose

To determine associations between pulmonary hemodynamics measured by PC-MRI and short-term mortality in patients with ILD.

Material and Methods

Pulmonary hemodynamics, measured by PC-MRI in 43 patients with ILD, were reviewed retrospectively. Evaluation parameters included heart rate, right cardiac output, average flow, average velocity, acceleration time, acceleration volume (AV), maximal change in flow rate during ejection (M), M/AV, maximum area, minimum area, and relative area change in the pulmonary artery (PA). All causes of death within one year from the day of the MRI examination were assessed by reviewing medical records. Associations between evaluation parameters and outcome were determined by univariate and multivariate Cox regression analysis.

Results

Six patients (13.9%) died by the one-year follow-up. Age (hazard ratio [HR] 1.116, 95% confidence interval [CI] 1.015–1.269), average flow (HR 0.932, 95% CI 0.870–0.984), average velocity (HR 0.778, 95% CI 0.573–0.976), right cardiac output (HR 0.870, 95% CI 0.758–0.967), AV (HR 0.840, 95% CI 0.669–0.985), M/AV (HR 1.008, 95% CI 1.001–1.014), and PA relative area change (HR 0.715, 95% CI 0.459–0.928) predicted death in univariate Cox analysis. Multivariate Cox analysis showed decreased right cardiac output (HR 0.547, 95% CI 0.160–0.912) and decreased PA relative area change (HR 0.538, 95% CI 0.177–0.922) were independently associated with death.

Conclusion

Reduction in right cardiac output and decreased PA relative area change, detected by PC-MRI, were associated with increased mortality in ILD.

Keywords

Outcomes assessment lung disease phase-contrast magnetic resonance imaging cardiac output pulmonary fibrosis prognosis

Introduction

Right ventricular dysfunction and pulmonary hypertension are important complications of interstitial lung diseases (ILD) and are associated with increased mortality (1 –3). Right ventricular dysfunction is observed in patients with idiopathic pulmonary fibrosis (IPF), even if they do not have pulmonary hypertension (4). A previous study showed that mortality in IPF was predicted by right ventricular dysfunction measured by echocardiography and higher pulmonary vascular resistance measured by right heart catheterization (RHC); however, pulmonary artery pressure was not a predictive factor (3).

Cardiovascular magnetic resonance imaging (MRI) is an accurate, repeatable, and reproducible way of assessing right cardiac function and is currently regarded as the non-invasive gold standard for quantification of right ventricular function (5). It has been reported that right ventricular ejection fraction derived from cine cardiac MRI was a strong predictor of future adverse events in mild ILD with or without pulmonary hypertension (6). This was the only study of MRI in the prognostic evaluation of patients with ILD.

Phase-contrast MRI (PC-MRI) is used for non-invasive evaluation of hemodynamics in the heart and great vessels in the assessment of pulmonary hypertension. Generally, this method is used in combination with cine images acquired using a balanced steady-state free precession (bSSFP) sequence. Swift et al. (7) found that the right ventricular end-systolic volume index adjusted for age and sex, which was measured by the bSSPF method, and the relative area change of the pulmonary artery (PA) measured by PC-MRI were independent predictors of death in patients with pulmonary hypertension. However, pulmonary hemodynamic parameters measured by PC-MRI have not been reported to be of prognostic value in patients with ILD. The purpose of this study was to determine if PC-MRI measurements can predict outcomes in patients with fibrotic ILD.

Material and Methods

Study population

This retrospective and observational study was approved by the Ethics Committee for Clinical Research of University of the Ryukyus (approval number 623) and informed consent was waived.

We collected patients with a diagnosis of fibrotic ILD who underwent PC-MRI from July 2007 to April 2014 from the database of other prospective studies in two institutions. The diagnosis of fibrotic ILD, as agreed by both pulmonologists (TO, SY, SH) and chest radiologists (TI, HK, TM, YA), was based on clinical, radiographic, and pulmonary function testing (PFT). We reviewed 45 patients with fibrotic ILDs who underwent PC-MRI and excluded one with poor image quality and one who did not have follow-up after MRI. There were 43 patients (19 men, mean age = 68 years, age range = 48–82 years; 24 women, mean age = 59 years, age range = 24–80 years) analyzed in the present study (Fig. 1). The clinical etiologies of fibrotic ILD were as follows: 17 patients had idiopathic pulmonary fibrosis (14 with a usual interstitial pneumonia pattern [UIP] and three with a non-specific interstitial pneumonia [NSIP] pattern; three patients had hypersensitivity pneumonia; 21 patients had collagen vascular disease (one with rheumatoid arthritis, nine with scleroderma, five with polymyositis/dermatomyositis [PM/DM], one with Sjogren’s syndrome [SS], two with mixed connective tissue disease [MCTD], one with combined DM and SS, and two with anti-synthetase syndrome); and two patients had combined pulmonary fibrosis and emphysema. Seventeen patients underwent surgical lung biopsy and were diagnosed with fibrotic ILD based on histopathology (seven UIP, five NSIP, three hypersensitivity pneumonitis, and two non-classifiable fibrosis). The others without biopsy were clinically diagnosed. Echocardiography was performed in 19 (44.1%) patients and pulmonary hypertension was suspected in 11 (25.6%) patients. Among the 11 patients with suspicion of pulmonary hypertension, 4 (9.3%) patients underwent RHC and were diagnosed with pulmonary hypertension. There were no patients on vasodilator therapy for pulmonary hypertension and anti-fibrotic therapy for IPF/UIP. Nine patients received oral immune-suppressive therapy for collagen-vascular diseases (Cyclosporine or Tacrolimus Hydrate).We collected demographic data including clinical data (height, weight, smoking history, use of home oxygen therapy, previous history of acute exacerbation), laboratory data (PaO2, KL-6), pulmonary function test (VC % predicted, FVC % predicted, FEV1% predicted, DLco % predicted) from the dataset of other prospective study.

Fig. 1.

Flow chart of study design.

Phase-contrast MRI

MRI was performed using one of two 1.5-T systems (Magnetom Avanto: Siemens Medical Solutions, Erlangen, Germany; Achieva: Philips Medical Solutions, Best, The Netherlands). Participants received an MRI exam when they registered for the other prospective study. On the day of the MRI examination, no patient had symptoms of acute exacerbation, acute heart failure, or respiratory infections. The condition of each patient was stable during MRI and all examinations were performed in the supine position. In 14 patients, the exam was performed under low-dose oxygen administration (2–3 L/min by nasal cannula). MRI was performed with retrospective ECG triggering during free-breathing, which is more accurate than during breath-holding because there is less influence of the intrathoracic pressure change (8).

The sequence parameters for the Magnetom Avanto MRI system were as follows: fast low angle shot (FLASH) 2D; repetition time (TR) = 27.25 ms/echo time (TE) = 3.14 ms; field of view (FOV) = 260 mm; matrix = 256 × 256; segmentation factor = 1; number of acquisitions = 1; slice thickness = 6 mm; receiver bandwidth = 391 Hz/pixel; flip angle = 30°; velocity encoding = 150 cm/s. The sequence parameters for the Achieva MRI system were as follows: fast field echo (FFE); TR/TE = 12/8.5 ms; FOV = 240 mm; matrix = 256 × 256; segmentation factor = 1; number of acquisitions = 2; slice thickness = 6 mm; receiver bandwidth = 398.6 Hz/pixel; flip angle = 30°; velocity encoding = 200 cm/s. The time frame per cardiac cycle was 32 frames. The flow was measured perpendicular to the vessel, using a double-oblique slice orientation, and the region of interest (ROI) was set in the pulmonary artery truncus (Fig. 2). The flow analysis was conducted by two cardiopulmonary radiologists (NT, TI) with seven years and 25 years of experience, respectively, in each institution. The ROI setting was semi-automated, so that when a ROI was set manually on one portion of a cardiac cycle, other ROIs were automatically set for the entire cardiac cycle. After that, all ROI settings were confirmed by radiologists and corrected if needed. The measurements included heart rate, average velocity, average flow, right cardiac output, the maximum cross-sectional area (Max Area), the minimum cross-sectional area (Min Area), and the PA relative area change throughout a cardiac cycle. These parameters were automatically calculated by the MRI workstation after the ROI was set. In addition, acceleration time (AT) and acceleration volume (AV), the maximal change of flow rate during ejection (M), and the M/AV were derived from a time-flow curve obtained by PC-MRI. These measurements were calculated by waveform analysis software (Flex Pro7.0, WEISANG, Ingbert, Germany). The reproducibility of quantitative parameters obtained by the two different MRI systems in normal controls was confirmed beforehand (9).

Fig. 2.

Sagittal (a) and horizontal (b) T1-weighted imaging cross-sections of the pulmonary trunk (PT) with double-oblique slice orientation. Magnitude (c) and velocity (d) images, captured at identical locations and time phases, for evaluation of flow. The circular pulmonary trunk indicates a perpendicular orientation. Dashed circles are the region of interest.

The definitions and meanings of pulmonary hemodynamic parameters measured by PC-MRI are as follows. Average velocity was defined as the average mean flow velocity throughout a cardiac cycle. Average flow was defined as the average mean flow volume throughout a cardiac cycle. As pulmonary vascular resistance rises, average velocity and average flow decrease (10). Right cardiac output was calculated as heart rate multiplied by right cardiac stroke volume, which was measured as flow in the pulmonary trunk throughout a cardiac cycle. AT was defined as the time interval from the beginning of the anterograde flow upslope to peak systolic flow. AV was obtained by the integration of the flow rate from the onset of ejection to peak systolic flow. The maximal change in flow rate during ejection (M) was defined as the maximal value of the ascending slope of the flow rate, and M/AV was defined as M divided by AV (11) (Fig. 3). As pulmonary vascular resistance rises, the slope of the time-flow curve steepens, AT and AV decrease, and M and M/AV rise (11). PC-MRI allows estimation of pulmonary artery (PA) distensibility by measuring the relative area change between systole (Max Area) and diastole (Min Area) via segmentation of the vessel area throughout the cardiac cycle. The following formula was used to calculate the relative area change: (Max Area – Min Area)/Max Area × 100. In patients with pulmonary hypertension, the minimum area increases and the PA relative area change decreases (12).

Fig. 3.

Pulmonary hemodynamic parameters obtained from the PC-MRI time-flow curve. Acceleration time (AT) is defined as the time interval from the beginning of the anterograde flow upslope in systole to the peak systolic flow. Acceleration volume (AV) was obtained by integration of the flow rate from the onset of ejection to the peak systolic flow. The maximal change in flow rate during ejection (M) is defined as the maximal value of the ascending slope of the flow rate.

Statistical analysis

Statistical analyses were performed using JMP 11 (SAS Institute Japan, Tokyo, Japan.) Frequency counts and percentages were obtained to summarize categorical variables. Continuous variables were expressed as median and interquartile range. PC-MRI parameters were compared between survivor and non-survivor using a Mann–Whitney U test. Univariate Cox regression analysis was used to determine the associations between PC-MRI parameters and morality in patients with fibrotic ILD. Univariate Cox regression analysis was also used to determine the associations between demographic data and morality in patients with fibrotic ILD. Multivariate cox regression analysis was conducted using two different models. In the first model, all variables of PC-MRI parameters were included that showed a significant association (P < 0.05) in univariate analysis. In the second model, if there was a strong correlation among variables, only the variable with the lowest P value was selected among the variables that showed a strong correlation. A strong correlation between two variables was defined as Pearson correlation coefficient (r) ≧ 0.7. Receiver operating characteristic (ROC) curves were constructed to assess the ability of variables to predict adverse events; only variables that were significant predictors of mortality in multivariate Cox regression analysis were used to construct ROC curves. Kaplan–Meier analysis was used to assess the prognostic value of PC-MRI parameters using the cut-off values obtained by ROC analysis. The analysis endpoint was all cause of death within one year from the day when participants received the MRI examination. A P value < 0.05 was considered significant.

Results

The baseline characteristics of the 43 patients are shown in Table 1. Six patients (13.9%) died during the one- year follow-up. The causes of death were as follows: 2 (66.6%) deaths were due to acute exacerbation; 1 (16.6%) was due to pulmonary hypertension; 1 (16.6%) was due to pneumothorax; 1 (16.6%) was due to fulminant hepatitis; and 1 (16.6%) was due to an unknown cause. The median time to death was 150 days (range = 13–244 days). Four (66.6%) of six non-survivors had a previous history of acute exacerbation. Three (75%) of six non-survivors had underlying pulmonary hypertension, which was diagnosed by RHC or echocardiography. Five (83.3%) of six non-survivors had a previous history of acute exacerbation. The detailed information of non-survivors is in Suppl. Table 1.

Table 1.

Characteristics of patients (n = 43).

Sex (Male: Female)	19:24
Age (years)	63 ± 13 (24–82)
Height (cm)	156 ± 9
Weight (kg)	57 ± 12
Smoking
Never	23 (53.5)
Past	18 (41.9)
Current	2 (4.7)
Home oxygen therapy	14 (32.6)
Previous history of acute exacerbation	7 (16.3)
PaO₂ (mmHg, under room air)	77 ± 12
KL-6 (U/mL)	1084 ± 832
UIP/DM cohort	20 (46.5)
Pulmonary function test
VC % predicted	75.3 ± 21.2
FVC % predicted	76.6 ± 22.1
FEV₁ % predicted	75.1 ± 21.6
DLCO % predicted	59.0 ± 17.8
Mortality
Death	6 (13.9)
Death due to pulmonary cause	3 (6.9)

Values are given as n (%) or mean ± SD.

D_LCO, diffusing capacity of the lungs for carbon monoxide; FEV, forced expiratory volume; FVC, forced vital capacity; VC, vital capacity.

As shown in Table 2, among the PC-MRI parameters, average flow (P = 0.01), average velocity (P = 0.03), right cardiac output (P = 0.01), and PA relative area change (P = 0.01) were decreased in the non-survivor group.

Table 2.

PC-MRI parameters compared between survivors and non-survivors

	Non-survivor (n = 6)	Survivor (n = 37)	P value
Heart rate (beats/min)	79 (75.6–87.9)	79 (75.6–87.9)	0.2
Average flow (mL/s)	55.4 (41.1–60.3)	70.1 (56.6–90.4)	0.01
Average velocity (cm/s)	9.3 (6.5–10.7)	12.1 (9.6–15.4)	0.03
Right cardiac output (L/min)	3.3 (2.8–3.6)	4.2 (3.6–5.4)	0.01
Acceleration time (ms)	112 (81–129)	106 (96–119)	0.8
Acceleration volume (mL/s)	12.8 (8.7–15.0)	18.5 (11.9–23.2)	0.07
Maximal change in flow rate during ejection	3646 (3272–4603)	4284 (3340–5134)	0.5
M/AV (s⁻²)	277 (206–544)	258 (183–290)	0.2
Maximum area (cm²)	8.1 (5.7–9.2)	7.6 (5.7–8.5)	0.6
Minimum area (cm²)	6.1 (4.0–7.1)	4.5 (3.5–5.7)	0.2
PA relative area change (%)	24.2 (22.1–29.8)	35.0 (28.7–44.0)	0.01

Values are given as median (range).

M/AV, maximal change in flow rate during ejection/acceleration volume; PA, pulmonary artery; PC-MRI, phase-contrast magnetic resonance imaging.

In univariate Cox regression analysis, age (P = 0.01), average flow (P = 0.008), average velocity (P = 0.02), right cardiac output (P = 0.006), AV (P = 0.03), M/AV (P = 0.01), and PA relative area change (P = 0.004) were associated with mortality. In addition, home oxygen therapy (P = 0.002), history of acute exacerbation (P = 0.006), and %DLCO (P = 0.007) were related to mortality (Suppl. Table 2). In the first multivariate Cox regression model that used all variables of PC-MRI measurements that showed a significant association with death in univariate analysis, there was no variable that was an independent predictor of death. Since there were strong correlations among average flow, average velocity, and right cardiac output (Suppl. Table 3), we selected right cardiac output as a parameter to use in the second multivariate Cox regression model based on P value. Since there was a strong correlation between AV and M/AV, we also selected M/AV as a parameter to use in the second Cox regression model based on the P value. The second multivariate Cox regression model included age, right cardiac output, M/AV, and PA relative area change, and this model showed that right cardiac output (P = 0.004) and PA relative area change (P = 0.007) predicted death (Table 3).

Table 3.

Cox regression analysis for death in patients with fibrotic ILD (PC-MRI measurements).

	HR	95% CI	P value
Univariate analysis
Age	1.116	1.015–1.269	0.01
Heart rate	1.062	0.982–1.166	0.1
Average flow	0.932	0.870–0.984	0.008
Average velocity	0.77	0.573–0.976	0.02
Right cardiac output (per 0.1 L/min increase)	0.87	0.758–0.967	0.006
Acceleration time	0.995	0.953–1.040	0.8
Acceleration volume (AV)	0.840	0.669–0.985	0.03
Maximum change in flow rate during ejection (M)	0.999	0.998–1.000	0.4
M/AV	1.008	1.001–1.014	0.01
Maximum area (cm²)	1.035	0.610–1.653	0.8
Minimum area (cm²)	1.446	0.770–2.815	0.2
PA relative area change (%)	0.715	0.459–0.928	0.004
Multivariate analysis
Age	0.981	0.733–1.235	0.8
Right cardiac output (per 0.1 L/min increase)	0.0024	0.001–0.399	0.004
M/AV	1.001	0.980–1.024	0.9
PA relative area change	0.538	0.177–0.922	0.007

CI, confidence interval; HR, hazard ratio; ILD, interstitial lung disease; M/AV, maximal change in flow rate during ejection/acceleration volume; PC-MRI, phase-contrast magnetic resonance imaging.

ROC curve analysis was conducted using right cardiac output and PA relative area change, since these variables were independent predictors of death in multivariate Cox regression analysis. ROC curve analysis showed that the variables able to distinguish between survivor and non-survivor with fibrotic ILD were right cardiac output (AUC = 0.82, sensitivity = 0.8, specificity = 0.6, cut-off value = 3.57 L/min; P = 0.005) and PA relative area change (AUC = 0.87, sensitivity = 1.0, specificity = 0.66, cut-off value = 31%; P = 0.004).

Kaplan–Meier plots for right cardiac output and PA relative area change are presented in Figs. 4 and 5, respectively. Right cardiac output ≤3.57 L/min (P = 0.001) significantly predicted adverse events including death and acute exacerbation in patients with fibrotic ILD (Fig. 4). PA relative area change ≤31% (P = 0.01) was associated with significantly worse outcomes in fibrotic ILD patients (Fig. 5).

Fig. 4.

Kaplan–Meier plots showing one-year survival in patients with fibrotic interstitial lung disease according to right cardiac output.

Fig. 5.

Kaplan–Meier plots showing one-year survival in patients with fibrotic interstitial lung disease according to the relative area change in the pulmonary artery.

Discussion

This study assessed pulmonary hemodynamic parameters measured by PC-MRI in the prognostic evaluation of patients with fibrotic ILD. Right cardiac output was found to predict death. In a previous study, right ventricular stroke volume and right ventricular cardiac output measured by PC-MRI were directly correlated with the values of these parameters measured by RHC. Moreover, studies in which these parameters were measured simultaneously by PC-MRI and RHC have shown satisfactory agreement in patients with pulmonary hypertension (13,14). One of the most attractive aspects of PC-MRI compared with RHC is the fact that PC-MRI is non-invasive.

This study demonstrated that average flow, average velocity, right cardiac output, and PA relative area change were significantly reduced in non-survivors of fibrotic ILD patients. In addition, these measurements were significantly associated with the risk of death in univariate Cox regression analysis. This suggests that there is increased pulmonary vascular resistance in fibrotic ILD patients with poor outcome. Several reports demonstrated that measurements obtained by PC-MRI reflect an increase in pulmonary vascular resistance (10,11). Sanz et al. (10) reported strong correlations of average velocity with mean pulmonary artery pressure (r = –0.73) and pulmonary vascular resistance (r = –0.86) in patients with pulmonary hypertension. A cut-off value of 11.7 cm/s revealed a high accuracy for identifying mean pulmonary artery pressure >25 mmHg. In this study, the mean value of average velocity in the group with adverse events was 9.2 cm/s. This smaller average velocity indicated that patients with adverse events had a higher pulmonary vascular resistance. Higher pulmonary vascular resistance measured by RHC (3) and echocardiography (15) was reported as a risk factor for death. These previous findings and our results reveal that right heart dysfunction due to increased afterload caused by increased pulmonary vascular resistance is related to death in patients with fibrotic ILD.

In the present study, we tried to determine the PC-MRI parameter with the greatest prognostic value using multivariate Cox regression analysis. At first, all parameters showing statistical significance in univariate Cox analysis to predict death were used in multivariate analysis; however, no significant predictors of death were identified. The reason for the negative results was thought to be the strong correlation between parameters, which is why a second Cox regression analysis was performed which excluded parameters with strong correlations. When there is a very strong correlation between the parameters, they are canceled as confounding factors, so it is assumed that no significant results were obtained. In the Cox regression analysis, it is desirable that there will be 10 events for each predictor variable, but there were as many predictor variables as seven (the first analysis), so a significant result may not have been obtained. In this second Cox regression analysis, decreased right cardiac output and PA relative area change were independent predictors of a worse prognosis in fibrotic ILD patients.

The right cardiac output measured by PC-MRI could be the best prognostic predictor of death in fibrotic ILD. It is likely that average velocity and average flow, which have a strong correlation with right cardiac output, can also predict death. Kato et al. (6) showed that right ventricular ejection fraction derived from cardiac MRI was a strong predictor of future events in ILD patients. They also showed a reduction in right ventricular systolic function in ILD patients with or without pulmonary hypertension, as compared with a control group. D’Andrea et al. (4) found right ventricular dysfunction in IPF, despite the absence of pulmonary hypertension. Furthermore, it has been reported that pulmonary blood flow volume measured by PC-MRI was reduced in ILD patients with or without pulmonary hypertension. The mechanism is presumed to be due to the effects of inflammation or endothelial dysfunction (6). These results suggest that right ventricular dysfunction does not always occur secondary to pulmonary hypertension in ILD. Half of non-survivors were diagnosed with pulmonary hypertension. Therefore, the examination of right cardiac function is very important to assess prognosis in ILD, regardless of the presence or absence of pulmonary hypertension.

Another prognostic marker, PA relative area change that reflects stiffness of the pulmonary vasculature, was found in our study. Swift et al. (7) studied 576 patients with pulmonary arterial hypertension to determine the prognostic value of cardiac MRI. They found that right ventricular end-systolic volume index adjusted for age and sex, and the PA relative area change were independent predictors of death. This conclusion is similar to our results, and the PA relative area change is a common prognostic marker in patients with pulmonary hypertension and those with fibrotic ILD.

The advantage of measuring cardiac output by PC-MRI is that it is easier than acquiring CINE images using a bSSFP sequence. This is because the shape of the pulmonary artery is less complex than the right ventricle, especially in cases that have pronounced right ventricular dysfunction. In addition, the length of PC-MRI examination (1 min when using free-breathing method or a single 15-s breath-hold) is shorter than the bSSFP methods (20-s breath-hold × 4 times). However, the bSSFP method is well established as the reference standard for the assessment of right ventricular function and can provide other parameters that cannot be measured by PC-MRI (5). A combined MRI protocol, which might include pulmonary flow information derived from PC-MRI, in addition to other parameters derived from the bSSFP method, might be helpful for assessing prognosis in fibrotic ILD patients.

There are several limitations of this study. First, this was a retrospective observational study and the number of patients in the non-survivor group was small. Because of the retrospective study design, there is a risk of selection bias and there was a variable time interval between PC-MRI and other measurements (PFT, echocardiography). Regarding the multivariate Cox regression, a required number of cases is over 10 times of the occurrence number of the outcome. In this study, the occurrence number of outcome (short-term mortality) was six patients, therefore 60 cases are needed at least. We did not include demographic parameters even they are statistically significance because of small number of cases to deal with many factors in multivariate Cox analysis. In addition, there is lack of some clinical information such as 6-min walk test, chest CT findings, lab results (Pro BNP). Moreover, the study population had a mixed etiology and severity of fibrotic ILD. Finally, RHC was not performed in all patients in this study.

In conclusion, a reduction in right cardiac output and PA relative area change, as detected by PC-MRI, was associated with an increased risk of death in patients with fibrotic ILD. MRI to detect right ventricular dysfunction is useful for predicting a poor prognosis in fibrotic ILD patients, even when these patients do not have concomitant pulmonary hypertension.

Supplemental Material

sj-pdf-1-acr-10.1177_0284185120901503 - Supplemental material for Pulmonary flow assessment by phase-contrast MRI can predict short-term mortality of fibrosing interstitial lung diseases

Supplemental material, sj-pdf-1-acr-10.1177_0284185120901503 for Pulmonary flow assessment by phase-contrast MRI can predict short-term mortality of fibrosing interstitial lung diseases by Nanae Tsuchiya, Tae Iwasawa, Takashi Ogura, Tsuneo Yamashiro, Satomi Yara, Jiro Fujita and Sadayuki Murayama in Acta Radiologica

Footnotes

Acknowledgements

The authors are grateful to Yuichiro Ayukawa, MD, PhD, for helping MR analysis, Shusaku Haranaga, MD, PhD, and Ms. Chihiro Siroma for contribution for collecting data and Mark L. Schiebler, MD and Alejandro Roldan-Alzate, PhD for editorial assistance.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Nagao Memorial Fund and the Japan Society for the Promotion of Science (Grant No. 24591782).

ORCID iDs

Nanae Tsuchiya

Tae Iwasawa

Tsuneo Yamashiro

Supplemental material

Supplemental material for this article is available online.

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