Magnetic Resonance Elastography-derived Stiffness Predicts Renal Function Loss and Is Associated With Microvascular Inflammation in Kidney Transplant Recipients

Shatil, Anwar S.; Kirpalani, Anish; Younus, Eyesha; Tyrrell, Pascal N.; Krizova, Adriana; Yuen, Darren A.

doi:10.1097/txd.0000000000001334

Cited by 3 publications

(9 citation statements)

References 45 publications

(63 reference statements)

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“…Therefore, reduced stiffness can be linked to reduced blood flow, a surrogate for fibrosis, which per se increases stiffness (Lee et al, 2012;Kline et al, 2018;Lang et al, 2019;Marticorena Garcia et al, 2019;Brown et al, 2020;Zhang et al, 2021;Güven et al, 2022). But other studies found an increase in stiffness with (suggested) higher levels of fibrosis (Marticorena Kirpalani et al, 2017;Han et al, 2020;Elsingergy et al, 2023) or inflammation (Shatil et al, 2022). Therefore, measuring fasting and hydration related changes in patients could be a useful tool to unveil insights into pathophysiological processes.…”

Section: Hydration-related Changesmentioning

confidence: 99%

“…This hydrostatic pressure enables a relatively constant filtration of blood in the glomeruli, i.e., glomerular filtration rate (∼120 mL/min; GFR). Therefore, quantifying biomechanical properties—even with contributions from perfusion and fibrosis—has the potential to assess kidney function ( Marticorena Garcia et al, 2016 ; Kirpalani et al, 2017 ; Marticorena Garcia et al, 2018a ; Lang et al, 2019 ; Beck-Tölly et al, 2020 ; Brown et al, 2020 ; Zhang et al, 2021 ; Chen et al, 2022 ; Shatil et al, 2022 ).…”

Section: Introductionmentioning

confidence: 99%

“…Since then, MRE methods have been improved and have shed light on the potential to assess (patho-) physiological renal processes ( Morrell et al, 2017 ). According to a Pubmed search, 20 October 2023, we could identify 26 studies on the human kidney (excluding animal, ex-vivo and tumor studies) ( Bensamoun et al, 2011 ; Rouvière et al, 2011 ; Lee et al, 2012 ; Streitberger et al, 2014 ; Low et al, 2015 ; Marticorena Garcia et al, 2016 ; Dittmann et al, 2017 ; Kirpalani et al, 2017 ; Marticorena Garcia et al, 2018a ; Marticorena Garcia et al, 2018b ; Kline et al, 2018 ; Gandhi et al, 2019 ; Lang et al, 2019 ; Marticorena Garcia et al, 2019 ; Brown et al, 2020 ; Gandhi et al, 2020 ; Han et al, 2020 ; Kennedy et al, 2020 ; Marticorena Garcia et al, 2021 ; Zhang et al, 2021 ; Dillman et al, 2022 ; Güven et al, 2022 ; Shatil et al, 2022 ; Chen et al, 2023a ; Chen et al, 2023b ; Elsingergy et al, 2023 ). So far, only pneumatic ( Bensamoun et al, 2011 ; Rouvière et al, 2011 ; Lee et al, 2012 ; Low et al, 2015 ; Marticorena Garcia et al, 2016 ; Dittmann et al, 2017 ; Kirpalani et al, 2017 ; Marticorena Garcia et al, 2018a ; Marticorena Garcia et al, 2018b ; Kline et al, 2018 ; Gandhi et al, 2019 ; Lang et al, 2019 ; Marticorena Garcia et al, 2019 ; Brown et al, 2020 ; Gandhi et al, 2020 ; Han et al, 2020 ; Kennedy et al, 2020 ; Marticorena Garcia et al, 2021 ; Zhang et al, 2021 ; Dillman et al, 2022 ; Güven et al, 2022 ; Shatil et al, 2022 ; Chen et al, 2023a ; Chen et al, 2023b ...…”

Section: Introductionmentioning

confidence: 99%

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Magnetic resonance elastography resolving all gross anatomical segments of the kidney during controlled hydration

Wolf,

Darwish,

Neji

et al. 2024

Front. Physiol.

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Introduction: Magnetic resonance elastography (MRE) is a non-invasive method to quantify biomechanical properties of human tissues. It has potential in diagnosis and monitoring of kidney disease, if established in clinical practice. The interplay of flow and volume changes in renal vessels, tubule, urinary collection system and interstitium is complex, but physiological ranges of in vivo viscoelastic properties during fasting and hydration have never been investigated in all gross anatomical segments simultaneously.Method: Ten healthy volunteers underwent two imaging sessions, one following a 12-hour fasting period and the second after a drinking challenge of >10 mL per kg body weight (60–75 min before the second examination). High-resolution renal MRE was performed using a novel driver with rotating eccentric mass placed at the posterior-lateral wall to couple waves (50 Hz) to the kidney. The biomechanical parameters, shear wave speed (cs in m/s), storage modulus (Gd in kPa), loss modulus (Gl in kPa), phase angle (Υ=2πatanGlGd) and attenuation (α in 1/mm) were derived. Accurate separation of gross anatomical segments was applied in post-processing (whole kidney, cortex, medulla, sinus, vessel).Results: High-quality shear waves coupled into all gross anatomical segments of the kidney (mean shear wave displacement: 163 ± 47 μm, mean contamination of second upper harmonics <23%, curl/divergence: 4.3 ± 0.8). Regardless of the hydration state, median Gd of the cortex and medulla (0.68 ± 0.11 kPa) was significantly higher than that of the sinus and vessels (0.48 ± 0.06 kPa), and consistently, significant differences were found in cs, Υ, and Gl (all p < 0.001). The viscoelastic parameters of cortex and medulla were not significantly different. After hydration sinus exhibited a small but significant reduction in median Gd by −0.02 ± 0.04 kPa (p = 0.01), and, consequently, the cortico-sinusoidal-difference in Gd increased by 0.04 ± 0.07 kPa (p = 0.05). Only upon hydration, the attenuation in vessels became lower (0.084 ± 0.013 1/mm) and differed significantly from the whole kidney (0.095 ± 0.007 1/mm, p = 0.01).Conclusion: High-resolution renal MRE with an innovative driver and well-defined 3D segmentation can resolve all renal segments, especially when including the sinus in the analysis. Even after a prolonged hydration period the approach is sensitive to small hydration-related changes in the sinus and in the cortico-sinusoidal-difference.

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Section: Hydration-related Changesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Magnetic resonance elastography resolving all gross anatomical segments of the kidney during controlled hydration

Wolf,

Darwish,

Neji

et al. 2024

Front. Physiol.

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“…For magnetic resonance elastography (MRE), a number of studies investigating disorders of abdominal organs such as liver (15)(16)(17)(18)(19)(20)(21)(22), spleen (23)(24)(25), kidney (26)(27)(28)(29), and pancreas (30)(31)(32)(33)(34) have been performed. However, studies investigating MRE of the gastrointestinal tract are limited.…”

Section: Introductionmentioning

confidence: 99%

Ex vivo magnetic resonance elastography of the small bowel in Crohn’s disease

Loch¹,

Kamphues²,

Beyer³

et al. 2023

Quant Imaging Med Surg

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Background: Conventional magnetic resonance enterography is limited in differentiating active inflammation and fibrosis in lesions of Crohn's disease (CD), thus providing a restricted basis for therapeutic decision making. Magnetic resonance elastography (MRE) is an emerging imaging tool that differentiates soft tissues on the basis of their viscoelastic properties. The aim of this study was to demonstrate the feasibility of MRE in assessing the viscoelastic properties of small bowel samples and quantifying differences in viscoelastic properties between healthy ileum and ileum affected by CD.Methods: Twelve patients (median age: 48 years) were prospectively enrolled in this study between September 2019 and January 2021. Patients of the study group (n=7) underwent surgery for terminal ileal CD, while patients of the control group (n=5) underwent segmental resection of healthy ileum. MRE of ileal tissue samples of surgical specimens from both groups was performed in a compact tabletop MRI scanner.Penetration rate (a in m/s) and shear wave speed (c in m/s) were determined as markers of viscosity and stiffness for vibration frequencies f of 1,000, 1,500, 2,000, 2,500, and 3,000 Hz. Additionally, damping ratio γ was deduced, and frequency-independent viscoelastic parameters were calculated using the viscoelastic spring-pot model.Results: Penetration rate a was significantly lower in CD-affected ileum compared to healthy ileum for all vibration frequencies (P<0.05). Consistently, damping ratio γ was higher in CD-affected ileum, averaged over all frequencies (healthy: 0.58±0.12, CD: 1.04±0.55, P=0.03), as well as at 1,000 and 1,500 Hz individually (P<0.05). Spring-pot-derived viscosity parameter η was also significantly reduced in CD-affected tissue (2.62±1.37 versus 10.60±12.60 Pa•s, P=0.02). No significant difference was found for shear wave speed c between healthy and diseased tissue at any frequency (P>0.05).^ ORCID: 0000-0003-1513-8339.Conclusions: MRE of surgical small bowel specimens is feasible, allowing determination of viscoelastic properties and reliable quantification of differences in viscoelastic properties between healthy and CDaffected ileum. Thus, the results presented here are an important prerequisite for future studies investigating comprehensive MRE mapping and exact histopathological correlation including characterization and quantification of inflammation and fibrosis in CD.

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“…Renal perfusion, as another important contributor to renal stiffness, was also suggested by others in. 7,9 Very recently, Shatil et al 10 reported that renal stiffness quantified by MRE was positively associated with microvascular inflammation. Based on the literature, there appears to be a multifactorial influence of CKD-related pathological features on in vivo renal stiffness that could be explored further with animal models.…”

Section: Introductionmentioning

confidence: 99%

Characterization of renal fibrosis in rats with chronic kidney disease by in vivo tomoelastography

Krehl,

Hahndorf,

Stolzenburg

et al. 2023

NMR in Biomedicine

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Chronic kidney disease (CKD) is characterized by structural changes, such as tubular atrophy, renal fibrosis, and glomerulosclerosis, all of which affect the viscoelastic properties of biological tissues. However, detection of renal viscoelasticity changes because diagnostic markers by in vivo elastography lack histopathological validation through animal models.Therefore, we investigated in vivo multiparametric magnetic resonance imaging (mp‐MRI), including multifrequency magnetic resonance elastography‐based tomoelastography, in the kidneys of 10 rats with adenine‐induced CKD and eight healthy controls. Kidney volume (in mm3), water diffusivity (apparent diffusion coefficient [ADC] in mm2/s), shear wave speed (SWS; in m/s; related to stiffness), and wave penetration rate (PR; in m/s; related to inverse viscosity) were quantified by mp‐MRI and correlated with histopathologically determined renal fibrosis (collagen area fraction [CAF]; in %). Kidney volume (40% ± 29%, p = 0.009), SWS (11% ± 12%, p = 0.016), and PR (20% ± 15%, p = 0.004) were significantly increased in CKD, which was accompanied by ADC (−24% ± 27%, p = 0.02). SWS, PR, and ADC were correlated with CAF with R = 0.63, 0.75, and −0.5 (all p < 0.05), respectively. In the CKD rats, histopathology showed tubule dilation due to adenine crystal deposition. Collectively, our results suggest that collagen accumulation during CKD progression transforms soft‐compliant renal tissue into a more rigid‐solid state with reduced water mobility. We hypothesized that tubule dilation—a specific feature of our model—might lead to higher intraluminal pressure, which could also contribute to elevated renal stiffness. Tomoelastography is a promising tool for noninvasively assessing disease progression, detecting biomechanical properties that are sensitive to different pathologic features of CKD.

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Magnetic Resonance Elastography-derived Stiffness Predicts Renal Function Loss and Is Associated With Microvascular Inflammation in Kidney Transplant Recipients

Cited by 3 publications

References 45 publications

Magnetic resonance elastography resolving all gross anatomical segments of the kidney during controlled hydration

Magnetic resonance elastography resolving all gross anatomical segments of the kidney during controlled hydration

Ex vivo magnetic resonance elastography of the small bowel in Crohn’s disease

Characterization of renal fibrosis in rats with chronic kidney disease by in vivo tomoelastography

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