Establishment of multifrequency magnetic resonance elastography for adrenal gland imaging: feasibility and reproducibility for assessing stiffness and fluidity in the healthy adrenal gland

Introduction

The adrenal glands are located in the retroperitoneal abdominal cavity on the upper poles of the kidneys and embedded in fatty tissue. Their central role as endocrine glands is the biosynthesis and secretion of steroid hormones and catecholamines (1,2). Adrenal masses are occasionally discovered during routine imaging examinations with a prevalence of 1.4% to 7.3% in computed tomography (2-4). In order to specify functional activity and rule out malignancy, patients are subject to many consecutive examinations to curb the wide variety of outcomes (5). For instance, the adrenocortical carcinoma is a rare tumor that is often associated with an increased production of steroid hormones and shows aggressive behavior with a poor prognosis when diagnosed at a later stage (6,7).

Noninvasive medical imaging modalities such as computed tomography and magnetic resonance imaging (MRI) are limited in differentiating benign and malignant adrenal lesions (2). Therefore, histopathology remains the ultimate tool for confirmation of malignancy. Unlike other primary cancers, suspicious adrenal tumors need to be resected surgically because of potential tumor dissemination by fine needle biopsy (8).

Multifrequency magnetic resonance elastography (MRE) with tomoelastography post-processing (tomoelastography) is a phase contrast-based MRI technique that has recently proven to be a suitable method for assessing a biological tissue’s viscoelastic properties by generating quantitative stiffness maps (elastograms) based on externally induced shear waves. Besides stiffness, multifrequency MRE measures the loss angle of the complex shear modulus, which defines a material’s internal friction or fluidity. The term “fluidity” refers to a material’s tendency to exhibit viscous behavior, indicated by the loss angle, which describes the balance between elastic and viscous properties, with higher values representing more fluid-like characteristics (9). The loss angle is bounded between 0 for entirely solid materials and π/2 for purely fluid material properties (10). Successful use of multifrequency MRE in various abdominal organs (11-15), such as the liver (16), the intestines (15), the spleen (17), the kidney (18) and the pancreas (19), has shown superior detail resolution. These encouraging results motivate investigations of small anatomical structures such as adrenal glands. However, no MRE studies of the adrenal glands have been published to date.

This study aimed to establish multifrequency MRE for characterization of healthy adrenal viscoelasticity. To this end, we focused on three key points: (I) generating consistent high-resolution elastograms of the adrenal gland, (II) providing reference values and testing the repeatability and interobserver variation of the method, and (III) optimizing detail resolution and stiffness fidelity by motion correction. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1011/rc).

Methods

This prospective cross-sectional study complied with the Declaration of Helsinki (as revised in 2013) and was approved by the internal review board of Charité – Universitätsmedizin Berlin (No. EA1/076/17). Written informed consent was obtained from all participants. Multifrequency MRE was developed at Charité – Universitätsmedizin Berlin, and the study was performed without financial support from industry. The authors had control of the data and information submitted for publication.

Subjects

The study was conducted in a tertiary care academic center using outpatient participants, enrolled through convenience sampling. Fifteen healthy volunteers [median age, interquartile range (IQR), 25 (23–30) years, eight women] without any medical history of the adrenal gland, malignancies, or endocrine disorders were included from December 2020 to November 2021. The inclusion criteria required participants to be free of any known endocrine or adrenal disorders, while exclusion criteria included a history of malignancies, chronic diseases, or other major medical conditions. To test the repeatability of the method, test-retest examinations of a subgroup of twelve volunteers were performed consecutively by the same examiner after disassembling and reassembling the MRE-setup. Independent interpretation of findings by two observers (A.W. with three years of experience in elastography and S.R.M.G. a radiologist with >10 years of experience in clinical radiology and elastography) was used for testing the interobserver variability.

MRE

MRE was performed on a 3-Tesla MRI scanner (Lumina, Siemens, Erlangen) with a 12-channel phased-array surface coil as reported in (20). All volunteers were examined in supine position after two hours without drinking or eating. Two posterior and two anterior actuators were used to induce mechanical vibrations at harmonic frequencies of 30, 40, 50, and 60 Hz. Medical compressed air from a source in the scanner room was used to power the actuators, connected to two parallel hoses and two electromagnetic valves. The anterior actuators were placed on the lower costal arch on the midclavicular line, whereas the posterior actuators were placed paravertebrally at the same height. The entire MRE exam was performed during free breathing and took 3.5 minutes. A single-shot, spin-echo planar imaging (EPI) sequence with flow-compensated motion-encoding gradients was used to acquire the wave images (21).

For anatomical orientation, T2-weighted HASTE (half-Fourier single-shot turbo spin-echo) and 3D T1-weighted VIBE (volumetric interpolated breath-hold examination) sequences were acquired. The imaging volume consisted of 25 axially oriented slices of 5 mm thickness with a field of view (FOV) of 280×224 mm² (matrix size: 140×112) and 2.0×2.0×2.0 mm³ voxel size.

Imaging parameters were as follows: repetition time =1,200 ms; echo time =55 ms; parallel imaging with a GRAPPA factor of 2; frequency of the motion-encoding gradient =48.45 Hz for consecutive mechanical frequencies of 40, 50, and 60 Hz; amplitude of the motion-encoding gradient =34 mT/m.

MRE data processing

2D tomoelastography image reconstruction based on multifrequency wave number-based dual elasto-visco (k-MDEV) inversion was used for reconstruction of shear wave speed (SWS, in m/s) as a surrogate for tissue stiffness (21). Loss angle (loss angle of the complex shear modulus, in rad), as a surrogate for fluidity, were reconstructed by direct-inversion-based MDEV inversion (22). The mean of all four frequencies, with amplitude weighting, was calculated for SWS and loss angle. MRE post-processing was performed using a server-based software (https://bioqic-apps.charite.de). Regions of interest covering the entire adrenal gland in each slice, with a small safety distance to the margin to minimize boundary effects, were manually drawn on the SWS and fluidity maps after matching with MRE-magnitude images using ImageJ (Version 1.52k, Wayne Rasband, US National Institutes of Health, Bethesda, MD, USA).

Motion correction

Motion correction was performed on the MRE-dataset of all healthy volunteers. 2D slice-wise motion correction was applied to maximize detail resolution. It was based on registration of MRE magnitude images using the Fourier-Mellin transform (23). To quantify the effect of motion correction, sharpness of the images was quantified by computing the variance (σ) of the Laplacian Δ (24) of time-averaged MRE magnitude images as described by Shahryari et al. (25).

Statistical analysis

Group values were presented as median with IQR. Side differences were calculated by two-tailed Wilcoxon test. After no side differences were detected, the left adrenal gland was used for further analysis. Differences between women and men were calculated by two-tailed Mann-Whitney test. Repeatability was assessed using the intraclass correlation coefficient (ICC) (26) and the coefficient of repeatability (CR) (27). Interobserver variability was analyzed by ICC (28). Repeatability and interobserver variability were classified from poor to excellent (poor, <0.50; moderate, 0.50–0.75; good, >0.75–0.90; excellent, >0.90) (29). Correlation between SWS and both age and body mass index (BMI) were calculated by Spearman r. The relative increase in sharpness after motion correction was calculated by two-tailed Wilcoxon test. P values <0.05 from two-sided tests were considered statistically significant. Statistical analysis was performed with GraphPad Prism (v9, GraphPad Software, La Jolla, CA, USA) and MATLAB R2020b (The MathWorks, Natick, MA, USA).

Results

MRE allowed analysis of the adrenal gland in all volunteers, with analyzable data obtained for all participants, resulting in a success rate of 100%. An example for illustration is presented in Figure 1. Detailed characteristics of the study population are summarized in Table 1.

Figure 1 Representative MRI magnitude image and shear wave speed map (elastogram) of a healthy volunteer. The left adrenal gland is magnified in the yellow boxes and marked with a yellow arrow in both images. MRI, magnetic resonance imaging; SWS, shear wave speed.

A median (IQR) SWS of 1.31 (1.24–1.33) m/s and loss angle of 0.84 (0.79–0.91) rad were calculated. No differences were found between left and right adrenal glands for SWS (median difference, 0.02; P=1.13) and loss angle (0.2; P=0.06) or for sex (P=0.78 for SWS/P=0.69 for loss angle).

Repeated measurement showed very good repeatability for SWS (CR =0.05/ICC =0.89) and loss angle (CR =0.12 and ICC =0.73). Bland-Altman plots of SWS and loss angle are given in Figure 2.

Figure 2 Bland-Altman plots of repeatability. Presenting differences of two measures: (A) shear wave speed (stiffness) and (B) loss angle of the complex shear modulus (fluidity). n=15. Dotted line (blue) = mean, upper dashed line (23) =+1.96 SD, lower dashed line (23) =−1.96 SD. SD, standard deviation.

A very good interobserver variability was found for both SWS (ICC =0.86; P<0.01) and loss angle (ICC =0.9; P<0.01). Bland-Altman plots of SWS and loss angle are provided in Figure 3.

Figure 3 Bland-Altman plot of interobserver agreement. Presenting differences of two observers: (A) shear wave speed (stiffness) and (B) loss angle of the complex shear modulus (fluidity). n=15. Dotted line (blue) = mean, upper dashed line (23) =+1.96 SD, lower dashed line (23) =−1.96 SD. SD, standard deviation.

Neither SWS nor loss angle correlated with age (SWS, r=−0.26; P=0.35; loss angle, r=−0.04; P=0.89). SWS did not correlate with BMI (SWS, r=−0.28; P=0.31). In contrast, loss angle was negatively correlated with BMI (r=−0.55; P=0.04), see Figure 4.

Figure 4 Correlation of the variables age and BMI with stiffness and fluidity. (A) Stiffness, with SWS as a surrogate, does not correlate with age. (B) Stiffness does not correlate with BMI. (C) Fluidity does not correlate with age. (D) Fluidity is negatively correlated with BMI. BMI, body mass index; SWS, shear wave speed.

Motion correction failed in three healthy volunteers and therefore, only twelve healthy volunteers were included in this analysis. Slightly sharper borders of the adrenal glands were observed in elastograms after motion correction, see Figure 5A,5B. A relative increase in sharpness of 12%±12% was determined (P=0.04), see Figure 5C.

Figure 5 Visualisations demonstrating the impact of 2D motion correction on MRI of the adrenal gland. (A) Representative MRI magnitude and elastogram without motion correction. (B) Representative MRI magnitude and elastogram with 2D motion correction. The healthy left adrenal gland is marked with a yellow arrow in each image. (C) A relative increase in sharpness of 12%±12% was determined after motion correction (P=0.04). 2D, 2-dimensional; MRI, magnetic resonance imaging; SWS, shear wave speed.

All results are summarized in Table 2.

Discussion

In this study, we quantified for the first time in-vivo viscoelasticity of adrenal glands by multifrequency MRE. Our findings provide strong evidence for excellent feasibility, repeatability, and interobserver agreement.

Due to their deep location in the abdomen and the surrounding fatty tissue, shear waves are attenuated more markedly before reaching the adrenal glands. Use of multiple mechanical frequencies alleviates potential wave voids and improves wave signal-to-noise ratio (SNR), which is a notable strength of multifrequency MRE (13,30,31).

Our results’ outstanding repeatability and interobserver consistency serve as evidence for this. There are no published adrenal MRE data available to compare with our viscoelasticity.

To the best of our knowledge, the adrenal gland has only been the subject of one ultrasound-based elastography study, which revealed differences in the stiffness of benign adrenal tumors (32). The focus of this study was on the detection of adrenal masses by acoustic radiation force imaging, and no healthy adrenal glands, which are much smaller than adrenal masses, were analyzed. The authors reported myelolipomas (29.4 kPa =3.13 m/s) to be stiffer than adenomas (6.8 kPa =1.51 m/s) and nodular hyperplasia (6.3 kPa =1.45 m/s, converting kPa to m/s using SWS²ρ = Youngs modulus/3 with unit mass density ρ of 1 kg/L). These stiffness values are higher than the median SWS we observed in healthy adrenal glands in the present study (1.32 m/s). However, it is important to note that healthy adrenal glands and adrenal masses are not directly comparable due to differences in tissue composition and pathology.

With their endo- and exocrine function, the adrenal glands and the pancreas are the only organs with a glandular structure in the abdomen. The two organs have similar viscoelastic properties [healthy pancreas, 1.25–1.32 m/s (19)]. In contrast, the fluidity of the healthy pancreas of 1.20±0.15 rad (19) is much higher than that of adrenal gland tissue (0.83 rad). While the adrenal gland and the pancreas share some of the same cell-cell adhesion molecules, the divergence in cell-cell adhesion may predominate (33). This difference may explain the higher cell density of the pancreas compared to the adrenal gland.

Due to the anatomical proximity, we can compare adrenal gland viscoelastic properties with those of the kidneys. MRE of normal kidneys has revealed regional differences in stiffness between the cortex and medulla: while cortical SWS was 2.10±0.17 m/s, medullary SWS was softer at 1.35±0.11 m/s. With a total parenchymal SWS of 1.71±0.16 m/s, healthy renal stiffness is higher than healthy adrenal stiffness (34).

Negative correlation of the loss angle to the BMI may be attributed to the general increase of proportional body fat with an increasing BMI. Fat, being less viscous than other tissue, may affect the viscoelastic properties of nearby organs. A higher BMI also is linked to metabolic syndrome, which could influence tissue composition and water content, resulting in lower loss angle.

Breathing-related motion of all abdominal organs degrades the resolution of MRE maps acquired during free breathing. Patient motion over time results in blurring of edges in the time averaged MRE magnitude maps, which is reflected in a lower variance in the Laplacian image. As shown in the present study, 2D motion correction can slightly improve the sharpness of stiffness maps. Notably, images with small motion amplitudes were only minorly degraded by motion artifacts and negligibly contributed to changes in sharpness.

Despite encouraging results, our study has limitations. Our analysis was designed as a pilot study, and our results need to be validated in a larger population of subjects at different sites. Furthermore, physiological variations such as circadian cortisone secretion were not considered. Finally, we could not resolve very small subregions within the adrenal gland including the medulla and cortex.

Conclusions

In summary, multifrequency MRE provides robust, high-resolution elastograms of the adrenal glands within a short scan time, with very good repeatability and interobserver agreement. This study presents the first reference values of adrenal gland stiffness and fluidity for future differentiation of adrenal masses and treatment monitoring in the clinical context.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-1011/rc

Funding: This study was financially supported by the German Research Foundation (No. DFG FOR5628 to I.S. and S.R.M.G.; No. 467843609 to S.R.M.G.; No. SFB1340 to B.H. and I.S.; and No. BIOQIC GRK 2260 to I.S.).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1011/coif). S.R.M.G. receives funding from the German Research Foundation (Nos. DFG FOR5628 and 467843609) and ESGAR Seed Grant. M.T.M. receives honoraria for lectures by Sanofi, Eickeler and serves as secretary of the CAEK/DGAV (Chirurgische Arbeitsgemeinschaft Endokrinologie/Deutsche Gesellschaft für Allgemein- und Viszeralchirurgie). I.S. is patent holder to a technical development related to magnetic resonance elastography and receives funding from the German Research Foundation (Nos. DFG FOR5628, 467843609, and BIOQIC GRK 2260). B.H. receives grant money from 302 companies or nonprofit organizations to the Department of Radiology, a consulting honorarium from Canon and holds the following board memberships: Deutsche Röntgengesellschaft, European Congress of Radiology, European Society of Radiology, ESMRMB, European School of Radiology, Deutsche Forschungsgemeinschaft (support for travel). The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This prospective study complied with the Declaration of Helsinki (as revised in 2013) and was approved by the internal review board of Charité – Universitätsmedizin Berlin (No. EA1/076/17). Written informed consent was obtained from all participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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