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Zhong G, Chen L, Lin Z, Xiang Z. Evaluation of renal function in chronic kidney disease using histogram analysis based on multiple diffusion models. Br J Radiol 2024; 97:803-811. [PMID: 38291900 PMCID: PMC11027312 DOI: 10.1093/bjr/tqae024] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/16/2023] [Revised: 12/22/2023] [Accepted: 01/24/2024] [Indexed: 02/01/2024] Open
Abstract
OBJECTIVES To compare the diagnostic value of histogram features of multiple diffusion metrics in predicting early renal impairment in chronic kidney disease (CKD). METHODS A total of 77 patients with CKD (mild group, estimated glomerular filtration rate (eGFR) ≥60 mL/min/1.73 m2) and 30 healthy controls (HCs) were enrolled. Diffusion-weighted imaging was performed by using single-shot echo planar sequence with 13 b values (0, 20, 50, 80, 100, 150, 200, 500, 800, 1000, 1500, 2000, and 2500 s/mm2). Diffusion models including mono-exponential (Mono), intravoxel incoherent motion (IVIM), stretched-exponential (SEM), and kurtosis (DKI) were calculated, and their histogram features were analysed. All diffusion models for predicting early renal impairment in CKD were established using logistic regression analysis, and diagnostic efficiency was compared among the models. RESULTS All diffusion models had high differential diagnosis efficiency between the mild group and HCs. The areas under the curve (AUCs) of Mono, IVIM, SEM, DKI, and the combined diffusion model for predicting early renal impairment in CKD were 0.829, 0.809, 0.760, 0.825, and 0.861, respectively. There were no significant differences in AUCs except SEM and combined model, SEM, and DKI model. There were significant correlations between eGFR/serum creatinine and some of histogram features. CONCLUSIONS Histogram analysis based on multiple diffusion metrics was practicable for the non-invasive assessment of early renal impairment in CKD. ADVANCES IN KNOWLEDGE Advanced diffusion models provided microstructural information. Histogram analysis further reflected histological characteristics and heterogeneity. Histogram analysis based on multiple diffusion models could provide an accurate and non-invasive method to evaluate the early renal damage of CKD.
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Affiliation(s)
- Guimian Zhong
- The First Affiliated Hospital of Jinan University, Guangzhou 510632, China
- Department of Radiology, Guangzhou Panyu Central Hospital, Guangzhou 511400, China
| | - Luyan Chen
- Department of Radiology, Guangzhou Panyu Central Hospital, Guangzhou 511400, China
| | | | - Zhiming Xiang
- Department of Radiology, Guangzhou Panyu Central Hospital, Guangzhou 511400, China
- Jinan University, Guangzhou 510632, China
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Guo R, Lu F, Lin J, Fu C, Liu M, Yang S. Multi-b-value DWI to evaluate the synergistic antiproliferation and anti-heterogeneity effects of bufalin plus sorafenib in an orthotopic HCC model. Eur Radiol Exp 2024; 8:43. [PMID: 38467904 PMCID: PMC10928042 DOI: 10.1186/s41747-024-00448-y] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/22/2023] [Accepted: 02/06/2024] [Indexed: 03/13/2024] Open
Abstract
BACKGROUND Multi-b-value diffusion-weighted imaging (DWI) with different postprocessing models allows for evaluating hepatocellular carcinoma (HCC) proliferation, spatial heterogeneity, and feasibility of treatment strategies. We assessed synergistic effects of bufalin+sorafenib in orthotopic HCC-LM3 xenograft nude mice by using intravoxel incoherent motion (IVIM), diffusion kurtosis imaging (DKI), a stretched exponential model (SEM), and a fractional-order calculus (FROC) model. METHODS Twenty-four orthotopic HCC-LM3 xenograft mice were divided into bufalin+sorafenib, bufalin, sorafenib treatment groups, and a control group. Multi-b-value DWI was performed using a 3-T scanner after 3 weeks' treatment to obtain true diffusion coefficient Dt, pseudo-diffusion coefficient Dp, perfusion fraction f, mean diffusivity (MD), mean kurtosis (MK), distributed diffusion coefficient (DDC), heterogeneity index α, diffusion coefficient D, fractional order parameter β, and microstructural quantity μ. Necrotic fraction (NF), standard deviation (SD) of hematoxylin-eosin staining, and microvessel density (MVD) of anti-CD31 staining were evaluated. Correlations of DWI parameters with histopathological results were analyzed, and measurements were compared among four groups. RESULTS In the final 22 mice, f positively correlated with MVD (r = 0.679, p = 0.001). Significantly good correlations of MK (r = 0.677), α (r = -0.696), and β (r= -0.639) with SD were observed (all p < 0.010). f, MK, MVD, and SD were much lower, while MD, α, β, and NF were higher in bufalin plus sorafenib group than control group (all p < 0.050). CONCLUSION Evaluated by IVIM, DKI, SEM, and FROC, bufalin+sorafenib was found to inhibit tumor proliferation and angiogenesis and reduce spatial heterogeneity in HCC-LM3 models. RELEVANCE STATEMENT Multi-b-value DWI provides potential metrics for evaluating the efficacy of treatment in HCC. KEY POINTS • Bufalin plus sorafenib combination may increase the effectiveness of HCC therapy. • Multi-b-value DWI depicted HCC proliferation, angiogenesis, and spatial heterogeneity. • Multi-b-value DWI may be a noninvasive method to assess HCC therapeutic efficacy.
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Affiliation(s)
- Ran Guo
- Department of Radiology, Shanghai Municipal Hospital of Traditional Chinese Medicine, Shanghai University of Traditional Chinese Medicine, 274 Middle Zhi-jiang Road, Shanghai, 200071, People's Republic of China
| | - Fang Lu
- Department of Radiology, Shuguang Hospital Affiliated to Shanghai University of Traditional Chinese Medicine, Shanghai, 201203, People's Republic of China
| | - Jiang Lin
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai, 200032, People's Republic of China
- Shanghai Institute of Medical Imaging, Shanghai, 200032, People's Republic of China
| | - Caixia Fu
- MR Application Development, Siemens Shenzhen Magnetic Resonance Ltd, Shenzhen, 518057, People's Republic of China
| | - Mengxiao Liu
- MR scientific Marketing, Diagnostic Imaging, Siemens Healthineers Ltd, Shanghai, 201318, People's Republic of China
| | - Shuohui Yang
- Department of Radiology, Shanghai Municipal Hospital of Traditional Chinese Medicine, Shanghai University of Traditional Chinese Medicine, 274 Middle Zhi-jiang Road, Shanghai, 200071, People's Republic of China.
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Obara M, Kwon J, Yoneyama M, Ueda Y, Cauteren MV. Technical Advancements in Abdominal Diffusion-weighted Imaging. Magn Reson Med Sci 2023; 22:191-208. [PMID: 36928124 PMCID: PMC10086402 DOI: 10.2463/mrms.rev.2022-0107] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 03/18/2023] Open
Abstract
Since its first observation in the 18th century, the diffusion phenomenon has been actively studied by many researchers. Diffusion-weighted imaging (DWI) is a technique to probe the diffusion of water molecules and create a MR image with contrast based on the local diffusion properties. The DWI pixel intensity is modulated by the hindrance the diffusing water molecules experience. This hindrance is caused by structures in the tissue and reflects the state of the tissue. This characteristic makes DWI a unique and effective tool to gain more insight into the tissue's pathophysiological condition. In the past decades, DWI has made dramatic technical progress, leading to greater acceptance in clinical practice. In the abdominal region, however, acquiring DWI with good quality is challenging because of several reasons, such as large imaging volume, respiratory and other types of motion, and difficulty in achieving homogeneous fat suppression. In this review, we discuss technical advancements from the past decades that help mitigate these problems common in abdominal imaging. We describe the use of scan acceleration techniques such as parallel imaging and compressed sensing to reduce image distortion in echo planar imaging. Then we compare techniques developed to mitigate issues due to respiratory motion, such as free-breathing, respiratory-triggering, and navigator-based approaches. Commonly used fat suppression techniques are also introduced, and their effectiveness is discussed. Additionally, the influence of the abovementioned techniques on image quality is demonstrated. Finally, we discuss the current and future clinical applications of abdominal DWI, such as whole-body DWI, simultaneous multiple-slice excitation, intravoxel incoherent motion, and the use of artificial intelligence. Abdominal DWI has the potential to develop further in the future, thanks to scan acceleration and image quality improvement driven by technological advancements. The accumulation of clinical proof will further drive clinical acceptance.
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Affiliation(s)
| | | | | | - Yu Ueda
- MR Clinical Science, Philips Japan Ltd
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Solomon E, Lemberskiy G, Baete S, Hu K, Malyarenko D, Swanson S, Shukla-Dave A, Russek SE, Zan E, Kim SG. Time-dependent diffusivity and kurtosis in phantoms and patients with head and neck cancer. Magn Reson Med 2023; 89:522-535. [PMID: 36219464 PMCID: PMC9712275 DOI: 10.1002/mrm.29457] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/05/2022] [Revised: 08/22/2022] [Accepted: 08/23/2022] [Indexed: 12/13/2022]
Abstract
PURPOSE To assess the reliability of measuring diffusivity, diffusional kurtosis, and cellular-interstitial water exchange time with long diffusion times (100-800 ms) using stimulated-echo DWI. METHODS Time-dependent diffusion MRI was tested on two well-established diffusion phantoms and in 5 patients with head and neck cancer. Measurements were conducted using an in-house diffusion-weighted STEAM-EPI pulse sequence with multiple diffusion times at a fixed TE on three scanners. We used the weighted linear least-squares fit method to estimate time-dependent diffusivity,D ( t ) $$ D(t) $$ , and diffusional kurtosis,K ( t ) $$ K(t) $$ . Additionally, the Kärger model was used to estimate cellular-interstitial water exchange time (τ ex $$ {\tau}_{ex} $$ ) fromK ( t ) $$ K(t) $$ . RESULTS Diffusivity measured by time-dependent STEAM-EPI measurements and commercial SE-EPI showed comparable results with R2 above 0.98 and overall 5.4 ± 3.0% deviation across diffusion times. Diffusional kurtosis phantom data showed expected patterns: constantD $$ D $$ andK $$ K $$ = 0 for negative controls and slow varyingD $$ D $$ andK $$ K $$ for samples made of nanoscopic vesicles. Time-dependent diffusion MRI in patients with head and neck cancer found that the Kärger model could be considered valid in 72% ± 23% of the voxels in the metastatic lymph nodes. The median cellular-interstitial water exchange time estimated for lesions was between 58.5 ms and 70.6 ms. CONCLUSIONS Based on two well-established diffusion phantoms, we found that time-dependent diffusion MRI measurements can provide stable diffusion and kurtosis values over a wide range of diffusion times and across multiple MRI systems. Moreover, estimation of cellular-interstitial water exchange time can be achieved using the Kärger model for the metastatic lymph nodes in patients with head and neck cancer.
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Affiliation(s)
- Eddy Solomon
- Department of Radiology, MRI Research Institute, Weill Cornell Medical College, New York, NY, United States
| | - Gregory Lemberskiy
- Department of Radiology, MRI Research Institute, Weill Cornell Medical College, New York, NY, United States
| | - Steven Baete
- Department of Radiology, MRI Research Institute, Weill Cornell Medical College, New York, NY, United States
| | - Kenneth Hu
- Department of Radiation Oncology, New York University, New York, NY, United States
| | - Dariya Malyarenko
- Department of Radiology, Michigan Medicine, University of Michigan, Ann Arbor, MI, United States
| | - Scott Swanson
- Department of Radiology, Michigan Medicine, University of Michigan, Ann Arbor, MI, United States
| | - Amita Shukla-Dave
- Departments of Medical Physics and Radiology, Memorial Sloan Kettering Cancer Center, New York, NY, United States
| | - Stephen E Russek
- National Institute of Standards and Technology, Boulder, CO, United States
| | - Elcin Zan
- Department of Radiology, MRI Research Institute, Weill Cornell Medical College, New York, NY, United States
| | - Sungheon Gene Kim
- Department of Radiology, MRI Research Institute, Weill Cornell Medical College, New York, NY, United States
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Tadimalla S, Wang W, Haworth A. Role of Functional MRI in Liver SBRT: Current Use and Future Directions. Cancers (Basel) 2022; 14:cancers14235860. [PMID: 36497342 PMCID: PMC9739660 DOI: 10.3390/cancers14235860] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/23/2022] [Revised: 11/23/2022] [Accepted: 11/24/2022] [Indexed: 11/30/2022] Open
Abstract
Stereotactic body radiation therapy (SBRT) is an emerging treatment for liver cancers whereby large doses of radiation can be delivered precisely to target lesions in 3-5 fractions. The target dose is limited by the dose that can be safely delivered to the non-tumour liver, which depends on the baseline liver functional reserve. Current liver SBRT guidelines assume uniform liver function in the non-tumour liver. However, the assumption of uniform liver function is false in liver disease due to the presence of cirrhosis, damage due to previous chemo- or ablative therapies or irradiation, and fatty liver disease. Anatomical information from magnetic resonance imaging (MRI) is increasingly being used for SBRT planning. While its current use is limited to the identification of target location and size, functional MRI techniques also offer the ability to quantify and spatially map liver tissue microstructure and function. This review summarises and discusses the advantages offered by functional MRI methods for SBRT treatment planning and the potential for adaptive SBRT workflows.
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Affiliation(s)
- Sirisha Tadimalla
- Institute of Medical Physics, School of Physics, Faculty of Science, The University of Sydney, Camperdown, NSW 2006, Australia
- Correspondence:
| | - Wei Wang
- Crown Princess Mary Cancer Centre, Sydney West Radiation Oncology Network, Western Sydney Local Health District, Sydney, NSW 2145, Australia
| | - Annette Haworth
- Institute of Medical Physics, School of Physics, Faculty of Science, The University of Sydney, Camperdown, NSW 2006, Australia
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Qin YL, Wang S, Chen F, Liu HX, Yue KT, Wang XZ, Ning HF, Dong P, Yu XR, Wang GZ. Prediction of outcomes by diffusion kurtosis imaging in patients with large (≥5 cm) hepatocellular carcinoma after liver resection: A retrospective study. Front Oncol 2022; 12:939358. [DOI: 10.3389/fonc.2022.939358] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/16/2022] [Accepted: 10/18/2022] [Indexed: 11/18/2022] Open
Abstract
PurposeTo evaluate preoperative diffusion kurtosis imaging (DKI) in predicting the outcomes of large hepatocellular carcinoma (HCC) after liver resection (LR).Materials and methodsFrom January 2015 to December 2017, patients with a large (≥5cm) HCC who underwent preoperative DKI were retrospectively reviewed. The correlations of the mean kurtosis (MK), mean diffusivity (MD), and apparent diffusion coefficient (ADC) with microvascular invasion (MVI) or histological grade were analyzed. Cox regression analyses were performed to identify the predictors of recurrence-free survival (RFS) and overall survival (OS). A nomogram to predict RFS was established. P<0.05 was considered as statistically significant.ResultsA total of 97 patients (59 males and 38 females, 56.0 ± 10.9 years) were included in this study. The MK, MD, and ADC values were correlated with MVI or histological grade (P<0.01). With a median follow-up time of 41.2 months (range 12-69 months), 67 patients (69.1%) experienced recurrence and 41 patients (42.3%) were still alive. The median RFS and OS periods after LR were 29 and 45 months, respectively. The 1-, 3-, and 5-year RFS and OS rates were 88.7%, 41.2%, and 21.7% and 99.0%, 68.3%, and 25.6%, respectively. MK (P<0.001), PVT (P<0.001), and ADC (P=0.033) were identified as independent predictor factors for RFS. A nomogram including the MK value for RFS showed the best performance, and the C-index was 0.895.ConclusionThe MK value obtained from DKI is a potential predictive factor for recurrence and poor survival, which could provide valuable information for guiding the efficacy of LR in patients with large HCC.
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Cao X, Shi H, Dou WQ, Zhao XY, Zheng YX, Ge YP, Cheng HC, Geng DY, Wang JY. Can DKI-MRI predict recurrence and invasion of peritumoral zone of hepatocellular carcinoma after transcatheter arterial chemoembolization? World J Gastrointest Surg 2022; 14:1150-1160. [PMID: 36386402 PMCID: PMC9640335 DOI: 10.4240/wjgs.v14.i10.1150] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/18/2022] [Revised: 07/29/2022] [Accepted: 09/21/2022] [Indexed: 02/07/2023] Open
Abstract
BACKGROUND Hepatocellular carcinoma (HCC) is a major cause of cancer-related mortality worldwide. Transcatheter arterial chemoembolization (TACE) has been performed as a palliative treatment for patients with HCC. However, HCC is easy to recur after TACE. Magnetic resonance imaging (MRI) has clinical potential in evaluating the TACE treatment effect for patients with liver cancer. However, traditional MRI has some limitations.
AIM To explore the clinical potential of diffusion kurtosis imaging (DKI) in predicting recurrence and cellular invasion of the peritumoral liver zone of HCC after TACE.
METHODS Seventy-six patients with 82 HCC nodules were recruited in this study and underwent DKI after TACE. According to pathological examinations or the overall modified response evaluation criteria in solid tumors (mRECIST) criterion, 48 and 34 nodules were divided into true progression and pseudo-progression groups, respectively. The TACE-treated area, peritumoral liver zone, and far-tumoral zone were evaluated on DKI-derived metric maps. Non-parametric U test and receiver operating characteristic curve (ROC) analysis were used to evaluate the prediction performance of each DKI metric between the two groups. The independent t-test was used to compare each DKI metric between the peritumoral and far-tumoral zones of the true progression group.
RESULTS DKI metrics, including mean diffusivity (MD), axial diffusivity (DA), radial diffusivity (DR), axial kurtosis (KA), and anisotropy fraction of kurtosis (Fak), showed statistically different values between the true progression and pseudo-progression groups (P < 0.05). Among these, MD, DA, and DR values were higher in pseudo-progression lesions than in true progression lesions, whereas KA and FAk values were higher in true progression lesions than in pseudo-progression lesions. Moreover, for the true progression group, the peritumoral zone showed significantly different DA, DR, KA, and FAk values from the far-tumoral zone. Furthermore, MD values of the liver parenchyma (peritumoral and far-tumoral zones) were significantly lower in the true progression group than in the pseudo-progression group (P < 0.05).
CONCLUSION DKI has been demonstrated with robust performance in predicting the therapeutic response of HCC to TACE. Moreover, DKI might reveal cellular invasion of the peritumoral zone by molecular diffusion-restricted change.
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Affiliation(s)
- Xin Cao
- Department of Medical Imaging, The First Affiliated Hospital of Shandong First Medical University & Shandong Province Qianfoshan Hospital, Jinan 250014, Shandong Province, China
- Department of Radiology, Huashan Hospital, Fudan University, Shanghai 200040, China
- Center for Shanghai Intelligent Imaging for Critical Brain Diseases Engineering and Technology Research, Shanghai 200040, China
| | - Hao Shi
- Department of Medical Imaging, The First Affiliated Hospital of Shandong First Medical University & Shandong Province Qianfoshan Hospital, Jinan 250014, Shandong Province, China
| | | | - Xin-Yao Zhao
- Department of Radiology, Yantaishan Hospital, Yantai 264001, Shandong Province, China
| | - Ying-Xin Zheng
- Department of Magnetic Resonance Imaging, Zhangqiu District People's Hospital, Jinan 250200, Shandong Province, China
| | - Ya-Ping Ge
- Department of Medical Imaging, The First Affiliated Hospital of Shandong First Medical University & Shandong Province Qianfoshan Hospital, Jinan 250014, Shandong Province, China
| | - Hai-Chao Cheng
- Department of Medical Imaging, The First Affiliated Hospital of Shandong First Medical University & Shandong Province Qianfoshan Hospital, Jinan 250014, Shandong Province, China
| | - Dao-Ying Geng
- Department of Radiology, Huashan Hospital, Fudan University, Shanghai 200040, China
- Center for Shanghai Intelligent Imaging for Critical Brain Diseases Engineering and Technology Research, Shanghai 200040, China
| | - Jun-Ying Wang
- Department of Medical Imaging, The First Affiliated Hospital of Shandong First Medical University & Shandong Province Qianfoshan Hospital, Jinan 250014, Shandong Province, China
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Qiu C, Xie S, Sun Y, Yu Y, Zhang K, Wang X, Zhu J, Grimm R, Shen W. Multi-parametric magnetic resonance imaging of liver regeneration in a standardized partial hepatectomy rat model. BMC Gastroenterol 2022; 22:430. [PMID: 36210451 PMCID: PMC9549623 DOI: 10.1186/s12876-022-02517-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/04/2022] [Accepted: 09/19/2022] [Indexed: 11/10/2022] Open
Abstract
Abstract
Background
We aimed to evaluate the correlation between the pathological changes and multi-parameter MRI characteristics of liver regeneration (LR) in a standard partial hepatectomy (PH) rat model.
Methods
Seventy Sprague–Dawley rats were randomly divided into two groups: MR scan group (n = 14) and pathologic analysis (PA) group (n = 56). All 14 rats in the MR group underwent liver T1 mapping, T2 mapping, and diffusion kurtosis imaging before and the 1st, 2nd, 3rd, 5th, 7th, 14th, and 21st day after 70% hepatectomy. Seven rats in the PA group were euthanized at each time point to determine Ki-67 indices, hepatocyte size (HTS), steatosis grade, and inflammation score.
Results
Liver T1 and T2 values increased to maximum on day 2 (P < 0.001 vs. baseline), D and K values decreased to minimum on day 3 and 2, respectively (P < 0.001 vs. baseline), then all parameters returned to baseline gradually. Hepatocyte Ki-67, hepatocyte size, steatosis grade, and inflammation score initially increased after surgery (P < 0.05 vs. baseline), followed by a gradual decline over time. Both T2 and K values correlated well with Ki-67 indices (r = 0.765 and − 0.807, respectively; both P < 0.001), inflammation (r = 0.809 and − 0.724, respectively; both P < 0.001), steatosis grade (r = 0.814 and − 0.725, respectively; both P < 0.001), and HTS (r = 0.830 and − 0.615, respectively; both P < 0.001).
Conclusions
PH induced liver changes that can be observed on MRI. The MRI parameters correlate with the LR activity and allow monitoring of LR process.
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Granata V, Fusco R, Belli A, Danti G, Bicci E, Cutolo C, Petrillo A, Izzo F. Diffusion weighted imaging and diffusion kurtosis imaging in abdominal oncological setting: why and when. Infect Agent Cancer 2022; 17:25. [PMID: 35681237 PMCID: PMC9185934 DOI: 10.1186/s13027-022-00441-3] [Citation(s) in RCA: 12] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/30/2022] [Accepted: 05/30/2022] [Indexed: 12/13/2022] Open
Abstract
This article provides an overview of diffusion kurtosis (DKI) imaging in abdominal oncology. DKI allows for more data on tissue structures than the conventional diffusion model (DWI). However, DKI requires high quality images at b-values greater than 1000 s/mm2 and high signal-to-noise ratio (SNR) that traditionally MRI systems are not able to acquire and therefore there are generally amplified anatomical distortions on the images due to less homogeneity of the field. Advances in both hardware and software on modern MRI scanners have currently enabled ultra-high b-value imaging and offered the ability to apply DKI to multiple extracranial sites. Previous studies have evaluated the ability of DKI to characterize and discriminate tumor grade compared to conventional DWI. Additionally, in several studies the DKI sequences used were based on planar echo (EPI) acquisition, which is susceptible to motion, metal and air artefacts and prone to low SNRs and distortions, leading to low quality images for some small lesions, which may affect the accuracy of the results. Another problem is the optimal b-value of DKI, which remains to be explored and not yet standardized, as well as the manual selection of the ROI, which could affect the accuracy of some parameters.
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Affiliation(s)
- Vincenza Granata
- Division of Radiology, "Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli", I-80131, Naples, Italy.
| | | | - Andrea Belli
- Division of Hepatobiliary Surgical Oncology, "Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli", I-80131, Naples, Italy
| | - Ginevra Danti
- Department of Radiology, Azienda Ospedaliero-Universitaria Careggi, Florence, Italy.,Italian Society of Medical and Interventional Radiology, SIRM Foundation, Milan, Italy
| | - Eleonora Bicci
- Department of Radiology, Azienda Ospedaliero-Universitaria Careggi, Florence, Italy
| | - Carmen Cutolo
- Department of Medicine, Surgery and Dentistry, University of Salerno, Salerno, Italy
| | - Antonella Petrillo
- Division of Radiology, "Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli", I-80131, Naples, Italy
| | - Francesco Izzo
- Division of Hepatobiliary Surgical Oncology, "Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli", I-80131, Naples, Italy
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Lundholm L, Montelius M, Jalnefjord O, Forssell-Aronsson E, Ljungberg M. VERDICT MRI for radiation treatment response assessment in neuroendocrine tumors. NMR IN BIOMEDICINE 2022; 35:e4680. [PMID: 34957637 DOI: 10.1002/nbm.4680] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 05/20/2021] [Revised: 12/09/2021] [Accepted: 12/10/2021] [Indexed: 06/14/2023]
Abstract
Noninvasive methods to study changes in tumor microstructure enable early assessment of treatment response and thus facilitate personalized treatment. The aim of this study was to evaluate the diffusion MRI model, Vascular, Extracellular and Restricted Diffusion for Cytometry in Tumors (VERDICT), for early response assessment to external radiation treatment and to compare the results with those of more studied sets of parameters derived from diffusion-weighted MRI data. Mice xenografted with human small intestine tumors were treated with external radiation treatment, and diffusion MRI experiments were performed on the day before and up to 2 weeks after treatment. The diffusion models VERDICT, ADC, IVIM, and DKI were fitted to MRI data, and the treatment response of each tumor was calculated based on pretreatment tumor growth and post-treatment tumor volume regression. Linear regression and correlation analysis were used to evaluate each model and their respective parameters for explaining the treatment response. VERDICT analysis showed significant changes from day -1 to day 3 for the intracellular and extracellular volume fraction, as well as the cell radius index (p < 0.05; Wilcoxon signed-rank test). The strongest correlation between the diffusion model parameters and the tumor treatment response was seen for the ADC, kurtosis-corrected diffusion coefficient, and intracellular volume fraction on day 3 (τ = 0.47, 0.52, and -0.49, respectively, p < 0.05; Kendall rank correlation coefficient). Of all the tested models, VERDICT held the strongest explanatory value for the tumor treatment response on day 3 (R2 = 0.75, p < 0.01; linear regression). In conclusion, VERDICT has potential for early assessment of external radiation treatment and may provide further insights into the underlying biological effects of radiation on tumor tissue. In addition, the results suggest that the time window for assessment of treatment response using dMRI may be narrow.
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Affiliation(s)
- Lukas Lundholm
- Department of Medical Radiation Sciences, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
| | - Mikael Montelius
- Department of Medical Radiation Sciences, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
| | - Oscar Jalnefjord
- Department of Medical Radiation Sciences, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Department of Medical Physics and Biomedical Engineering, MRI Center, Sahlgrenska University Hospital, Gothenburg, Sweden
| | - Eva Forssell-Aronsson
- Department of Medical Radiation Sciences, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Department of Medical Physics and Biomedical Engineering, MRI Center, Sahlgrenska University Hospital, Gothenburg, Sweden
| | - Maria Ljungberg
- Department of Medical Radiation Sciences, Institute of Clinical Sciences, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden
- Department of Medical Physics and Biomedical Engineering, MRI Center, Sahlgrenska University Hospital, Gothenburg, Sweden
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Comparison of the Effects of Hepatic Steatosis on Monoexponential DWI, Intravoxel Incoherent Motion Diffusion-weighted Imaging and Diffusion Kurtosis Imaging. Acad Radiol 2021; 28 Suppl 1:S203-S209. [PMID: 34119399 DOI: 10.1016/j.acra.2021.04.016] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/30/2020] [Revised: 03/30/2021] [Accepted: 04/05/2021] [Indexed: 12/15/2022]
Abstract
RATIONALE AND OBJECTIVES Diffusion-weighted imaging (DWI) techniques have drawn attention for their capability of staging hepatic fibrosis. However, the diagnostic performance of DWI for hepatic fibrosis might be affected by hepatic steatosis because hepatic steatosis and fibrosis may have a similar effect on diffusion/perfusion parameters. Therefore, the purpose of our study is to investigate the effect of hepatic steatosis on DWI parameters. MATERIALS AND METHODS 51 patients with MR elastography liver stiffness values below 3.45kPa underwent DWI with multiple b-values and a multi-echo Dixon sequence for fat quantification. Correlation analysis was conducted between fat fraction and DWI parameters, and DWI parameters were compared between steatosis and non-steatosis groups. RESULTS Significant negative correlation was observed between fat fraction and apparent diffusion coefficient (ADC) (r = -0.62, p <0.001), pure molecular diffusion (D) (r = -0.62, p <0.001), corrected ADC (Dapp) (r = -0.36, p = 0.01) and a positive correlation with mean kurtosis (Kapp) (r = 0.53, p <0.001). The results of the comparison of DWI parameters were that ADC, D and Dapp were statistically lower in the steatosis group (p < 0.001, p < 0.001 and p = 0.026, respectively) and Kapp was significantly higher in the steatosis group (p <0.001) compared to the non-steatosis group. However, perfusion-related parameters (D* and f) did not show any statistical significance. CONCLUSION DWI parameters except for perfusion-related parameters (D* and f) are affected by changes in hepatic steatosis. Thus, hepatic steatosis may be considered as a possible confounding factor in DWI-based assessment of liver fibrosis.
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Xu H, Zhang N, Yang DW, Ren A, Ren H, Zhang Q, Zhu JX, Li GJ, Yang ZH. Feasibility study of simultaneous multislice diffusion kurtosis imaging with different acceleration factors in the liver. BMC Med Imaging 2021; 21:132. [PMID: 34503482 PMCID: PMC8431937 DOI: 10.1186/s12880-021-00661-w] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/31/2021] [Accepted: 08/28/2021] [Indexed: 12/02/2022] Open
Abstract
Background Simultaneous multislice diffusion-weighted imaging (SMS-DWI) has been used to reduce image acquisition time. The purpose of this study was to investigate the feasibility of diffusion kurtosis imaging (DKI) based on the SMS technique in the liver and the influence of this method compared with that of conventional DWI sequences on image quality and DKI-derived quantitative parameters. Methods Forty volunteers underwent SMS-DWI sequences with acceleration factors of 2 and 3 (SMS2-DWI, SMS3-DWI) and conventional DWI (C-DWI) of the liver with three b-values (50, 800, 2000 s/mm2) in a 3T system. Qualitative image quality parameters and quantitative measurements of the signal-to-noise ratio (SNR), mean kurtosis (MK), mean apparent diffusivity (MD) and apparent diffusion coefficient (ADC) for the liver were compared between the three sequences. Results The scan times of C-DWI, SMS2-DWI, and SMS3-DWI were 4 min 11 s, 2 min 2 s, and 1 min 34 s, respectively. For all image quality parameters, there were no significant differences observed between C-DWI and SMS2-DWI (all p > 0.05) in the images with b-values of 800 and 2000 s/mm2. C-DWI and SMS2-DWI exhibited better scores than SMS3-DWI (all p < 0.01) in the images with b-values of 2000 s/mm2. In the images with b-values of 800 s/mm2, C-DWI and SMS2-DWI exhibited better scores than SMS3-DWI for artefacts and overall image quality (all p < 0.01), and C-DWI exhibited better scores than SMS3-DWI for the visibility of intrahepatic vessels (p < 0.001). There were no significant differences in the sharpness of the right lobe edge (p = 0.144), conspicuity of the left lobe (p = 0.370) or visibility of intrahepatic vessels (p = 0.109) between SMS2-DWI and SMS3-DWI. There were no significant differences in the sharpness of the right lobe edge (p = 0.066) or conspicuity of the left lobe (p = 0.131) between C-DWI and SMS3-DWI. For the b-value of 800 s/mm2, there were no statistically significant differences between SMS2-DWI and C-DWI (p = 1.000) or between SMS2-DWI and SMS3-DWI (p = 0.059), whereas SMS3-DWI had a significantly lower SNR than C-DWI (p = 0.024). For the DKI-derived parameters (MK and MD) and ADC values, there were no significant differences between the three sequences (MK, p = 0.606; MD, p = 0.831; ADC, p = 0.264). Conclusions SMS-DWI with an acceleration factor of 2 is feasible for the liver, resulting in considerable reductions in scan time while maintaining similar image quality, comparable DKI parameters and ADC values compared with those of C-DWI.
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Affiliation(s)
- Hui Xu
- Department of Radiology, Beijing Friendship Hospital, Capital Medical University, 95 Yong an Road, Xicheng District, Beijing, 100050, China
| | - Nan Zhang
- Department of Radiology, Beijing Friendship Hospital, Capital Medical University, 95 Yong an Road, Xicheng District, Beijing, 100050, China
| | - Da-Wei Yang
- Department of Radiology, Beijing Friendship Hospital, Capital Medical University, 95 Yong an Road, Xicheng District, Beijing, 100050, China
| | - Ahong Ren
- Department of Radiology, Beijing Friendship Hospital, Capital Medical University, 95 Yong an Road, Xicheng District, Beijing, 100050, China
| | - Hao Ren
- Department of Radiology, Beijing Friendship Hospital, Capital Medical University, 95 Yong an Road, Xicheng District, Beijing, 100050, China
| | - Qian Zhang
- Clinical Epidemiology and EBM Unit, Beijing Friendship Hospital, Capital Medical University, Beijing, 100050, China
| | - Jin-Xia Zhu
- MR Collaboration, Siemens Healthineers Ltd., Beijing, China
| | - Gui-Jin Li
- MR Application, Siemens Healthineers Ltd., Guangzhou, China
| | - Zheng-Han Yang
- Department of Radiology, Beijing Friendship Hospital, Capital Medical University, 95 Yong an Road, Xicheng District, Beijing, 100050, China.
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Granata V, Grassi R, Fusco R, Belli A, Cutolo C, Pradella S, Grazzini G, La Porta M, Brunese MC, De Muzio F, Ottaiano A, Avallone A, Izzo F, Petrillo A. Diagnostic evaluation and ablation treatments assessment in hepatocellular carcinoma. Infect Agent Cancer 2021; 16:53. [PMID: 34281580 PMCID: PMC8287696 DOI: 10.1186/s13027-021-00393-0] [Citation(s) in RCA: 30] [Impact Index Per Article: 7.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/15/2021] [Accepted: 07/06/2021] [Indexed: 02/07/2023] Open
Abstract
This article provides an overview of diagnostic evaluation and ablation treatment assessment in Hepatocellular Carcinoma (HCC). Only studies, in the English language from January 2010 to January 202, evaluating the diagnostic tools and assessment of ablative therapies in HCC patients were included. We found 173 clinical studies that satisfied the inclusion criteria.HCC may be noninvasively diagnosed by imaging findings. Multiphase contrast-enhanced imaging is necessary to assess HCC. Intravenous extracellular contrast agents are used for CT, while the agents used for MRI may be extracellular or hepatobiliary. Both gadoxetate disodium and gadobenate dimeglumine may be used in hepatobiliary phase imaging. For treatment-naive patients undergoing CT, unenhanced imaging is optional; however, it is required in the post treatment setting for CT and all MRI studies. Late arterial phase is strongly preferred over early arterial phase. The choice of modality (CT, US/CEUS or MRI) and MRI contrast agent (extracelllar or hepatobiliary) depends on patient, institutional, and regional factors. MRI allows to link morfological and functional data in the HCC evaluation. Also, Radiomics is an emerging field in the assessment of HCC patients.Postablation imaging is necessary to assess the treatment results, to monitor evolution of the ablated tissue over time, and to evaluate for complications. Post- thermal treatments, imaging should be performed at regularly scheduled intervals to assess treatment response and to evaluate for new lesions and potential complications.
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Affiliation(s)
- Vincenza Granata
- Division of Radiology, Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli, Naples, Italy
| | - Roberta Grassi
- Division of Radiology, Università degli Studi della Campania Luigi Vanvitelli, Naples, Italy
- Italian Society of Medical and Interventional Radiology SIRM, SIRM Foundation, Milan, Italy
| | | | - Andrea Belli
- Division of Hepatobiliary Surgical Oncology, Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli, Naples, Italy
| | - Carmen Cutolo
- Department of Medicine, Surgery and Dentistry, University of Salerno, Salerno, Italy
| | - Silvia Pradella
- Radiology Division, Azienda Ospedaliero-Universitaria Careggi, Florence, Italy
| | - Giulia Grazzini
- Radiology Division, Azienda Ospedaliero-Universitaria Careggi, Florence, Italy
| | | | - Maria Chiara Brunese
- Department of Medicine and Health Sciences "Vincenzo Tiberio", University of Molise, Campobasso, Italy
| | - Federica De Muzio
- Department of Medicine and Health Sciences "Vincenzo Tiberio", University of Molise, Campobasso, Italy
| | - Alessandro Ottaiano
- Abdominal Oncology Division, Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli, Naples, Italy
| | - Antonio Avallone
- Abdominal Oncology Division, Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli, Naples, Italy
| | - Francesco Izzo
- Division of Hepatobiliary Surgical Oncology, Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli, Naples, Italy
| | - Antonella Petrillo
- Division of Radiology, Istituto Nazionale Tumori IRCCS Fondazione Pascale - IRCCS di Napoli, Naples, Italy
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Evaluation of Synovitis of Hand in Patients With Rheumatoid Arthritis Using Diffusion Kurtosis Magnetic Resonance Imaging: Initial Findings. J Comput Assist Tomogr 2021; 45:557-563. [PMID: 34176880 DOI: 10.1097/rct.0000000000001176] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/09/2023]
Abstract
OBJECTIVE To explore the role of diffusion kurtosis magnetic resonance (MR) imaging in the noninvasive identification of synovitis in hand arthritis. METHODS A total of 30 patients with rheumatoid arthritis (RA) and 10 patients suspected of RA were enrolled in the prospective study. A 3.0-T MR imaging including the diffusion kurtosis MR imaging sequence (b = 0, 500, 1000, 1500, 2000 s·mm2) was performed. A total of 210 regions of interest were confirmed and diffusion kurtosis MR imaging parameters were generated. The suspected synovitis or effusion was scored on a scale of 0 (effusion) to 3 (mild, moderate, severe synovitis), according to RA-MR imaging scoring system. The performance of diffusion kurtosis MR imaging parameters (the apparent diffusion coefficient [ADC], diffusion coefficient [D], and kurtosis [K]) in distinguishing different synovitis scores was evaluated. RESULTS There were significant differences in ADC, D, and K values among different synovitis scores (all P < 0.001). Synovitis scores were negatively correlated with the ADC and D values significantly (r = -0.725, -0.757, respectively, all P < 0.001), but positively correlated with the K values significantly (r = 0.429, P < 0.001). The area under the curve values of D, ADC, and K values were 0.884, 0.874, and 0.728 for differentiating score 1-3 from score 0, respectively. Diffusion coefficient and ADC had similar diagnostic performance, and both were higher than K in detecting synovitis. No significant difference was found between the ADC and D values in detecting synovitis. CONCLUSIONS The diffusion kurtosis MR imaging may be feasible as a noninvasive method for the diagnosis and grading of synovitis in the hands of RA patients, and the D and ADC values showed similar diagnostic performance, both of which were higher than K values.
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The Role of Non-Gaussian Models of Diffusion Weighted MRI in Hepatocellular Carcinoma: A Systematic Review. J Clin Med 2021; 10:jcm10122641. [PMID: 34203995 PMCID: PMC8232758 DOI: 10.3390/jcm10122641] [Citation(s) in RCA: 9] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/07/2021] [Revised: 06/10/2021] [Accepted: 06/14/2021] [Indexed: 12/14/2022] Open
Abstract
The importance of Diffusion Weighted Imaging (DWI) in hepatocellular carcinoma (HCC) has been widely handled in the literature. Due to the mono-exponential model limitations, several studies recently investigated the role of non-Gaussian DWI models in HCC. However, their results are variable and inconsistent. Therefore, the aim of this systematic review is to summarize current knowledge on non-Gaussian DWI techniques in HCC. A systematic search of the literature, including PubMed, Google Scholar, MEDLINE, and ScienceDirect databases, was performed to identify original articles since 2010 that evaluated the role of non-Gaussian DWI models for HCC diagnosis, grading, response to treatment, and prognosis. Studies were grouped and summarized according to the non-Gaussian DWI models investigated. We focused on the most used non-Gaussian DWI models (Intravoxel Incoherent Motion (IVIM), Diffusion Kurtosis Imaging (DKI), and Stretched Exponential—SE). The quality of included studies was evaluated by using QUADAS-2 and QUIPS tools. Forty-three articles were included, with IVIM and DKI being the most investigated models. Although the role of non-Gaussian DWI models in clinical settings has not fully been established, our findings showed that their parameters may potentially play a role in HCC. Further studies are required to identify a standardized DWI acquisition protocol for HCC diagnosis, grading, response to treatment, and prognosis.
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Zhang J, Lemberskiy G, Moy L, Fieremans E, Novikov DS, Kim SG. Measurement of cellular-interstitial water exchange time in tumors based on diffusion-time-dependent diffusional kurtosis imaging. NMR IN BIOMEDICINE 2021; 34:e4496. [PMID: 33634508 PMCID: PMC8170918 DOI: 10.1002/nbm.4496] [Citation(s) in RCA: 12] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 10/03/2020] [Accepted: 02/08/2021] [Indexed: 05/10/2023]
Abstract
PURPOSE To assess the feasibility of using diffusion-time-dependent diffusional kurtosis imaging (tDKI) to measure cellular-interstitial water exchange time (τex ) in tumors, both in animals and in humans. METHODS Preclinical tDKI studies at 7 T were performed with the GL261 glioma model and the 4T1 mammary tumor model injected into the mouse brain. Clinical studies were performed at 3 T with women who had biopsy-proven invasive ductal carcinoma. tDKI measurement was conducted using a diffusion-weighted STEAM pulse sequence with multiple diffusion times (20-800 ms) at a fixed echo time, while keeping the b-values the same (0-3000 s/mm2 ) by adjusting the diffusion gradient strength. The tDKI data at each diffusion time t were used for a weighted linear least-squares fit method to estimate the diffusion-time-dependent diffusivity, D(t), and diffusional kurtosis, K(t). RESULTS Both preclinical and clinical studies showed that, when diffusion time t ≥ 200 ms, D(t) did not have a noticeable change while K(t) decreased monotonically with increasing diffusion time in tumors and t ≥ 100 ms for the cortical ribbon of the mouse brain. The estimated τex averaged median and interquartile range (IQR) of GL261 and 4T1 tumors were 93 (IQR = 89) ms and 68 (78) ms, respectively. For the cortical ribbon, the estimated τex averaged median and IQR were 41 (34) ms for C57BL/6 and 30 (17) ms for BALB/c. For invasive ductal carcinoma, the estimated τex median and IQR of the two breast cancers were 70 (94) and 106 (92) ms. CONCLUSION The results of this proof-of-concept study substantiate the feasibility of using tDKI to measure cellular-interstitial water exchange time without using an exogenous contrast agent.
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Affiliation(s)
- Jin Zhang
- Center for Biomedical Imaging (CBI), Center for Advanced Imaging Innovation and Research (CAI2R), Department of Radiology, New York University School of Medicine, New York, New York, USA
- Department of Radiology, Weill Cornell Medical College, New York, New York, USA
| | - Gregory Lemberskiy
- Center for Biomedical Imaging (CBI), Center for Advanced Imaging Innovation and Research (CAI2R), Department of Radiology, New York University School of Medicine, New York, New York, USA
| | - Linda Moy
- Center for Biomedical Imaging (CBI), Center for Advanced Imaging Innovation and Research (CAI2R), Department of Radiology, New York University School of Medicine, New York, New York, USA
| | - Els Fieremans
- Center for Biomedical Imaging (CBI), Center for Advanced Imaging Innovation and Research (CAI2R), Department of Radiology, New York University School of Medicine, New York, New York, USA
| | - Dmitry S Novikov
- Center for Biomedical Imaging (CBI), Center for Advanced Imaging Innovation and Research (CAI2R), Department of Radiology, New York University School of Medicine, New York, New York, USA
| | - Sungheon Gene Kim
- Center for Biomedical Imaging (CBI), Center for Advanced Imaging Innovation and Research (CAI2R), Department of Radiology, New York University School of Medicine, New York, New York, USA
- Department of Radiology, Weill Cornell Medical College, New York, New York, USA
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Mao W, Ding Y, Ding X, Fu C, Zeng M, Zhou J. Diffusion kurtosis imaging for the assessment of renal fibrosis of chronic kidney disease: A preliminary study. Magn Reson Imaging 2021; 80:113-120. [PMID: 33971241 DOI: 10.1016/j.mri.2021.05.002] [Citation(s) in RCA: 15] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/02/2020] [Revised: 04/30/2021] [Accepted: 05/05/2021] [Indexed: 01/18/2023]
Abstract
PURPOSE To investigate the potential of diffusion kurtosis imaging (DKI) for the assessment of renal fibrosis in chronic kidney disease (CKD), using histopathology as the reference standard. METHODS Eighty-nine CKD patients and twenty healthy volunteers were recruited in this study. DKI was performed in all participants and all CKD patients received renal biopsy. The values of mean diffusivity (MD) and mean kurtosis (MK) in the renal cortex and medulla were compared between CKD patients and healthy volunteers. The Spearman correlation coefficient was calculated to assess the relationship between MD, MK values and the estimated glomerular filtration rate (eGFR), serum creatinine (SCr), 24 h urinary protein (24 h-UPRO), histopathological fibrosis score. RESULTS The medullary MD values were significantly lower than cortex, while the cortical MK values were significantly lower than medulla for all participants. Renal parenchymal MD values were significantly lower in the CKD patients than healthy controls, whereas MK values were significantly higher in the CKD patients than healthy controls. In the CKD patients, the significantly negative correlation was observed between the renal parenchymal MD values and the 24 h-UPRO, SCr, histopathological fibrosis score, as well as between the renal parenchymal MK values and the eGFR, while the significantly positive correlation was found between the renal parenchymal MD values and the eGFR, as well as between the renal parenchymal MK values and the 24 h-UPRO, SCr, histopathological fibrosis score. CONCLUSION DKI shows great potential in the noninvasive assessment of renal fibrosis in CKD.
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Affiliation(s)
- Wei Mao
- Department of Radiology, Zhongshan Hospital, Fudan University; Shanghai Institute of Medical Imaging, 180 Fenglin Road, Shanghai 200032, People's Republic of China
| | - Yuqin Ding
- Department of Radiology, Zhongshan Hospital, Fudan University; Shanghai Institute of Medical Imaging, 180 Fenglin Road, Shanghai 200032, People's Republic of China
| | - Xiaoqiang Ding
- Department of Nephrology, Zhongshan Hospital, Fudan University; 180 Fenglin Road, Shanghai 200032, People's Republic of China
| | - Caixia Fu
- Siemens Shenzhen Magnetic Resonance Ltd, Shenzhen, People's Republic of China
| | - Mengsu Zeng
- Department of Radiology, Zhongshan Hospital, Fudan University; Shanghai Institute of Medical Imaging, 180 Fenglin Road, Shanghai 200032, People's Republic of China.
| | - Jianjun Zhou
- Department of Radiology, Zhongshan Hospital, Fudan University; Shanghai Institute of Medical Imaging, 180 Fenglin Road, Shanghai 200032, People's Republic of China; Department of Radiology, Xiamen Branch, Zhongshan Hospital, Fudan University, Xiamen, China.
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Mao W, Ding Y, Ding X, Wang Y, Fu C, Zeng M, Zhou J. Pathological assessment of chronic kidney disease with DWI: Is there an added value for diffusion kurtosis imaging? J Magn Reson Imaging 2021; 54:508-517. [PMID: 33634937 DOI: 10.1002/jmri.27569] [Citation(s) in RCA: 23] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/07/2020] [Revised: 02/04/2021] [Accepted: 02/04/2021] [Indexed: 12/18/2022] Open
Abstract
BACKGROUND Chronic kidney disease (CKD) is a worldwide health problem, precise functional and pathological assessment is beneficial to better treatment. Diffusion kurtosis imaging (DKI) can evaluate non-Gaussian diffusion and may help to assess renal pathology and function. PURPOSE To assess pathological and functional alterations in CKD using DKI compared with diffusion-weighted imaging (DWI). STUDY TYPE Prospective study. POPULATION 70 CKD patients and 20 healthy volunteers. FIELD STRENGTH 1.5 T. ASSESSMENT All participants underwent DKI, and apparent diffusion coefficient (ADC), mean diffusivity (MD), and mean kurtosis (MK) of renal parenchyma were acquired. Correlation between renal parenchymal ADC, MD, MK, and estimated glomerular filtration rate (eGFR), pathological scores were assessed. The diagnostic efficacy of ADC, MD, and MK for assessing the degree of renal pathological injury were compared. STATISTICAL TESTS ANOVA, Spearman correlation analysis, and ROC curve analysis. RESULTS The cortical ADC, MD were significantly higher than medulla for all participants, whereas medullary MK was significantly higher than cortex (P < 0.01). Whether eGFR reduced or not, renal parenchymal MK were significantly higher in patients than controls (P < 0.05). Positive correlation was found between eGFR and ADC (cortex, r = 0.562; medulla, r = 0.527), and negative correlation between eGFR and MK (cortex, r = -0.786; medulla, r = -0.709) (all P < 0.001). There was positive correlation between MK and glomerular injury (cortex, r = 0.681; medulla, r = 0.652), tubulointerstitial lesion (cortex, r = 0.650; medulla, r = 0.599) (all P < 0.001). For discrimination between mild and m-s renal injury group, the AUC values of ADC, MD, MK were cortex: 0.723, 0.655, 0.864 and medulla: 0.718, 0.581, 0.829. The AUC values of ADC, MD, MK were cortex: 0.708, 0.679, 0.770 and medulla: 0.713, 0.830, 0.780 for differentiating control group from mild renal injury group. DATA CONCLUSION DKI is practicable for noninvasive assessment of renal pathology and function of CKD, DKI offer better diagnostic performance than DWI. Evidence Level 1 Technical Efficacy 2.
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Affiliation(s)
- Wei Mao
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, 200032, China
| | - Yuqin Ding
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, 200032, China
| | - Xiaoqiang Ding
- Department of Nephrology, Zhongshan Hospital, Fudan University, Shanghai, 200032, China
| | - Yaqiong Wang
- Department of Nephrology, Zhongshan Hospital, Fudan University, Shanghai, 200032, China
| | - Caixia Fu
- Siemens Shenzhen Magnetic Resonance Ltd., Shenzhen, China
| | - Mengsu Zeng
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, 200032, China
| | - Jianjun Zhou
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, 200032, China.,Department of Radiology, Xiamen Branch, Zhongshan Hospital, Fudan University, Xiamen, China
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Lai LY, Huang MP, Su S, Shu J. Liver Fibrosis Staging with Gadolinium Ethoxybenzyl Diethylenetriamine Penta-Acetic Acid-enhanced: A Systematic Review and Meta-analysis. Curr Med Imaging 2020; 17:854-863. [PMID: 33256584 DOI: 10.2174/1573405616666201130101229] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/26/2020] [Revised: 07/25/2020] [Accepted: 08/09/2020] [Indexed: 11/22/2022]
Abstract
OBJECTIVE While liver biopsy is the golden standard for liver-fibrosis diagnosis, it is also invasive and has many limitations. Non-invasive techniques such as Magnetic Resonance Imaging (MRI) need to be further developed for liver fibrosis staging. This study aimed to evaluate the diagnostic accuracy of Gadolinium Ethoxybenzyl Diethylenetriamine Penta-acetic Acid (Gd-EOBDTPA)- enhanced MRI for liver fibrosis through systematic review and meta-analysis. METHODS This study comprehensively searched relevant article in PubMed, Embase, and the Cochrane Library published from 2004 to 2018 to find studies analyzing the diagnostic accuracy of Gd-EOB-DTPA-enhanced MRI for liver fibrosis. Two reviewers independently screened the retrieved articles, extracted the required data from the included studies, and evaluated the methodological quality of the studies. The pooled sensitivity, specificity, positive likelihood ratio, negative likelihood ratio, diagnostic odds ratio, and Summary Receiver Operating Characteristics (SROC) curve were assessed. RESULTS This study finally included 16 studies (n = 1,599) and selected a random-effects model based on the results of the I2 statistic to combine them. The areas under the SROC curve for the detection of F1 or greater, F2 or greater, F3 or greater, or F4 liver fibrosis were 0.8669, 0.8399, 0.8481, and 0.8858, respectively. CONCLUSION Gd-EOB-DTPA-enhanced MRI showed a good diagnostic performance for staging liver fibrosis, especially for F4 liver fibrosis.
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Affiliation(s)
- Lu-Yao Lai
- Department of Radiology, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan, China
| | - Meng-Ping Huang
- Department of Radiology, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan, China
| | - Song Su
- Department of Hepatobiliary Surgery, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan, China
| | - Jian Shu
- Department of Radiology, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan, China
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Cruz M, Ferreira AA, Papanikolaou N, Banerjee R, Alves FC. New boundaries of liver imaging: from morphology to function. Eur J Intern Med 2020; 79:12-22. [PMID: 32571581 DOI: 10.1016/j.ejim.2020.06.004] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/05/2020] [Revised: 05/20/2020] [Accepted: 06/04/2020] [Indexed: 12/12/2022]
Abstract
From an invisible organ to one of the most explored non-invasively, the liver is, today, one of the cornerstones for current cross-sectional imaging techniques and minimally invasive procedures. After the achievements of US, CT and, most recently, MRI in providing highly accurate morphological and structural information about the organ, a significant scientific development has gained momentum for the last decades, coupling morphology to liver function and contributing far most to what we know today as precision medicine. In fact, dedicated tailor-made investigations are now possible in order to detect and, most of all, quantify physiopathological processes with unprecedented certitude. It is the intention of this review to provide a better insight to the reader of several functional imaging techniques applied to liver imaging. Contrast enhanced imaging, diffusion weighted imaging, elastography, spectral computed tomography and fat and iron assessment techniques are commonly performed clinically. Diffusion kurtosis imaging, magnetic resonance spectroscopy, T1 relaxometry and radiomics remain largely limited to advanced clinical research. Each of them has its own value and place on the diagnostic armamentarium and provide unique qualitative and quantitative information regarding the pathophysiology of diseases, contributing at a large scale to model therapeutic decisions and patient follow-up. Therefore, state-of-the-art liver imaging acts today as a non-invasive surrogate biomarker of many focal and diffuse liver diseases.
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Affiliation(s)
- Manuel Cruz
- Department of Radiology, Faculty of Medicine, University Hospital Coimbra and CIBIT/ICNAS research center, University of Coimbra, Coimbra, Portugal.
| | - Ana Aguiar Ferreira
- Department of Radiology, Faculty of Medicine, University Hospital Coimbra and CIBIT/ICNAS research center, University of Coimbra, Coimbra, Portugal
| | - Nikolaos Papanikolaou
- Computational Clinical Imaging Group, Centre for the Unknown, Champalimaud Foundation, Lisbon, Portugal
| | - Rajarshi Banerjee
- Department of Acute Medicine, Oxford University Hospitals NHS Trust, Oxford, United Kingdom
| | - Filipe Caseiro Alves
- Department of Radiology, Faculty of Medicine, University Hospital Coimbra and CIBIT/ICNAS research center, University of Coimbra, Coimbra, Portugal
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Xie S, Li Q, Cheng Y, Zhou L, Xia S, Li J, Shen W. Differentiating mild and substantial hepatic fibrosis from healthy controls: a comparison of diffusion kurtosis imaging and conventional diffusion-weighted imaging. Acta Radiol 2020; 61:1012-1020. [PMID: 31825764 DOI: 10.1177/0284185119889566] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
Abstract
BACKGROUND Early and accurate detection of liver fibrosis are important for clinical treatment. PURPOSE To compare the diagnostic accuracy of liver diffusion kurtosis imaging (DKI) and conventional diffusion-weighted imaging (cDWI) in differentiating patients with mild and substantial fibrosis from normal individuals. MATERIAL AND METHODS Twenty-seven healthy volunteers with no fibrosis (S0) and 45 patients with mild (S1) or substantial (S2) liver fibrosis underwent DWI with multiple b-values. Liver mean apparent diffusion (MD) and mean kurtosis (MK) values derived from DKI and apparent diffusion coefficient (ADC) derived from cDWI were measured and compared. Their discriminative abilities were analyzed and compared by receiver operating characteristic (ROC) curve analysis. RESULTS Significant differences in MD and ADC values were found between groups (P < 0.05). MD value was statistically different between S0 and S1 (P = 0.028) and S0 and S2 (P = 0.005). ADC value was statistically different between S0 and S2 (P = 0.012). MK value was similar between groups (P = 0.646). MD and ADC values significantly correlated with fibrosis stages (rs = -0.668, -0.341; P < 0.01). MK values had no correlation with fibrosis stages (rs = 0.180; P = 0.130). The area under ROC curves (AUC) for MD and ADC was 0.937 and 0.707 for characterization of S1-2 and 0.817 and 0.658 for S2, respectively. MD performed better than ADC for characterization of S1-2 and S2 (P < 0.05). CONCLUSION Differentiating patients with mild or substantial fibrosis from normal individuals is feasible using DKI, which performs better than cDWI.
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Affiliation(s)
- Shuangshuang Xie
- Department of Radiology, Tianjin First Central Hospital, Tianjin Imaging Medical Institute, Nankai District, Tianjin, PR China
| | - Qing Li
- Department of Radiology, Tianjin First Central Hospital, Tianjin Imaging Medical Institute, Nankai District, Tianjin, PR China
| | - Yue Cheng
- Department of Radiology, Tianjin First Central Hospital, Tianjin Imaging Medical Institute, Nankai District, Tianjin, PR China
| | - Li Zhou
- Department of Hepatology, Tianjin Second People’s Hospital, Nankai District, Tianjin, PR China
| | - Shuang Xia
- Department of Radiology, Tianjin First Central Hospital, Tianjin Imaging Medical Institute, Nankai District, Tianjin, PR China
| | - Jia Li
- Department of Hepatology, Tianjin Second People’s Hospital, Nankai District, Tianjin, PR China
| | - Wen Shen
- Department of Radiology, Tianjin First Central Hospital, Tianjin Imaging Medical Institute, Nankai District, Tianjin, PR China
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Wang GZ, Guo LF, Gao GH, Li Y, Wang XZ, Yuan ZG. Magnetic Resonance Diffusion Kurtosis Imaging versus Diffusion-Weighted Imaging in Evaluating the Pathological Grade of Hepatocellular Carcinoma. Cancer Manag Res 2020; 12:5147-5158. [PMID: 32636677 PMCID: PMC7334009 DOI: 10.2147/cmar.s254371] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/18/2020] [Accepted: 05/21/2020] [Indexed: 12/27/2022] Open
Abstract
Purpose To investigate the diagnostic efficacy of diffusion kurtosis imaging (DKI) and conventional diffusion-weighted imaging (DWI) for pathological grading. Methods From December 2015 to January 2017, consecutive patients suspected of having hepatocellular carcinoma (HCC) without prior treatment were prospectively enrolled in this study. MRI examinations were performed before surgical treatment. HCC patients confirmed by surgical pathology were included in the study. The mean diffusivity (MD) values, mean kurtosis (MK) values, and apparent diffusion coefficient (ADC) were calculated. The differences and correlations of these parameters among different pathological grades were analyzed. The diagnostic efficiency of DKI and DWI for predicting high-grade HCC was evaluated by receiver operating characteristic (ROC) curves. Logistic regression analyses were used to evaluate the predictive factors for pathological grade. Results A total of 128 patients (79 males and 49 females, age: 56.9±10.9 years, range, 32–80) with primary HCC were included: grade I: 22 (17.2%) patients, grade II: 37 (28.9%) patients, grade III: 43 (33.6%) patients, grade IV: 26 (20.3%) patients. The MK values of stage I, II, III, and IV were 0.86±0.13, 1.06±0.11, 1.27±0.17, and 1.57±0.13, respectively. The MK values were significantly higher in the high-grade group than in the low-grade group and were positively correlated with pathological grade (rho =0.7417, P<0.001). The MK value demonstrated a larger area under the curve (AUC), with a value of 0.93 than the MD value, which had an AUC of 0.815 (P<0.001), and ADC, which had an AUC of 0.662 (P=0.01). The MK value (>1.19), ADC (≤1.29×10–3 mm2/s), and HBV (+) were independent predictors for the pathological grade of HCCs. Conclusion The MK values derived from DKI and the ADC values obtained from traditional DWI were more valuable than the MD values in predicting the histological grade of HCCs and could potentially guide clinical treatment before surgery.
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Affiliation(s)
- Guang-Zhi Wang
- Cheeloo College of Medicine, Shandong University, Jinan 250021, People's Republic of China.,Department of Medical Imaging Center, Affiliated Hospital, Weifang Medical University, Weifang 261053, People's Republic of China
| | - Ling-Fei Guo
- Department of MRI, Shandong Medical Imaging Research Institute, Cheeloo College of Medicine, Shandong University, Jinan 250021, People's Republic of China
| | - Gui-Hua Gao
- Department of MRI, Shandong Medical Imaging Research Institute, Cheeloo College of Medicine, Shandong University, Jinan 250021, People's Republic of China
| | - Yao Li
- Zhucheng People's Hospital Affiliated to Weifang Medical University, Weifang 262200, People's Republic of China
| | - Xi-Zhen Wang
- Department of Medical Imaging Center, Affiliated Hospital, Weifang Medical University, Weifang 261053, People's Republic of China
| | - Zhen-Guo Yuan
- Cheeloo College of Medicine, Shandong University, Jinan 250021, People's Republic of China.,Department of MRI, Shandong Medical Imaging Research Institute, Cheeloo College of Medicine, Shandong University, Jinan 250021, People's Republic of China
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Zhang G, Li W, Wang G, He X, Xu L, Wang S, Peng W. Multimode tumor ablation therapy induced different diffusion and microvasculature related parameters change on functional magnetic resonance imaging compared to radiofrequency ablation in liver tumor: An observational study. Medicine (Baltimore) 2020; 99:e20795. [PMID: 32590762 PMCID: PMC7329015 DOI: 10.1097/md.0000000000020795] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/22/2022] Open
Abstract
To explore different posttreatment changes between multimode tumor ablation therapy (MTAT) and radiofrequency ablation (RFA) using intravoxel incoherent motion diffusion-weighted imaging (IVIM-DWI) and diffusion kurtosis imaging (DKI) in patients with hepatic malignancies.Eighty - seven patients with one hundred and twenty eight hepatic lesions receiving MTAT or RFA underwent IVIM-DWI and DKI before and after treatment. The mean value of apparent diffusion coefficient (ADC), IVIM-DWI parameters, including true diffusion coefficient (D), pseudo-diffusion coefficient (DP), perfusion fraction (f), and DKI parameters including diffusion coefficient (DK), apparent diffusional kurtosis (K) were retrospectively compared prior to and following treatment as well as between treatment groups. The degree of parameters change after ablation was compared between 2 treatment modalities.The mean value of ADC, D, and DK increased while f, and K decreased significantly in MTAT group. In RFA group, just ADC and K showed significantly change following treatment. The ADC and D value were higher in MTAT group than in RFA group 1 month after treatment. While f was lower in MTAT group after treatment compared with RFA group. The ADC, D and DK increased (21.89 ± 24.95% versus 8.76 ± 19.72%, P = .04 for ADC, 33.78 ± 54.01% versus 7.91 ± 25.16%, P = .03 for D, 25.91 ± 36.28% versus 1.75 ± 46.42%, P = .01 for DK) while f declined (-32.62 ± 41.48% versus 6.51 ± 44.16%, P < .001) more in MTAT group.The MTAT induced different posttreatment changes on water molecule diffusion and microvasculature related functional MR parameters compared to RFA in patients with liver tumors.
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Affiliation(s)
- Guangyuan Zhang
- Department of Radiology, Shanghai Proton and Heavy Ion Center
- Department of Radiology
- Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, People's Republic of China
| | - Wentao Li
- Department of Interventional Radiology, Fudan University Shanghai Cancer Center
- Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, People's Republic of China
| | - Guangzhi Wang
- Department of Interventional Radiology, Fudan University Shanghai Cancer Center
| | - Xinhong He
- Department of Interventional Radiology, Fudan University Shanghai Cancer Center
| | - Lichao Xu
- Department of Interventional Radiology, Fudan University Shanghai Cancer Center
| | | | - Weijun Peng
- Department of Radiology
- Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, People's Republic of China
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Roberts TA, Hyare H, Agliardi G, Hipwell B, d'Esposito A, Ianus A, Breen-Norris JO, Ramasawmy R, Taylor V, Atkinson D, Punwani S, Lythgoe MF, Siow B, Brandner S, Rees J, Panagiotaki E, Alexander DC, Walker-Samuel S. Noninvasive diffusion magnetic resonance imaging of brain tumour cell size for the early detection of therapeutic response. Sci Rep 2020; 10:9223. [PMID: 32514049 PMCID: PMC7280197 DOI: 10.1038/s41598-020-65956-4] [Citation(s) in RCA: 25] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/21/2018] [Accepted: 05/07/2020] [Indexed: 01/09/2023] Open
Abstract
Cancer cells differ in size from those of their host tissue and are known to change in size during the processes of cell death. A noninvasive method for monitoring cell size would be highly advantageous as a potential biomarker of malignancy and early therapeutic response. This need is particularly acute in brain tumours where biopsy is a highly invasive procedure. Here, diffusion MRI data were acquired in a GL261 glioma mouse model before and during treatment with Temozolomide. The biophysical model VERDICT (Vascular Extracellular and Restricted Diffusion for Cytometry in Tumours) was applied to the MRI data to quantify multi-compartmental parameters connected to the underlying tissue microstructure, which could potentially be useful clinical biomarkers. These parameters were compared to ADC and kurtosis diffusion models, and, measures from histology and optical projection tomography. MRI data was also acquired in patients to assess the feasibility of applying VERDICT in a range of different glioma subtypes. In the GL261 gliomas, cellular changes were detected according to the VERDICT model in advance of gross tumour volume changes as well as ADC and kurtosis models. VERDICT parameters in glioblastoma patients were most consistent with the GL261 mouse model, whilst displaying additional regions of localised tissue heterogeneity. The present VERDICT model was less appropriate for modelling more diffuse astrocytomas and oligodendrogliomas, but could be tuned to improve the representation of these tumour types. Biophysical modelling of the diffusion MRI signal permits monitoring of brain tumours without invasive intervention. VERDICT responds to microstructural changes induced by chemotherapy, is feasible within clinical scan times and could provide useful biomarkers of treatment response.
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Affiliation(s)
- Thomas A Roberts
- Centre for Advanced Biomedical Imaging, University College London, London, UK
| | - Harpreet Hyare
- Centre for Medical Imaging, Division of Medicine, University College London, London, UK
- Department of Brain Repair and Rehabilitation, UCL Institute of Neurology, London, UK
| | - Giulia Agliardi
- Centre for Advanced Biomedical Imaging, University College London, London, UK
| | - Ben Hipwell
- Centre for Advanced Biomedical Imaging, University College London, London, UK
| | - Angela d'Esposito
- Centre for Advanced Biomedical Imaging, University College London, London, UK
| | - Andrada Ianus
- Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK
| | | | - Rajiv Ramasawmy
- Centre for Advanced Biomedical Imaging, University College London, London, UK
| | - Valerie Taylor
- Centre for Advanced Biomedical Imaging, University College London, London, UK
| | - David Atkinson
- Centre for Medical Imaging, Division of Medicine, University College London, London, UK
| | - Shonit Punwani
- Centre for Medical Imaging, Division of Medicine, University College London, London, UK
| | - Mark F Lythgoe
- Centre for Advanced Biomedical Imaging, University College London, London, UK
| | - Bernard Siow
- Centre for Advanced Biomedical Imaging, University College London, London, UK
| | | | - Jeremy Rees
- National Hospital for Neurology and Neurosurgery, London, UK
| | - Eleftheria Panagiotaki
- Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK
| | - Daniel C Alexander
- Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK
| | - Simon Walker-Samuel
- Centre for Advanced Biomedical Imaging, University College London, London, UK.
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Cheng ZY, Feng YZ, Liu XL, Ye YJ, Hu JJ, Cai XR. Diffusional kurtosis imaging of kidneys in patients with hyperuricemia: initial study. Acta Radiol 2020; 61:839-847. [PMID: 31610679 DOI: 10.1177/0284185119878362] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/13/2022]
Abstract
BACKGROUND At present, there remains a lack of a reliable indicator for monitoring renal function in patients with hyperuricemia. PURPOSE This study aimed to evaluate the feasibility of diffusion kurtosis imaging in the assessment of renal function in patients with hyperuricemia. MATERIAL AND METHODS A total of 75 male participants, including 25 with asymptomatic hyperuricemia, 25 with gouty arthritis, and 25 age-matched male healthy controls, were enrolled in this study. Diffusion kurtosis imaging data were acquired to derive axial (Ka), radial (Kr), and mean kurtosis (MK), fractional anisotropy, axial (Da), radial (Dr), and mean diffusivity (MD) for comparisons among the three groups. They were also correlated with estimated glomerular filtration rate (eGFR). RESULTS The MK values of the renal cortex and medulla and Kr value of the renal medulla in patients with asymptomatic hyperuricemia and gouty arthritis significantly increased compared with those in the controls (P < 0.05). Patients with gouty arthritis showed significant higher cortical and medullary Ka values compared with the other two groups (P < 0.05). The cortical Kr values of the asymptomatic hyperuricemia and gouty arthritis patients were significantly higher than that of the controls (P < 0.05). The medullary fractional anisotropy value showed a significant difference between the control and gouty arthritis groups (P < 0.05). No correlation was found between any diffusion kurtosis imaging parameters and eGFR value. CONCLUSION Diffusion kurtosis imaging is feasible in the assessment of the early changes of renal cortex and medulla in patients with hyperuricemia.
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Affiliation(s)
- Zhong-Yuan Cheng
- Medical Imaging Center, the First Affiliated Hospital, Jinan University, Guangzhou, Guangdong, PR China
- *Equal contributors
| | - You-Zhen Feng
- Medical Imaging Center, the First Affiliated Hospital, Jinan University, Guangzhou, Guangdong, PR China
- *Equal contributors
| | - Xiao-Ling Liu
- Medical Imaging Center, Guangdong Provincial Hospital of Traditional Chinese Medicine Zhuhai Branch, Guangdong, PR China
| | - Yao-Jiang Ye
- Medical Imaging Center, the First Affiliated Hospital, Jinan University, Guangzhou, Guangdong, PR China
| | - Jun-Jiao Hu
- Medical Imaging Center, the First Affiliated Hospital, Jinan University, Guangzhou, Guangdong, PR China
| | - Xiang-Ran Cai
- Medical Imaging Center, the First Affiliated Hospital, Jinan University, Guangzhou, Guangdong, PR China
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Granata V, Fusco R, Sansone M, Grassi R, Maio F, Palaia R, Tatangelo F, Botti G, Grimm R, Curley S, Avallone A, Izzo F, Petrillo A. Magnetic resonance imaging in the assessment of pancreatic cancer with quantitative parameter extraction by means of dynamic contrast-enhanced magnetic resonance imaging, diffusion kurtosis imaging and intravoxel incoherent motion diffusion-weighted imaging. Therap Adv Gastroenterol 2020; 13:1756284819885052. [PMID: 32499833 PMCID: PMC7243396 DOI: 10.1177/1756284819885052] [Citation(s) in RCA: 41] [Impact Index Per Article: 8.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/19/2019] [Accepted: 10/07/2019] [Indexed: 02/04/2023] Open
Abstract
BACKGROUND Despite great technical advances in imaging, such as multidetector computed tomography and magnetic resonance imaging (MRI), diagnosing pancreatic solid lesions correctly remains challenging, due to overlapping imaging features with benign lesions. We wanted to evaluate functional MRI to differentiate pancreatic tumors, peritumoral inflammatory tissue, and normal pancreatic parenchyma by means of dynamic contrast-enhanced MRI (DCE-MRI)-, diffusion kurtosis imaging (DKI)-, and intravoxel incoherent motion model (IVIM) diffusion-weighted imaging (DWI)-derived parameters. METHODS We retrospectively analyzed 24 patients, each with histopathological diagnosis of pancreatic tumor, and 24 patients without pancreatic lesions. Functional MRI was acquired using a 1.5 MR scanner. Peritumoral inflammatory tissue was assessed by drawing regions of interest on the tumor contours. DCE-MRI, IVIM and DKI parameters were extracted. Nonparametric tests and receiver operating characteristic (ROC) curves were calculated. RESULTS There were statistically significant differences in median values among the three groups observed by Kruskal-Wallis test for the DKI mean diffusivity (MD), IVIM perfusion fraction (fp) and IVIM tissue pure diffusivity (Dt). MD had the best results to discriminate normal pancreas plus peritumoral inflammatory tissue versus pancreatic tumor, to separate normal pancreatic parenchyma versus pancreatic tumor and to differentiate peritumoral inflammatory tissue versus pancreatic tumor, respectively, with an accuracy of 84%, 78%, 83% and area under ROC curve (AUC) of 0.85, 0.82, 0.89. The findings were statistically significant compared with those of other parameters (p value < 0.05 using McNemar's test). Instead, to discriminate normal pancreas versus peritumoral inflammatory tissue or pancreatic tumor and to differentiate normal pancreatic parenchyma versus peritumoral inflammatory tissue, there were no statistically significant differences between parameters' accuracy (p > 0.05 at McNemar's test). CONCLUSIONS Diffusion parameters, mainly MD by DKI, could be helpful for the differentiation of normal pancreatic parenchyma, perilesional inflammation, and pancreatic tumor.
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Affiliation(s)
- Vincenza Granata
- Radiology Unit, ‘Istituto Nazionale Tumori – IRCCS – Fondazione G. Pascale’, Naples, Italy
| | - Roberta Fusco
- Department of Radiology, Istituto Nazionale Tumori Fondazione G. Pascale, via Mariano Semmola, Naples 80131, Italy
| | - Mario Sansone
- Department of Electrical Engineering and Information Technologies (DIETI), University of Naples Federico II, Naples, Italy
| | - Roberto Grassi
- Radiology Unit, Università della Campania Luigi Vanvitelli, Naples, Italy
| | - Francesca Maio
- Radiology Unit, University of Naples Federico II, Naples, Italy
| | - Raffaele Palaia
- Hepatobiliary Surgical Oncology Unit, ‘Istituto Nazionale Tumori – IRCCS – Fondazione G. Pascale’, Naples, Italy
| | - Fabiana Tatangelo
- Diagnostic Pathology Unit, ‘Istituto Nazionale Tumori – IRCCS – Fondazione G. Pascale’, Naples, Italy
| | - Gerardo Botti
- Diagnostic Pathology Unit, ‘Istituto Nazionale Tumori – IRCCS – Fondazione G. Pascale’, Naples, Italy
| | - Robert Grimm
- Siemens Healthcare GmbH, Erlangen, Bayern, Germany
| | - Steven Curley
- Department of Surgery, Baylor College of Medicine, Houston, TX, USA
| | - Antonio Avallone
- Abdominal Oncology Unit, ‘Istituto Nazionale Tumori – IRCCS – Fondazione G. Pascale’, Naples, Italy
| | - Francesco Izzo
- Hepatobiliary Surgical Oncology Unit, ‘Istituto Nazionale Tumori – IRCCS – Fondazione G. Pascale’, Naples, Italy
| | - Antonella Petrillo
- Radiology Unit, ‘Istituto Nazionale Tumori – IRCCS – Fondazione G. Pascale’, Naples, Italy
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Fu J, Tang L, Li ZY, Li XT, Zhu HF, Sun YS, Ji JF. Diffusion kurtosis imaging in the prediction of poor responses of locally advanced gastric cancer to neoadjuvant chemotherapy. Eur J Radiol 2020; 128:108974. [PMID: 32416553 DOI: 10.1016/j.ejrad.2020.108974] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/28/2019] [Revised: 02/15/2020] [Accepted: 03/19/2020] [Indexed: 12/11/2022]
Abstract
PURPOSE To assess the efficacy of diffusion kurtosis imaging (DKI) in the prediction of the treatment response to neoadjuvant chemotherapy in patients with locally advanced gastric cancer (LAGC). METHODS A total of 31 LAGC patients were enrolled in this prospective study. All patients underwent diffusion-weighted MRI examination (with b = 01, 2001, 5001, 8002, 10004, 15004, 20006 s/mm2, the subscript denotes the number of signal averages) before and after chemotherapy. DKI and mono-exponential (b = 0, 800 s/mm2) models were built. Apparent diffusion coefficient (ADC), mean diffusivity (MD) and mean kurtosis (MK) of the LAGC tumors were measured. The absolute change values (ΔX) and percentage change values (%ΔX) of the above parameters post neoadjuvant chemotherapy (NACT) were calculated. The response was evaluated according to the pathological tumor regression grade scores (effective response group: TRG 0-2, poor response group: TRG 3). Mann-Whitney U test and receiver operating characteristic (ROC) curves were applicated for statistical analysis. RESULTS There were 17 patients in the effective response group (ERG), and 14 patients in the poor response group (PRG). The MKpre and MKpost values in PRG were significantly higher than those in ERG [(0.671 ± 0.026) and (0.641 ± 0.019) vs. (0.584 ± 0.023) and (0.519 ± 0.018), p < 0.001]. ADCpost and MDpost in PRG were significantly lower than those in ERG (p = 0.005, p =0.001). Significant differences were also observed for % ΔMK, ΔMD and ΔMK between the two groups (p < 0.05). The area under the curve (AUC) for the prediction of PRG was highest for MKpost (AUC = 0.958, cutoff value = 0.614). The MKpre and MKpost had the highest sensitivity (91.70 %) and specificity (93.80 %) in the prediction of PRG, respectively. CONCLUSION Both DKI and ADC values show potential for the prediction of the PRG in LAGC patients. The DKI parameters, especially MKpost displayed the best performance.
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Affiliation(s)
- Jia Fu
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Radiology Department, Peking University Cancer Hospital & Institute, No. 52 Fu-Cheng Road, Hai-Dian District, Beijing 100142, China; Department of Radiology, Civil Aviation General Hospital, No. 1 Gaojingjia, Chaoyang Road, Chaoyang District, Beijing 100123, China.
| | - Lei Tang
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Radiology Department, Peking University Cancer Hospital & Institute, No. 52 Fu-Cheng Road, Hai-Dian District, Beijing 100142, China.
| | - Zi-Yu Li
- Department of Gastrointestinal Cancer Center Surgery, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Peking University Cancer Hospital & Institute, No. 52 Fu-Cheng Road, Hai-Dian District, Beijing 100142, China.
| | - Xiao-Ting Li
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Radiology Department, Peking University Cancer Hospital & Institute, No. 52 Fu-Cheng Road, Hai-Dian District, Beijing 100142, China.
| | - Hai-Feng Zhu
- Department of Radiology, Civil Aviation General Hospital, No. 1 Gaojingjia, Chaoyang Road, Chaoyang District, Beijing 100123, China.
| | - Ying-Shi Sun
- Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Radiology Department, Peking University Cancer Hospital & Institute, No. 52 Fu-Cheng Road, Hai-Dian District, Beijing 100142, China.
| | - Jia-Fu Ji
- Department of Gastrointestinal Cancer Center Surgery, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Peking University Cancer Hospital & Institute, No. 52 Fu-Cheng Road, Hai-Dian District, Beijing 100142, China.
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Diffusion kurtosis imaging in liver: a preliminary reproducibility study in healthy volunteers. MAGNETIC RESONANCE MATERIALS IN PHYSICS BIOLOGY AND MEDICINE 2020; 33:877-883. [PMID: 32377906 DOI: 10.1007/s10334-020-00846-4] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 01/06/2020] [Revised: 04/07/2020] [Accepted: 04/16/2020] [Indexed: 12/29/2022]
Abstract
OBJECTIVES To systematically test the reproducibility of DKI technique in normal liver and report a complete set of DKI measurement data. MATERIALS AND METHODS Thirty-two healthy volunteers were examined with liver DKI twice on the GE 3.0 T MRI scanner and reviewed by three professional experts. DKI-derived parameters fractional anisotropy of kurtosis (FAk), mean diffusivity (Md), axial diffusivity (Da), radial diffusivity (Dr), mean kurtosis (Mk), axial kurtosis (Ka), and radial kurtosis (Kr) in eight segments divided by Couinaud octagonal method were collected. Inter-class correlation coefficient (ICC) was used to assess the agreement between three experts. For each expert, the reproducibility of twice scans was evaluated by Bland-Altman method. Multivariate analysis of variance was to explore the regional distribution characteristics of DKI-derived parameters, and showed with box-plot graph. RESULTS Using ICC analysis, except for FAk (ICC 0.312, 0.307), other DKI metric values showed high reproducibility (0.716 < ICC < 0.907) between three experts for each of two DKI measurements. With Bland-Altman method, liver segment 5 (S5) showed the best reproducibility between two DKI measurement, and the reproducibility of segment 4 (S4) was the worst. The reproducibility of the right lobe was significantly higher than the left lobe. The values of diffusion metrics (Md, Da, and Dr) and kurtosis metrics (Mk, Ka, and Kr) existed significantly difference between the right and left hepatic lobes. CONCLUSION DKI has shown excellent reproducibility in liver imaging. The range of values for multiple DKI parameters, derived from the normal liver, was reported, and may provide data reference for further clinical DKI applications. Additionally, DKI technique is a non-invasive method to reflect the perfusion or structural differences between the left and right hepatic lobes from the molecular level.
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Wu J, Yan F, Chai W, Fu C, Yan X, Zhan Y, Sun K. Breast cancer recurrence risk prediction using whole-lesion histogram analysis with diffusion kurtosis imaging. Clin Radiol 2020; 75:239.e1-239.e8. [DOI: 10.1016/j.crad.2019.10.015] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/12/2019] [Accepted: 10/21/2019] [Indexed: 12/16/2022]
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Yuan ZG, Wang ZY, Xia MY, Li FZ, Li Y, Shen Z, Wang XZ. Diffusion Kurtosis Imaging for Assessing the Therapeutic Response of Transcatheter Arterial Chemoembolization in Hepatocellular Carcinoma. J Cancer 2020; 11:2339-2347. [PMID: 32127960 PMCID: PMC7052943 DOI: 10.7150/jca.32491] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Key Words] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/22/2018] [Accepted: 01/06/2020] [Indexed: 12/12/2022] Open
Abstract
Objective: This study aimed to evaluate the therapeutic response of hepatocellular carcinoma (HCC) after transcatheter arterial chemoembolization (TACE) with diffusion kurtosis imaging (DKI). Methods: Forty-three patients with fifty-nine hepatic cancer nodules were recruited for this study. All patients were treated by TACE. Magnetic resonance imaging (MRI) and DKI (b=0, 800, 1,500, 2,000mm2/s) were performed before and one month after initiating TACE. Patients were classified as either progressing groups or non-progressing groups. Mean kurtosis (MK), mean diffusion (MD), and apparent diffusion coefficient (ADC) values of the tumor tissue were analyzed. Results: Twenty-three HCCs were classified as progressing groups, and thirty-six HCCs were non-progressing groups. After TACE, the values of MD and ADC in non-progressing groups (1.92±0.36×10-3mm2/s, 1.36±0.23×10-3mm2/s) were greater than progressing groups (1.44±0.32× 10-3mm2/s, 1.10±0.23×10-3mm2/s), however, the MK values in non-progressing groups (0.47±0.12) were lower than progressing groups (0.72±0.14). The MK values of tumor among non-progressing patients decreased one month after TACE (0.47±0.12) relative to the preoperative values (0.71±0.12) (P<0.05). In the non-progressing groups, the MD and ADC values of tumor after TACE (1.92±0.36×10-3mm2/s, 1.36±0.23×10-3mm2/s) became higher than their preoperative values (1.44±0.35×10-3mm2/s, 1.09±0.22×10-3mm2/s) (P<0.05). In the progressing groups, the MK, MD, and ADC values of tumor after TACE remained similar before TACE (P>0.05). The sensitivity, specificity, and AUC of the ROC curve for the assessment of HCC progress after TACE by MK (85.2%, 97.5%, and 0.95, respectively) were greater than by ADC (78.6%, 66.5%, and 0.75, respectively) and MD (76.2%, 64.3%, and 0.71, respectively). Conclusions: DKI for assessing the therapeutic response of TACE in HCC shows great promise. MK is more advantageous in the assessment of HCC progress after TACE.
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Affiliation(s)
- Zhen-Guo Yuan
- Shandong Medical Imaging Research Institute Affiliated to Shandong University, Jinan 250021 P. R. China
| | - Zong-Ying Wang
- Medical Imaging Center of the Affiliated Hospital, Weifang Medical University, Weifang 261053 P. R.China
| | - Meng-Ying Xia
- Shandong Medical Imaging Research Institute Affiliated to Shandong University, Jinan 250021 P. R. China
| | - Feng-Zhi Li
- Medical Imaging Center of the Affiliated Hospital, Weifang Medical University, Weifang 261053 P. R.China
| | - Yao Li
- Shandong Medical Imaging Research Institute Affiliated to Shandong University, Jinan 250021 P. R. China
| | - Zhen Shen
- Medical Imaging Center of the Affiliated Hospital, Weifang Medical University, Weifang 261053 P. R.China
| | - Xi-Zhen Wang
- Medical Imaging Center of the Affiliated Hospital, Weifang Medical University, Weifang 261053 P. R.China
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Baboli M, Zhang J, Kim SG. Advances in Diffusion and Perfusion MRI for Quantitative Cancer Imaging. CURRENT PATHOBIOLOGY REPORTS 2019; 7:129-141. [PMID: 33344067 PMCID: PMC7747414 DOI: 10.1007/s40139-019-00204-7] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 12/14/2022]
Abstract
PURPOSE OF REVIEW This article is to review recent technical developments and their clinical applications in cancer imaging quantitative measurement of cellular and vascular properties of the tumors. RECENT FINDINGS Rapid development of fast Magnetic Resonance Imaging (MRI) technologies over last decade brought new opportunities in quantitative MRI methods to measure both cellular and vascular properties of tumors simultaneously. SUMMARY Diffusion MRI (dMRI) and dynamic contrast enhanced (DCE)-MRI have become widely used to assess the tissue structural and vascular properties, respectively. However, the ultimate potential of these advanced imaging modalities has not been fully exploited. The dependency of dMRI on the diffusion weighting gradient strength and diffusion time can be utilized to measure tumor perfusion, cellular structure, and cellular membrane permeability. Similarly, DCE-MRI can be used to measure vascular and cellular membrane permeability along with cellular compartment volume fractions. To facilitate the understanding of these potentially important methods for quantitative cancer imaging, we discuss the basic concepts and recent developments, as well as future directions for further development.
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Affiliation(s)
- Mehran Baboli
- Center for Biomedical Imaging, Department of Radiology, New York University School of Medicine, New York, NY 10016, USA
| | - Jin Zhang
- Center for Biomedical Imaging, Department of Radiology, New York University School of Medicine, New York, NY 10016, USA
| | - Sungheon Gene Kim
- Center for Biomedical Imaging, Department of Radiology, New York University School of Medicine, New York, NY 10016, USA
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Yoon JH, Lee JM, Lee KB, Kim D, Kabasawa H, Han JK. Comparison of monoexponential, intravoxel incoherent motion diffusion-weighted imaging and diffusion kurtosis imaging for assessment of hepatic fibrosis. Acta Radiol 2019; 60:1593-1601. [PMID: 30935212 DOI: 10.1177/0284185119840219] [Citation(s) in RCA: 11] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/05/2023]
Affiliation(s)
- Jeong Hee Yoon
- Radiology, Seoul National University Hospital, Seoul, Republic of Korea
- College of Medicine, Seoul, Republic of Korea
| | - Jeong Min Lee
- Radiology, Seoul National University Hospital, Seoul, Republic of Korea
- College of Medicine, Seoul, Republic of Korea
- Institute of Radiation Medicine, Seoul National University Medical Research Center, Seoul, Republic of Korea
| | - Kyung Bun Lee
- Department of Pathology, Seoul National University Hospital, Seoul, Republic of Korea
| | - Dongeun Kim
- GE Healthcare Korea, Seoul, Republic of Korea
| | | | - Joon Koo Han
- Radiology, Seoul National University Hospital, Seoul, Republic of Korea
- College of Medicine, Seoul, Republic of Korea
- Institute of Radiation Medicine, Seoul National University Medical Research Center, Seoul, Republic of Korea
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Optimal b-values for diffusion kurtosis imaging of the liver and pancreas in MR examinations. Phys Med 2019; 66:119-123. [DOI: 10.1016/j.ejmp.2019.09.238] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/05/2019] [Revised: 09/19/2019] [Accepted: 09/22/2019] [Indexed: 12/13/2022] Open
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Hu S, Sun C, Wang B, Zhou K, Pan L, Shangguan J, Yang J, Yaghmai V, Figini M, Zhang Z. Diffusion-Weighted MR Imaging to Evaluate Immediate Response to Irreversible Electroporation in a Rabbit VX2 Liver Tumor Model. J Vasc Interv Radiol 2019; 30:1863-1869. [PMID: 31542271 DOI: 10.1016/j.jvir.2019.05.030] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/23/2019] [Revised: 05/26/2019] [Accepted: 05/31/2019] [Indexed: 02/09/2023] Open
Abstract
PURPOSE To evaluate the feasibility of diffusion-weighted imaging (DWI) in magnetic resonance imaging for quantitative measurement of responses following irreversible electroporation (IRE) in a rabbit liver tumor model. MATERIALS AND METHODS Twelve rabbits underwent ultrasound-guided VX2 tumor implantation in the left medial and left lateral liver lobes. The tumors in the left medial lobe were treated with IRE, whereas those in the left lateral lobe served as internal controls. DWI was performed before and immediately after IRE. Tumors were then harvested for histopathologic staining. The apparent diffusion coefficient (ADC) and change in ADC (ΔADC) were calculated based on DWI. Tumor apoptosis index (AI) was assessed by terminal deoxynucleotidyl transferase dUTP nick-end labeling. These measurements from DWI and histopathology were compared between untreated and treated tumors. RESULTS The ADC values, ΔADC, and AI showed statistically significant differences between treated and untreated tumors (P < .05 for all). ADC values were higher in treated tumors than in untreated tumors (1.08 × 10-3 mm2/s ± 0.15 vs 0.88 × 10-3 mm2/s ± 0.19; P = .042). CONCLUSIONS DWI can be used to quantitatively evaluate treatment response in liver tumors immediately after IRE.
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Affiliation(s)
- Su Hu
- Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, China; Department of Radiology, Feinberg School of Medicine, Northwestern University, 737 N. Michigan Ave., 16th Floor, Chicago, IL 60611
| | - Chong Sun
- Department of Orthopedics, The Affiliated Hospital of Qingdao University, Qingdao, China
| | - Bin Wang
- Department of Radiology, Feinberg School of Medicine, Northwestern University, 737 N. Michigan Ave., 16th Floor, Chicago, IL 60611; Department of General Surgery, Nanfang Hospital, Southern Medical University, Guangdong Provincial Engineering Technology Research Center of Minimally Invasive Surgery, Guangzhou, China
| | - Kang Zhou
- Department of Radiology, Feinberg School of Medicine, Northwestern University, 737 N. Michigan Ave., 16th Floor, Chicago, IL 60611; Department of Radiology, Peking Union Medical College Hospital, Peking Union Medical College, Chinese Academy of Medical Sciences, Beijing, China
| | - Liang Pan
- Department of Radiology, Feinberg School of Medicine, Northwestern University, 737 N. Michigan Ave., 16th Floor, Chicago, IL 60611; Department of Radiology, The Third Affiliated Hospital of Soochow University, Changzhou, China
| | - Junjie Shangguan
- Department of Radiology, Feinberg School of Medicine, Northwestern University, 737 N. Michigan Ave., 16th Floor, Chicago, IL 60611
| | - Jia Yang
- Department of Radiology, Feinberg School of Medicine, Northwestern University, 737 N. Michigan Ave., 16th Floor, Chicago, IL 60611
| | - Vahid Yaghmai
- Department of Radiology, Feinberg School of Medicine, Northwestern University, 737 N. Michigan Ave., 16th Floor, Chicago, IL 60611; Robert H. Lurie Comprehensive Cancer Center, Northwestern University, Chicago, Illinois
| | - Matteo Figini
- Department of Radiology, Feinberg School of Medicine, Northwestern University, 737 N. Michigan Ave., 16th Floor, Chicago, IL 60611
| | - Zhuoli Zhang
- Department of Radiology, Feinberg School of Medicine, Northwestern University, 737 N. Michigan Ave., 16th Floor, Chicago, IL 60611; Robert H. Lurie Comprehensive Cancer Center, Northwestern University, Chicago, Illinois.
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Guo R, Yang SH, Lu F, Han ZH, Yan X, Fu CX, Zhao ML, Lin J. Evaluation of intratumoral heterogeneity by using diffusion kurtosis imaging and stretched exponential diffusion-weighted imaging in an orthotopic hepatocellular carcinoma xenograft model. Quant Imaging Med Surg 2019; 9:1566-1578. [PMID: 31667142 DOI: 10.21037/qims.2019.08.18] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/17/2022]
Abstract
Background To investigate the value of diffusion kurtosis imaging (DKI) and diffusion-weighted imaging (DWI) with a stretched exponential model (SEM) in the evaluation of tumor heterogeneity in an orthotopic hepatocellular carcinoma (HCC) xenograft model. Methods Thirty orthotopic HCC xenograft nude mice models were established and randomly divided into two groups, the sorafenib induction group (n=15) and control group (n=15). Every mouse in each group underwent MRI with DKI and SEM on a 1.5T MR scanner at 7, 14, and 21 days after sorafenib intervention. DKI and SEM parameters including mean kurtosis (MK), mean diffusivity (MD), α, and distributed diffusion coefficient (DDC) were measured, calculated, and compared between the two groups and among different time points. Sequential correlations between histopathological results including necrotic fraction (NF), micro-vessel density (MVD), Ki-67 index, standard deviation (SD), and kurtosis from hematoxylin-eosin staining, and DKI and SEM parameters were analyzed. Results MK, MD, and DDC of HCC in the sorafenib induction group were significantly higher than those in the control group at each time point (P<0.05), while α was significantly lower (P<0.05). Significantly positive correlations were found between MK and NF (r=0.693, P=0.010), SD (r =0.785, P=0.003), kurtosis (r=0.779, P=0.003), between MD and NF (r=0.794, P=0.003), SD (r=0.629, P=0.020), kurtosis (r=0.645, P=0.018), and between DDC and NF (r=0.800, P=0.003), SD (r=0.636, P=0.020), kurtosis (r=0.664, P=0.016), and significantly negative correlations were observed between α and NF (r=-0.704, P=0.009), SD (r=-0.754, P=0.003), and kurtosis (r=-0.792, P=0.003) in the sorafenib induction group. Conclusions DKI and SEM parameters may be potentially useful for evaluating intratumoral heterogeneity in HCC.
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Affiliation(s)
- Ran Guo
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai 200032, China.,Shanghai Institute of Medical Imaging, Shanghai 200032, China
| | - Shuo-Hui Yang
- Department of Radiology, Shuguang Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai 200021, China
| | - Fang Lu
- Department of Radiology, Shuguang Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai 200021, China
| | - Zhi-Hong Han
- Department of Pathology, Shuguang Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai 200021, China
| | - Xu Yan
- MR Scientific Marketing, Siemens Healthcare, Shanghai 201318, China
| | - Cai-Xia Fu
- Siemens Shenzhen Magnetic Resonance Ltd., Shenzhen 518057, China
| | - Meng-Long Zhao
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai 200032, China.,Shanghai Institute of Medical Imaging, Shanghai 200032, China
| | - Jiang Lin
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai 200032, China.,Shanghai Institute of Medical Imaging, Shanghai 200032, China
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Optimal b-values for diffusion kurtosis imaging in invasive ductal carcinoma versus ductal carcinoma in situ breast lesions. AUSTRALASIAN PHYSICAL & ENGINEERING SCIENCES IN MEDICINE 2019; 42:871-885. [DOI: 10.1007/s13246-019-00773-2] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Received: 11/15/2018] [Accepted: 06/27/2019] [Indexed: 12/13/2022]
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Diffusion Kurtosis MR Imaging versus Conventional Diffusion-Weighted Imaging for Distinguishing Hepatocellular Carcinoma from Benign Hepatic Nodules. CONTRAST MEDIA & MOLECULAR IMAGING 2019; 2019:2030147. [PMID: 31396023 PMCID: PMC6664697 DOI: 10.1155/2019/2030147] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 01/25/2019] [Revised: 06/09/2019] [Accepted: 07/03/2019] [Indexed: 12/17/2022]
Abstract
Objectives To assess the efficacy of diffusion kurtosis imaging (DKI) and compare DKI-derived parameters with conventional diffusion-weighted imaging (DWI) for distinguishing hepatocellular carcinoma (HCC) from benign hepatic nodules including focal nodular hyperplasia (FNH), hemangioma, and hepatocellular adenoma (HCA). Materials and Methods 151 patients with 182 hepatic nodules (114 HCCs and 68 benign nodules including 33 FNHs, 29 hemangiomas, and 6 HCAs) were analyzed. Preoperative MRI examinations including DKI (b values: 0, 200, 500, 800, 1500, and 2000 sec/mm2) were performed, and kurtosis (K), diffusivity (D), and apparent diffusion coefficient (ADC) were calculated. The efficacy of DKI-derived parameters K, D, and ADC for distinguishing HCC from these benign nodules was analyzed. Results ROC (receiver operating characteristic curve) analysis showed the optimal cutoff values of ADC, D, and K for identification of these benign nodules, and HCCs were 1.295 (area under the curve (AUC): 0.826; sensitivity 80.6%; specificity 70.8%), 1.787 (AUC: 0.770; sensitivity 83.6%; specificity 59.6%), and 1.002 (AUC: 0.761; sensitivity 65.5%; specificity 79.0%), respectively. Statistically significant differences were found in ADC, D, and K values between groups of HCC-FNH and HCC-hemangioma (P < 0.05). There were significant differences in K and ADC values between groups of FNH-hemangioma and HCA-hemangioma (P < 0.05), respectively. Using logistic regression analysis, a regression equation was obtained: Logit(P)=−1.982X1+1.385X3+1.948(X1: ADC; X3: K), and odds ratios (OR) were 0.138 (95% confidence interval (CI): 0.052, 0.367), and 8.996 (95% CI: 0.970, 16.460), respectively. Conclusion Both ADC value and DKI-derived parameters K and D values have demonstrated a higher preoperative efficacy in distinguishing HCC from FNH, hemangioma, and HCA. No evidence was shown to suggest D or K value was superior to the ADC value.
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Comment on "State of the art in magnetic resonance imaging of hepatocellular carcinoma": the role of DWI. Radiol Oncol 2019; 53:369-370. [PMID: 31318697 PMCID: PMC6765167 DOI: 10.2478/raon-2019-0031] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/06/2019] [Indexed: 12/13/2022] Open
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Yuan ZG, Wang ZY, Xia MY, Li FZ, Li Y, Shen Z, Wang XZ. Comparison of diffusion kurtosis imaging versus diffusion weighted imaging in predicting the recurrence of early stage single nodules of hepatocellular carcinoma treated by radiofrequency ablation. Cancer Imaging 2019; 19:30. [PMID: 31142356 PMCID: PMC6542145 DOI: 10.1186/s40644-019-0213-9] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/01/2019] [Accepted: 05/13/2019] [Indexed: 12/14/2022] Open
Abstract
Objective This study aimed to compare the diffusion kurtosis imaging (DKI) versus diffusion weighted imaging (DWI) in predicting the recurrence of early stage single nodules of hepatocellular carcinoma (HCC) treated by radiofrequency ablation (RFA). Materials and methods A retrospective analysis of 107 patients with early stage single nodules of HCC was performed, all patients treated by RFA. Recurrence rate of HCC was recorded after a median follow-up of 36 months. During follow-up, the data of magnetic resonance imaging (MRI), DWI and DKI were obtained in multiple time points. The predictive values of DWI and DKI were analyzed using ROC curves. Results The overall recurrence rate was 66.3% (71/107). The sensitivity, specificity, and AUC for ADC, MD and MK after RFA (78.6, 73.3% and 0.842; 85.7, 83.3% and 0.839; 85.7, 96.7% and 0.956) were higher than before RFA (44.3, 53.3% and 0.560; 51.2, 56.7% and 0.543; 43.6, 67.3% and 0.489). The sensitivity, specificity, and AUC for MK after RFA were 85.7, 96.7%, and 0.956, respectively, which were significantly greater than those of ADC (78.6, 73.3% and 0.842; P < 0.05) and MD (85.7, 83.3% and 0.839). Conclusions The prediction efficacy of DKI for the recurrence of early stage single nodules of HCC was better than that of DWI. And, MK was the most sensitive predictor among the DKI.
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Affiliation(s)
- Zhen-Guo Yuan
- Shandong Medical Imaging Research Institute Affiliated to Shandong University, Jinan, 250021, People's Republic of China
| | - Zong-Ying Wang
- Medical Imaging Center of the Affiliated Hospital, Weifang Medical University, Weifang, 261053, People's Republic of China
| | - Meng-Ying Xia
- Shandong Medical Imaging Research Institute Affiliated to Shandong University, Jinan, 250021, People's Republic of China
| | - Feng-Zhi Li
- Medical Imaging Center of the Affiliated Hospital, Weifang Medical University, Weifang, 261053, People's Republic of China
| | - Yao Li
- Shandong Medical Imaging Research Institute Affiliated to Shandong University, Jinan, 250021, People's Republic of China
| | - Zhen Shen
- Medical Imaging Center of the Affiliated Hospital, Weifang Medical University, Weifang, 261053, People's Republic of China
| | - Xi-Zhen Wang
- Medical Imaging Center of the Affiliated Hospital, Weifang Medical University, Weifang, 261053, People's Republic of China.
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Cao L, Chen J, Duan T, Wang M, Jiang H, Wei Y, Xia C, Zhou X, Yan X, Song B. Diffusion kurtosis imaging (DKI) of hepatocellular carcinoma: correlation with microvascular invasion and histologic grade. Quant Imaging Med Surg 2019; 9:590-602. [PMID: 31143650 PMCID: PMC6511714 DOI: 10.21037/qims.2019.02.14] [Citation(s) in RCA: 48] [Impact Index Per Article: 8.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/05/2023]
Abstract
BACKGROUND The aim of this study was to prospectively evaluate the diagnostic efficacy of diffusion kurtosis imaging (DKI) in predicting microvascular invasion (MVI) and histologic grade of hepatocellular carcinoma (HCC) with comparison to the conventional diffusion-weighted imaging (DWI). METHODS This prospective study was approved by the Institutional Review Board, and written informed consent was obtained from all patients. From September 2015 to January 2017, 74 consecutive HCC patients were enrolled in this study. Preoperative magnetic resonance imaging including DKI protocol was performed, and patients were followed up for at least one year after surgery. Diffusion parameters including the mean corrected apparent diffusion coefficient (MD), mean apparent kurtosis coefficient (MK), and apparent diffusion coefficient (ADC) were calculated. Differences of diffusion parameters among different histopathological groups were compared. For parameters that were significantly different between pathological groups, receiver operating characteristics (ROC) curve analyses were performed to evaluate the diagnostic efficiency for identifying MVI and predicting high-grade HCC. Univariate and multivariate logistic regression analyses were used to evaluate the relative value of clinical and laboratory variables and diffusion parameters as risk factors for early recurrence (≤1 year). RESULTS Among all the studied diffusion parameters, only MK differed significantly between the MVI-positive and MVI-negative group (0.91±0.10 vs. 0.82±0.09, P<0.001), and showed moderate diagnostic efficacy (AUC =0.77) for identifying MVI. High-grade HCCs showed significantly higher MK values (0.93±0.10 vs. 0.82±0.09, P<0.001), along with MD (1.34±0.18 vs. 1.54±0.22, P<0.001) and ADC values (1.17±0.15 vs. 1.30±0.16, P=0.001) than low-grade HCCs. For differentiating high-grade from low-grade HCCs, MK demonstrated a higher area under the ROC curve (AUC) and significantly higher specificity than MD and ADC (AUC =0.81 vs. 0.76 and 0.74; specificity =82.2% vs. 60.0% and 60.0%, P=0.02). In addition, higher MK (OR =5.700, P=0.002) and Barcelona Clinic Liver Cancer (BCLC) stage C (OR =6.329, P=0.005) were independent risk factors for early HCC recurrence. CONCLUSIONS DKI-derived MK values outperformed conventional ADC values for predicting MVI and histologic grade of HCC, and are associated with increased risk of early tumor recurrence.
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Affiliation(s)
- Likun Cao
- Department of Radiology, West China Hospital of Sichuan University, Chengdu 610041, China
| | - Jie Chen
- Department of Radiology, West China Hospital of Sichuan University, Chengdu 610041, China
| | - Ting Duan
- Department of Radiology, West China Hospital of Sichuan University, Chengdu 610041, China
| | - Min Wang
- Department of Radiology, Inner Mongolia People’s Hospital, Hohhot 010017, China
| | - Hanyu Jiang
- Department of Radiology, West China Hospital of Sichuan University, Chengdu 610041, China
| | - Yi Wei
- Department of Radiology, West China Hospital of Sichuan University, Chengdu 610041, China
| | - Chunchao Xia
- Department of Radiology, West China Hospital of Sichuan University, Chengdu 610041, China
| | | | - Xu Yan
- Siemens Healthcare Ltd., Shanghai 201318, China
| | - Bin Song
- Department of Radiology, West China Hospital of Sichuan University, Chengdu 610041, China
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Granata V, Fusco R, Setola SV, Palaia R, Albino V, Piccirillo M, Grimm R, Petrillo A, Izzo F. Diffusion kurtosis imaging and conventional diffusion weighted imaging to assess electrochemotherapy response in locally advanced pancreatic cancer. Radiol Oncol 2019; 53:15-24. [PMID: 30681974 PMCID: PMC6411027 DOI: 10.2478/raon-2019-0004] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.2] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/24/2018] [Accepted: 11/18/2018] [Indexed: 02/06/2023] Open
Abstract
Background The aim of the study was to evaluate diagnostic performance of functional parameters derived by conventional mono-exponential approach of diffusion weighted imaging (DWI) and by diffusion kurtosis imaging (DKI) in the assessment of pancreatic tumours treated with electrochemotherapy (ECT). Patients and methods Twenty-one consecutive patients with locally advanced pancreatic adenocarcinoma subjected to ECT were enrolled in a clinical approved trial. Among twenty-one enrolled patients, 13/21 (61.9%) patients were subjected to MRI before and after ECT. DWI was performed with a 1.5 T scanner; a free breathing axial single shot echo planar DWI pulse sequence parameters were acquired using seven b value = 0, 50, 100, 150, 400, 800, 1000 s/mm2. Apparent diffusion coefficient by conventional mono-exponential approach and mean of diffusion coefficient (MD) and mean of diffusional kurtosis (MK) by DKI approach were derived from DWI. Receiver operating characteristic (ROC) analysis was performed and sensitivity, specificity, positive and negative predictive value were calculated. Results Among investigated diffusion parameters, only the MD derived by DKI showed a significant variation of values between pre and post treatment (p = 0.02 at Wilcoxon test) and a significant statistically difference for percentage change between responders and not responders (p = 0.01 at Kruskal Wallis test). MD had a good diagnostic performance with a sensitivity of 80%, a specificity of 100% and area under ROC of 0.933. Conclusions MD derived by DKI allows identifying responders and not responders patients subject to ECT treatment. MD had higher diagnostic performance to assess ECT response compared to conventional DWI derived parameters.
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Affiliation(s)
- Vincenza Granata
- Division of Radiology, Instituto Nazionale Tumori – IRCCS – Fondazione G. Pascale, Napoli, Italia
- Vincenza Granata, Division of Radiology, Instituto Nazionale Tumori – IRCCS – Fondazione G. Pascale, Napoli, Italia. Phone: +39 081 5903 714; Fax:+39 0815903825;
| | | | - Sergio Venanzio Setola
- Division of Radiology, Instituto Nazionale Tumori – IRCCS – Fondazione G. Pascale, Napoli, Italia
| | - Raffaele Palaia
- Division of Hepatobiliary Surgical Oncology, Unit, Instituto Nazionale Tumori, IRCCS, Fondazione G. Pascale, Napoli, Italia
| | - Vittorio Albino
- Division of Hepatobiliary Surgical Oncology, Unit, Instituto Nazionale Tumori, IRCCS, Fondazione G. Pascale, Napoli, Italia
| | - Mauro Piccirillo
- Division of Hepatobiliary Surgical Oncology, Unit, Instituto Nazionale Tumori, IRCCS, Fondazione G. Pascale, Napoli, Italia
| | | | - Antonella Petrillo
- Division of Radiology, Instituto Nazionale Tumori – IRCCS – Fondazione G. Pascale, Napoli, Italia
| | - Francesco Izzo
- Division of Hepatobiliary Surgical Oncology, Unit, Instituto Nazionale Tumori, IRCCS, Fondazione G. Pascale, Napoli, Italia
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Yuan SJ, Qiao TK, Qiang JW. Diffusion-weighted imaging and diffusion kurtosis imaging for early evaluation of the response to docetaxel in rat epithelial ovarian cancer. J Transl Med 2018; 16:340. [PMID: 30518386 PMCID: PMC6282389 DOI: 10.1186/s12967-018-1714-1] [Citation(s) in RCA: 4] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/18/2018] [Accepted: 11/30/2018] [Indexed: 12/23/2022] Open
Abstract
Background To investigate diffusion-weighted magnetic imaging (DWI) and diffusion kurtosis magnetic imaging (DKI) for the early detection of the response to docetaxel (DTX) chemotherapy in rat epithelial ovarian cancer (EOC). Methods 7,12-Dimethylbenz[A]anthracene was applied to induce orthotopic EOC in Sprague–Dawley rats. Rats with EOC were treated with DTX on day 0 (treatment group) or were left untreated (control group). DWI and DKI were performed on days 0, 3, 7, 14 and 21 after treatment. On day 21, the tumors were categorized into the sensitive and insensitive groups according to the size change. The cutoff values of the DWI and DKI parameters for the early response were determined. The experiment was repeated, and the treatment group was divided into the sensitive and insensitive groups according to the initially obtained cutoff values. The DWI and DKI parameters were correlated with tumor size, proliferation, apoptosis and tumor necrosis. Results In the sensitive vs. insensitive or control group, significant differences were found in the Δ% of the DWI and DKI parameters (ADC, D and K) from day 3 and in tumor size from day 14. Early on day 7, the Δ% of K had an AUC of 1 and sensitivity and specificity values of 100% and 100%, respectively, to detect the response to DTX using a cutoff value of 19.03% reduction in K. From day 7, significant differences were found in the Δ% of Ki-67 and CA125 in the sensitive vs. control group and from day 14 in the sensitive vs. insensitive group. From day 14, there were significant differences in the Δ% of Bcl-2, apoptosis and tumor necrosis in the sensitive vs. control or insensitive group. The Δ% values of ADC and D were negatively correlated with the Δ% values of tumor size, Ki-67, CA125 and Bcl-2 and were positively correlated with the Δ% values of apoptosis and tumor necrosis. The Δ% of K was positively correlated with the Δ% values of tumor size, Ki-67, CA125 and Bcl-2 and was negatively correlated with the Δ% values of apoptosis and tumor necrosis. Conclusions DWI and DKI parameters, especially K, are superior for imaging tumor size for the early detection of the response to DTX chemotherapy in induced rat EOC.
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Affiliation(s)
- Su-Juan Yuan
- Department of Oncology, Jinshan Hospital, Shanghai Medical College, Fudan University, 1508 Longhang Road, Shanghai, 201508, People's Republic of China
| | - Tian-Kui Qiao
- Department of Oncology, Jinshan Hospital, Shanghai Medical College, Fudan University, 1508 Longhang Road, Shanghai, 201508, People's Republic of China
| | - Jin-Wei Qiang
- Department of Radiology, Jinshan Hospital, Shanghai Medical College, University, 1508 Longhang Road, Shanghai, 201508, People's Republic of China.
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Kuai ZX, Sang XQ, Yao YF, Chu CY, Zhu YM. Evaluation of non-monoexponential diffusion models for hepatocellular carcinoma using b values up to 2000 s/mm 2 : A short-term repeatability study. J Magn Reson Imaging 2018; 50:297-304. [PMID: 30447032 DOI: 10.1002/jmri.26563] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2018] [Revised: 10/15/2018] [Accepted: 10/16/2018] [Indexed: 12/25/2022] Open
Abstract
BACKGROUND Non-monoexponential diffusion models are being used increasingly for the characterization and curative effect evaluation of hepatocellular carcinoma (HCC). But the fitting quality of the models and the repeatability of their parameters have not been assessed for HCC. PURPOSE To evaluate kurtosis, stretched exponential, and statistical models for diffusion-weighted imaging (DWI) of HCC, using b-values up to 2000 s/mm2 , in terms of fitting quality and repeatability. STUDY TYPE Prospective. POPULATION Eighteen patients with HCC. FIELD STRENGTH/SEQUENCE Conventional and DW images (b = 0, 200, 500, 1000, 1500, 2000 s/mm2 ) were acquired at 3.0T. ASSESSMENT The parameters of the kurtosis, stretched exponential, and statistical models were calculated on regions of interest (ROIs) of each lesion. STATISTICAL TESTS The fitting quality was evaluated through comparing the fitting residuals produced on the average data of ROI between different models using a paired t-test or Wilcoxon rank-sum test. Repeatability of the fitted parameters at the median values on the voxelwise data of ROI was assessed using the within coefficient of variation (WCV), the intraclass correlation coefficient (ICC), and the 95% Bland-Altman limits of agreements (BA-LA). The repeatability was divided into four levels: excellent, good, acceptable, and poor, referring to the values of ICC and WCV. RESULTS Among three models, the stretched exponential model provided the best fit to HCC (P < 0.05), whereas the statistical model produced the largest fitting residuals (P < 0.05). The repeatability of K from the kurtosis model was excellent (ICC 0.915; WCV 8.79%), while the distributed diffusion coefficient (DDC) from the stretched model was just acceptable (ICC 0.477; WCV 27.83%). The repeatability was good for other diffusion-related parameters. DATA CONCLUSION Considering the model fit and repeatability, the kurtosis and stretched exponential models are the preferred models for the description of the DW signals of HCC with respect to the statistical model. LEVEL OF EVIDENCE 2 Technical Efficacy: Stage 2 J. Magn. Reson. Imaging 2019;50:297-304.
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Affiliation(s)
- Zi-Xiang Kuai
- Imaging Center, Harbin Medical University Cancer Hospital, Harbin, P.R. China
| | - Xi-Qiao Sang
- Division of Respiratory Disease, Fourth Hospital of Harbin Medical University, Harbin, 150001, China
| | - Yuan-Fei Yao
- Imaging Center, Harbin Medical University Cancer Hospital, Harbin, P.R. China
| | - Chun-Yu Chu
- College of Engineering, Bohai University, Jinzhou, P.R. China
| | - Yue-Min Zhu
- CREATIS, CNRS UMR 5220-INSERM U1206-University Lyon 1-INSA Lyon-University, Lyon, France
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Marzi S, Minosse S, Vidiri A, Piludu F, Giannelli M. Diffusional kurtosis imaging in head and neck cancer: On the use of trace-weighted images to estimate indices of non-Gaussian water diffusion. Med Phys 2018; 45:5411-5419. [PMID: 30317646 DOI: 10.1002/mp.13238] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/22/2018] [Revised: 10/02/2018] [Accepted: 10/03/2018] [Indexed: 12/11/2022] Open
Abstract
PURPOSE While previous studies have demonstrated the feasibility and potential usefulness of quantitative non-Gaussian diffusional kurtosis imaging (DKI) of the brain, more recent research has focused on oncological application of DKI in various body regions such as prostate, breast, and head and neck (HN). Given the need to minimize scan time during most routine magnetic resonance imaging (MRI) acquisitions of body regions, diffusion-weighted imaging (DWI) with only three orthogonal diffusion weighting directions (x, y, z) is usually performed. Moreover, as water diffusion within malignant tumors is generically thought to be almost isotropic, DWI with only three diffusion weighting directions is considered sufficient for oncological application and it represents the de facto standard in body DKI. In this context, since the kurtosis tensor and diffusion tensor cannot be obtained, the averages of the three directional (Kx , Ky , Kz ) and (Dx , Dy , Dz ) - namely K and D, respectively - represent the best-possible surrogates of directionless DKI-derived indices of kurtosis and diffusivity, respectively. This would require fitting the DKI model to the diffusion-weighted images acquired along each direction (x, y, z) prior to averaging. However, there is a growing tendency to perform only a single fit of the DKI model to the geometric means of the images acquired with diffusion-sensitizing gradient along (x, y, z), referred to as trace-weighted (TW) images. To the best of our knowledge, no in vivo studies have evaluated how TW images affect estimates of DKI-derived indices of K and D. Thus, the aim of this study was to assess the potential bias and error introduced in estimated K and D by fitting the DKI model to the TW images in HN cancer patients. METHODS Eighteen patients with histologically proven malignant tumors of the HN were enrolled in the study. They underwent pretreatment 3 T MRI, including DWI (b-values: 0, 500, 1000, 1500, 2000 s/mm2 ). Some patients had multiple lesions, and thus a total of 34 lesions were analyzed. DKI-derived indices were estimated, voxel-by-voxel, using single diffusion-weighted images along (x, y, z) as well as TW images. A comparison between the two estimation methods was performed by calculating the percentage error in D (Derr ) and K (Kerr ). Also, diffusivity anisotropy (Danis ) and diffusional kurtosis anisotropy (Kanis ) were estimated. Agreements between the two estimation methods were assessed by Bland-Altman plots. The Spearman rank correlation test was used to study the correlations between Kerr /Derr and Danis /Kanis. RESULTS: The median (95% confidence interval) Kerr and Derr were 5.1% (0.8%, 32.6%) and 1.7% (-2.5%, 5.3%), respectively. A significant relationship was observed between Kerr and Danis (correlation coefficient R = 0.694, P < 0.0001), as well as between Kerr and Kanis (R = 0.848, P < 0.0001). CONCLUSIONS In HN cancer, the fit of the DKI model to TW images can introduce bias and error in the estimation of K and D, which may be non-negligible for single lesions, and should hence be adopted with caution.
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Affiliation(s)
- Simona Marzi
- Medical Physics Laboratory, IRCCS Regina Elena National Cancer Institute, 00144, Rome, Italy
| | - Silvia Minosse
- Medical Physics Laboratory, IRCCS Regina Elena National Cancer Institute, 00144, Rome, Italy
| | - Antonello Vidiri
- Radiology and Diagnostic Imaging Department, IRCCS Regina Elena National Cancer Institute, 00144, Rome, Italy
| | - Francesca Piludu
- Radiology and Diagnostic Imaging Department, IRCCS Regina Elena National Cancer Institute, 00144, Rome, Italy
| | - Marco Giannelli
- Unit of Medical Physics, Pisa University Hospital "Azienda Ospedaliero-Universitaria Pisana", 56126, Pisa, Italy
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Dregely I, Prezzi D, Kelly‐Morland C, Roccia E, Neji R, Goh V. Imaging biomarkers in oncology: Basics and application to MRI. J Magn Reson Imaging 2018; 48:13-26. [PMID: 29969192 PMCID: PMC6587121 DOI: 10.1002/jmri.26058] [Citation(s) in RCA: 35] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/05/2018] [Accepted: 03/26/2018] [Indexed: 12/12/2022] Open
Abstract
Cancer remains a global killer alongside cardiovascular disease. A better understanding of cancer biology has transformed its management with an increasing emphasis on a personalized approach, so-called "precision cancer medicine." Imaging has a key role to play in the management of cancer patients. Imaging biomarkers that objectively inform on tumor biology, the tumor environment, and tumor changes in response to an intervention complement genomic and molecular diagnostics. In this review we describe the key principles for imaging biomarker development and discuss the current status with respect to magnetic resonance imaging (MRI). LEVEL OF EVIDENCE 5 TECHNICAL EFFICACY: Stage 5 J. Magn. Reson. Imaging 2018;48:13-26.
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Affiliation(s)
- Isabel Dregely
- Biomedical Engineering, School of Biomedical Engineering & Imaging SciencesKing's Health Partners, St Thomas' HospitalLondon, UK
| | - Davide Prezzi
- Cancer Imaging, School of Biomedical Engineering & Imaging Sciences King's College London, King's Health Partners, St Thomas' Hospital, LondonUK
- RadiologyGuy's & St Thomas' NHS Foundation TrustLondonUK
| | - Christian Kelly‐Morland
- Cancer Imaging, School of Biomedical Engineering & Imaging Sciences King's College London, King's Health Partners, St Thomas' Hospital, LondonUK
- RadiologyGuy's & St Thomas' NHS Foundation TrustLondonUK
| | - Elisa Roccia
- Biomedical Engineering, School of Biomedical Engineering & Imaging SciencesKing's Health Partners, St Thomas' HospitalLondon, UK
| | - Radhouene Neji
- Biomedical Engineering, School of Biomedical Engineering & Imaging SciencesKing's Health Partners, St Thomas' HospitalLondon, UK
- MR Research CollaborationsSiemens HealthcareFrimleyUK
| | - Vicky Goh
- Cancer Imaging, School of Biomedical Engineering & Imaging Sciences King's College London, King's Health Partners, St Thomas' Hospital, LondonUK
- RadiologyGuy's & St Thomas' NHS Foundation TrustLondonUK
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Sheng RF, Yang L, Jin KP, Wang HQ, Liu H, Ji Y, Fu CX, Zeng MS. Assessment of liver regeneration after associating liver partition and portal vein ligation for staged hepatectomy: a comparative study with portal vein ligation. HPB (Oxford) 2018; 20:305-312. [PMID: 29046260 DOI: 10.1016/j.hpb.2017.09.004] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/27/2017] [Revised: 06/02/2017] [Accepted: 09/17/2017] [Indexed: 12/12/2022]
Abstract
BACKGROUND To investigate the diagnostic value of diffusion kurtosis imaging (DKI) and diffusion-weighted imaging (DWI) in assessing liver regeneration after associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) compared with portal vein ligation (PVL). METHODS Thirty rats were divided into the ALPPS, PVL, and control groups. DKI and DWI were performed before and 7 days after surgery. Corrected apparent diffusion (D), kurtosis (K) and apparent diffusion coefficient (ADC) were calculated and compared, radiologic-pathologic correlations were evaluated. RESULTS The volume of the right median lobe increased significantly after ALPPS. There were larger cellular diameters after ALPPS and PVL (P = 0.0003). The proliferative indexes of Ki-67 and hepatocyte growth factor were higher after ALPPS (P = 0.0024/0.0433). D, K and ADC values differed between the groups (P = 0.021/0.0015/0.0008). A significant correlation existed between D and the hepatocyte size (r = -0.523), no correlations existed in ADC and K (P = 0.159/0.111). The proliferative indexes showed moderate negative correlations with ADC (r = -0.484/-0.537) and no correlations with D and K (P = 0.100-0.877). DISCUSSION Liver regeneration after ALPPS was effective and superior to PVL. DKI, especially the D map, may provide added value in evaluating the microstructure of liver regeneration after ALPPS, but this model alone may perform no better than the standard monoexponential model of DWI.
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Affiliation(s)
- Ruo-Fan Sheng
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, China
| | - Li Yang
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, China
| | - Kai-Pu Jin
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, China
| | - He-Qing Wang
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, China
| | - Hao Liu
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, China
| | - Yuan Ji
- Department of Pathology, Zhongshan Hospital, Fudan University, Shanghai, China
| | - Cai-Xia Fu
- MR Collaboration NEA, Siemens Ltd., China
| | - Meng-Su Zeng
- Department of Radiology, Zhongshan Hospital, Fudan University, Shanghai Institute of Medical Imaging, Shanghai, China.
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Staging liver fibrosis with DWI: is there an added value for diffusion kurtosis imaging? Eur Radiol 2018; 28:3041-3049. [PMID: 29383522 DOI: 10.1007/s00330-017-5245-6] [Citation(s) in RCA: 41] [Impact Index Per Article: 5.9] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/25/2017] [Revised: 11/29/2017] [Accepted: 12/05/2017] [Indexed: 12/21/2022]
Abstract
OBJECTIVES To assess liver fibrosis in patients with chronic liver disease using diffusion kurtosis imaging (DKI) in comparison with conventional diffusion-weighted imaging, with histology as reference standard. METHODS This prospective study included 81 patients and DKI with b-values of 0, 200, 500, 1,000, 1,500, 2,000 s/mm2 were performed. Mean diffusivity (MD), mean kurtosis (MK) and apparent diffusion coefficient (ADC) maps were calculated. The diagnostic efficacy of MD, MK and ADC for predicting stage 2 fibrosis or greater, and stage 3 fibrosis or greater were compared. RESULTS The MD (rho=-0.491, p<0.001), MK (rho=0.537, p<0.001) and ADC (rho=-0.496, p<0.001) correlated significantly with fibrosis stages, and ADC exhibited a strong negative correlation with MK (rho=-0.968; p<0.001) and a moderate association with MD (rho=0.601, p<0.001). Areas under the curves (AUCs) for predicting stage 2 fibrosis or greater were not significantly different (p>0.05) between MK (0.809) and ADC (0.797) as well as between MD (0.715) and ADC. AUCs were also similar for MD (0.710), MK (0.768) and ADC (0.747) for predicting stage 3 fibrosis or greater. CONCLUSION Although DKI is feasible for predicting liver fibrosis in patients with chronic liver disease, MD and MK offer similar diagnostic performance to ADC values. KEY POINTS • Diffusion kurtosis imaging is feasible for staging liver fibrosis. • Diffusion kurtosis and monoexponential model are highly correlated. • The kurtosis model offers no added value to the conventional, monoexponential model.
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Budjan J, Sauter EA, Zoellner FG, Lemke A, Wambsganss J, Schoenberg SO, Attenberger UI. Diffusion kurtosis imaging of the liver at 3 Tesla: in vivo comparison to standard diffusion-weighted imaging. Acta Radiol 2018; 59:18-25. [PMID: 28454487 DOI: 10.1177/0284185117706608] [Citation(s) in RCA: 15] [Impact Index Per Article: 2.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/27/2022]
Abstract
Background Functional techniques like diffusion-weighted imaging (DWI) are gaining more and more importance in liver magnetic resonance imaging (MRI). Diffusion kurtosis imaging (DKI) is an advanced technique that might help to overcome current limitations of DWI. Purpose To evaluate DKI for the differentiation of hepatic lesions in comparison to conventional DWI at 3 Tesla. Material and Methods Fifty-six consecutive patients were examined using a routine abdominal MR protocol at 3 Tesla which included DWI with b-values of 50, 400, 800, and 1000 s/mm2. Apparent diffusion coefficient maps were calculated applying a standard mono-exponential fit, while a non-Gaussian kurtosis fit was used to obtain DKI maps. ADC as well as Kurtosis-corrected diffusion ( D) values were quantified by region of interest analysis and compared between lesions. Results Sixty-eight hepatic lesions (hepatocellular carcinoma [HCC] [n = 25]; hepatic adenoma [n = 4], cysts [n = 18]; hepatic hemangioma [HH] [n = 18]; and focal nodular hyperplasia [n = 3]) were identified. Differentiation of malignant and benign lesions was possible based on both DWI ADC as well as DKI D-values ( P values were in the range of 0.04 to < 0.0001). Conclusion In vivo abdominal DKI calculated using standard b-values is feasible and enables quantitative differentiation between malignant and benign liver lesions. Assessment of conventional ADC values leads to similar results when using b-values below 1000 s/mm2 for DKI calculation.
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Affiliation(s)
- Johannes Budjan
- Department of Clinical Radiology and Nuclear Medicine, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
| | - Elke A Sauter
- Department of Clinical Radiology and Nuclear Medicine, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
| | - Frank G Zoellner
- Computer Assisted Clinical Medicine, Medical Faculty Mannheim, Heidelberg University, Germany
| | - Andreas Lemke
- Computer Assisted Clinical Medicine, Medical Faculty Mannheim, Heidelberg University, Germany
| | - Jens Wambsganss
- Department of Clinical Radiology and Nuclear Medicine, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
| | - Stefan O Schoenberg
- Department of Clinical Radiology and Nuclear Medicine, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
| | - Ulrike I Attenberger
- Department of Clinical Radiology and Nuclear Medicine, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
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Abstract
Diffusion-weighted imaging (DWI) is increasingly incorporated into routine body magnetic resonance imaging protocols. DWI can assist with lesion detection and even in characterization. Quantitative DWI has exhibited promise in the discrimination between benign and malignant pathology, in the evaluation of the biologic aggressiveness, and in the assessment of the response to treatment. Unfortunately, inconsistencies in DWI acquisition parameters and analysis have hampered widespread clinical utilization. Focusing primarily on liver applications, this article will review the basic principles of quantitative DWI. In addition to standard mono-exponential fitting, the authors will discuss intravoxel incoherent motion and diffusion kurtosis imaging that involve more sophisticated approaches to diffusion quantification.
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Affiliation(s)
- Myles T Taffel
- Department of Radiology, New York University School of Medicine, New York, NY
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Yoshimaru D, Miyati T, Suzuki Y, Hamada Y, Mogi N, Funaki A, Tabata A, Masunaga A, Shimada M, Tobari M, Nishino T. Diffusion kurtosis imaging with the breath-hold technique for staging hepatic fibrosis: A preliminary study. Magn Reson Imaging 2017; 47:33-38. [PMID: 29158186 DOI: 10.1016/j.mri.2017.11.001] [Citation(s) in RCA: 20] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/09/2017] [Revised: 10/31/2017] [Accepted: 11/13/2017] [Indexed: 12/31/2022]
Abstract
PURPOSE To evaluate the potential of diffusion kurtosis imaging (DKI) analysis with the breath-hold technique to assess the stage or classify hepatic fibrosis. MATERIALS AND METHODS Patients (n=67) suspected of having a disease of the hepatobiliary system examined by diffusion-weighted imaging (DWI) using a 3.0-T magnetic resonance imaging unit were enrolled in this study. To evaluate hepatic fibrosis, mean kurtosis, Mean apparent diffusion (MD) and apparent diffusion coefficient (ADC) values were compared between groups with varying fibrosis; F0-F1, F2-F3, and F4. The Steel-Dwass test was used for overall comparisons. Correlations between the fibrosis stage and mean kurtosis, MD or ADC values were assessed using Spearman's rank correlation. Discriminative capacities of DKI were evaluated using receiver operating characteristic (ROC) analysis. RESULTS There were significant differences in ADC, MD and mean kurtosis values between non-cirrhosis and cirrhosis groups. Moreover, the mean kurtosis value was statistically different between the F0-F1 and F2-F3, F0-F1 and F4, and F2-F3 and F4 groups (all P<0.05). MD value was statistically different between the F0-F1 and F4 groups, and F2-F3 and F4 groups (all P<0.05). However, there was no significant difference in ADC values for all groups (all P>0.05). In addition, mean kurtosis and MD values significantly correlated with the extent of hepatic fibrosis staging (Spearman's rank correlation coefficient, ρ=0.851 and -0.672; P<0.0001). However, ADC values did not reveal a correlation with the extent of hepatic fibrosis staging (ρ=-0.227; P=0.078). According to the ROC analysis for the assessment of no fibrosis (F0), fibrosis (≥F1), and advanced fibrosis (≥F2) and liver cirrhosis, the DKI cut-off values were 0.923, 0.955, and 1.11, respectively. CONCLUSION Using the DKI method with the breath-hold technique in the liver, the stage of hepatic fibrosis can be classified into normal and early hepatic fibrosis, substantial stages, and advanced hepatic fibrosis.
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Affiliation(s)
- Daisuke Yoshimaru
- Department of Medical Technology, Tokyo Women's Medical University Yachiyo Medical Center, Owada-shinden, Yachiyo, Chiba, Japan; Division of Health Sciences, Graduate School of Medical Science, Kanazawa University, Kodatsuno, Kanazawa, Ishikawa, Japan.
| | - Toshiaki Miyati
- Division of Health Sciences, Graduate School of Medical Science, Kanazawa University, Kodatsuno, Kanazawa, Ishikawa, Japan
| | - Yuichi Suzuki
- Department of Radiological Service, The University of Tokyo Hospital, Hongo, Bunkyo-ku, Tokyo, Japan
| | - Yuhki Hamada
- Department of Medical Technology, Tokyo Women's Medical University Yachiyo Medical Center, Owada-shinden, Yachiyo, Chiba, Japan
| | - Nozomi Mogi
- Department of Medical Technology, Tokyo Women's Medical University Medical Center East, Nishiogu, Arakawa-ku, Tokyo, Japan
| | - Ayumu Funaki
- Department of Medical Technology, Tokyo Women's Medical University Yachiyo Medical Center, Owada-shinden, Yachiyo, Chiba, Japan
| | - Ayumi Tabata
- Department of Medical Technology, Tokyo Women's Medical University Yachiyo Medical Center, Owada-shinden, Yachiyo, Chiba, Japan
| | - Atsuko Masunaga
- Department of Pathology, Tokyo Women's Medical University Yachiyo Medical Center, Owada-shinden, Yachiyo, Chiba, Japan
| | - Masahiko Shimada
- Department of Gastroenterological Medicine, Tokyo Women's Medical University Yachiyo Medical Center, Owada-shinden, Yachiyo, Chiba, Japan
| | - Maki Tobari
- Department of Gastroenterological Medicine, Tokyo Women's Medical University Yachiyo Medical Center, Owada-shinden, Yachiyo, Chiba, Japan
| | - Takayoshi Nishino
- Department of Gastroenterological Medicine, Tokyo Women's Medical University Yachiyo Medical Center, Owada-shinden, Yachiyo, Chiba, Japan
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