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Review
Application progress of IVIM imaging technology in evaluating physiological and pathological status of skeletal muscle
TIAN Dijiao  WAN Bing  LIU Yue  ZHANG Dewen  WANG Wen  HUANG Yitian 

Cite this article as: TIAN D J, WAN B, LIU Y, et al. Application progress of IVIM imaging technology in evaluating physiological and pathological status of skeletal muscle[J]. Chin J Magn Reson Imaging, 2024, 15(10): 222-227, 233. DOI:10.12015/issn.1674-8034.2024.10.038.


[Abstract] Skeletal muscle is an important motor organ in human body, and its function is closely related to human daily activities. However, the morphological manifestations of skeletal muscle lesions are lagging behind the microscopic pathological changes. In recent years, the evaluation of water molecule movement and capillary perfusion information of skeletal muscle from a microscopic perspective has gradually become a hot spot in clinical research. Intravoxel incoherent motion (IVIM) is a dual-exponential MR diffusion imaging technique, which uses the characteristics of water molecule diffusion and capillary network circulation to provide us with important information related to tissue function, including true diffusion coefficient (D), false diffusion coefficient (D*) and perfusion fraction (F), etc. This imaging mechanism coincides with the physiological characteristics of skeletal muscle. Based on the principles and parameters of IVIM imaging, combined with the physiological characteristics of skeletal muscle and the changes in aging and diseases, this paper summarizes the application research of IVIM technology in three aspects: physiological aging and degeneration of skeletal muscle, evaluation of skeletal muscle injury/repair in different exercise states, differential diagnosis of common muscle diseases and functional evaluation, and discusses the parameter setting, clinical significance and application limitations in related research, aiming at providing more reference value for the application of IVIM technology in skeletal muscle imaging.
[Keywords] intravoxel incoherent movement;skeletal muscle;functional magnetic resonance imaging;magnetic resonance imaging;water molecule dispersion;microcirculatory perfusion

TIAN Dijiao   WAN Bing*   LIU Yue   ZHANG Dewen   WANG Wen   HUANG Yitian  

Department of Radiology, Renhe Hospital affiliated to China Three Gorges University, Yichang 443001

Corresponding author: WAN B, E-mail: 23130293@qq.com

Conflicts of interest   None.

Received  2024-06-13
Accepted  2024-10-10
DOI: 10.12015/issn.1674-8034.2024.10.038
Cite this article as: TIAN D J, WAN B, LIU Y, et al. Application progress of IVIM imaging technology in evaluating physiological and pathological status of skeletal muscle[J]. Chin J Magn Reson Imaging, 2024, 15(10): 222-227, 233. DOI:10.12015/issn.1674-8034.2024.10.038.

[1]
PEPE G J, ALBRECHT E D. Microvascular skeletal-muscle crosstalk in health and disease[J/OL]. Int J Mol Sci, 2023, 24(13): 10425 [2024-07-04]. https://pubmed.ncbi.nlm.nih.gov/37445602/. DOI: 10.3390/ijms241310425.
[2]
HOOIJMANS M T, SCHLAFFKE L, BOLSTERLEE B, et al. Compositional and functional MRI of skeletal muscle: A review[J]. J Magn Reson Imaging, 2024, 60(3): 860-877. DOI: 10.1002/jmri.29091.
[3]
ENGLUND E K, REITER D A, SHAHIDI B, et al. Intravoxel incoherent motion magnetic resonance imaging in skeletal muscle: review and future directions[J]. J Magn Reson Imaging, 2022, 55(4): 988-1012. DOI: 10.1002/jmri.27875.
[4]
SASAKI M, SUMI, VAN CAUTEREN M, et al. Intravoxel incoherent motion imaging of masticatory muscles: pilot study for the assessment of perfusion and diffusion during clenching[J]. AJR Am J Roentgenol, 2013, 201(5): 1101-1107. DOI: 10.2214/AJR.12.9729.
[5]
NGUYEN A, LEDOUX J B, OMOUMI P, et al. Selective microvascular muscle perfusion imaging in the shoulder with intravoxel incoherent motion (IVIM)[J]. Magn Reson Imaging, 2017, 35: 91-97. DOI: 10.1016/j.mri.2016.08.005.
[6]
FILLI L, BOSS A, WURNIG M C, et al. Dynamic intravoxel incoherent motion imaging of skeletal muscle at rest and after exercise[J]. NMR Biomed, 2015, 28(2): 240-246. DOI: 10.1002/nbm.3245.
[7]
GRANATA V, FUSCO R, AMATO D M, et al. Beyond the vascular profile: conventional DWI, IVIM and kurtosis in the assessment of hepatocellular carcinoma[J]. Eur Rev Med Pharmacol Sci, 2020, 24(13): 7284-7293. DOI: 10.26355/eurrev_202007_21883.
[8]
LE BIHAN D. From Brownian motion to virtual biopsy: a historical perspective from 40 years of diffusion MRI[J/OL]. Jpn J Radiol, 2024 [2024-10-09]. https://pubmed.ncbi.nlm.nih.gov/39289243/. DOI: 10.1007/s11604-024-01642-z.
[9]
TIAN M T, DING C W. Application progress of diffusion-weighted imaging basded on mono-exponential and intravoxel incoherent motion imaging in autoimmune diseases[J]. Chin J Magn Reson Imag, 2023, 14(8): 158-164. DOI: 10.12015/issn.1674-8034.2023.08.028.
[10]
HU Y C, YAN L F, HAN Y, et al. Can the low and high b-value distribution influence the pseudodiffusion parameter derived from IVIM DWI in normal brain?[J/OL]. BMC Med Imaging, 2020, 20(1): 14 [2023-10-17]. https://pubmed.ncbi.nlm.nih.gov/32041549/. DOI: 10.1186/s12880-020-0419-0.
[11]
FOKKINGA E, HERNANDEZ-TAMAMES J A, IANUS A, et al. Advanced diffusion-weighted MRI for cancer microstructure assessment in body imaging, and its relationship with histology[J/OL]. J Magn Reson Imaging, 2023 [2024-07-10]. https://pubmed.ncbi.nlm.nih.gov/38032021/. DOI: 10.1002/jmri.29144.
[12]
CAROCA S, VILLAGRAN D, CHABERT S. Four functional magnetic resonance imaging techniques for skeletal muscle exploration, a systematic review[J/OL]. Eur J Radiol, 2021, 144: 109995 [2023-09-27]. https://pubmed.ncbi.nlm.nih.gov/34628310/. DOI: 10.1016/j.ejrad.2021.109995.
[13]
LIU K H, DING C W. The basic principle of intravoxel incoherent motion imaging and its application progress in Sjogren's syndrome[J]. Chin J Magn Reson Imag, 2022, 13(1): 161-163. DOI: 10.12015/issn.1674-8034.2022.01.038.
[14]
ZHANG J L, LEE V S. Renal perfusion imaging by MRI[J]. J Magn Reson Imaging, 2020, 52(2): 369-379. DOI: 10.1002/jmri.26911.
[15]
POOLE D C, MUSCH T I, COLBURN T D. Oxygen flux from capillary to mitochondria: integration of contemporary discoveries[J]. Eur J Appl Physiol, 2022, 122(1): 7-28. DOI: 10.1007/s00421-021-04854-7.
[16]
POOLE D C, MUSCH T I. Capillary-mitochondrial oxygen transport in muscle: paradigm shifts[J/OL]. Function, 2023, 4(3): zqad013 [2024-03-07]. https://pubmed.ncbi.nlm.nih.gov/37168497/. DOI: 10.1093/function/zqad013.
[17]
DVORETSKIY S, LIEBLEIN-BOFF J C, JONNALAGADDA S, et al. Exploring the association between vascular dysfunction and skeletal muscle mass, strength and function in healthy adults: a systematic review[J/OL]. Nutrients, 2020, 12(3): 715 [2023-12-21]. https://pubmed.ncbi.nlm.nih.gov/32156061/. DOI: 10.3390/nu12030715.
[18]
SWAIN M, UPPIN M. Evolving classification and role of muscle biopsy in diagnosis of inflammatory myopathies[J]. Indian J Pathol Microbiol, 2022, 65(Supplement): S241-S251. DOI: 10.4103/ijpm.ijpm_1033_21.
[19]
KODIPPILI K, RUDNICKI M A. Satellite cell contribution to disease pathology in Duchenne muscular dystrophy[J/OL]. Front Physiol, 2023, 14: 1180980 [2024-01-09]. https://pubmed.ncbi.nlm.nih.gov/37324396/. DOI: 10.3389/fphys.2023.1180980.
[20]
CHANG M Y, CAI Y, GAO Z H, et al. Duchenne muscular dystrophy: pathogenesis and promising therapies[J]. J Neurol, 2023, 270(8): 3733-3749. DOI: 10.1007/s00415-023-11796-x.
[21]
MAGOT A, WAHBI K, LETURCQ F, et al. Diagnosis and management of Becker muscular dystrophy: the French guidelines[J]. J Neurol, 2023, 270(10): 4763-4781. DOI: 10.1007/s00415-023-11837-5.
[22]
KAMPERMAN R G, VAN DER KOOI A J, VISSER M D, et al. Pathophysiological mechanisms and treatment of dermatomyositis and immune mediated necrotizing myopathies: a focused review[J/OL]. Int J Mol Sci, 2022, 23(8): 4301 [2023-10-29]. https://pubmed.ncbi.nlm.nih.gov/35457124/. DOI: 10.3390/ijms23084301.
[23]
XU T, GUO Y K, XU H Y, et al. Progressions in clinical application of magnetic resonance imaging in myopathy[J]. Chin J Magn Reson Imag, 2023, 14(7): 192-196, 202. DOI: 10.12015/issn.1674-8034.2023.07.035.
[24]
SIGMUND E E, BAETE S H, LUO T, et al. MRI assessment of the thigh musculature in dermatomyositis and healthy subjects using diffusion tensor imaging, intravoxel incoherent motion and dynamic DTI[J]. Eur Radiol, 2018, 28(12): 5304-5315. DOI: 10.1007/s00330-018-5458-3.
[25]
PARKER M, LILLEKER J, CHINOY H. Adult idiopathic inflammatory myopathies[J]. Medicine, 2022, 50(1): 70-75. DOI: 10.1016/j.mpmed.2021.10.011.
[26]
WANG Y Q, TIAN Z R, ZHANG L P, et al. Application of magnetic resonance image compilation in the diagnosis of dermatomyositis/polymyositis and quantitative assessment of activity[J]. Chin J Magn Reson Imag, 2023, 14(9): 92-96, 99. DOI: 10.12015/issn.1674-8034.2023.09.016.
[27]
QI J, OLSEN N J, PRICE R R, et al. Diffusion-weighted imaging of inflammatory myopathies: polymyositis and dermatomyositis[J]. J Magn Reson Imaging, 2008, 27(1): 212-217. DOI: 10.1002/jmri.21209.
[28]
RAN J, YIN C L, LIU C Y, et al. The diagnostic value of MR IVIM and T2 mapping in differentiating autoimmune Myositis from muscular dystrophy[J/OL]. Acad Radiol, 2021, 28(6): e182-e188 [2024-03-11]. https://pubmed.ncbi.nlm.nih.gov/32417032/. DOI: 10.1016/j.acra.2020.04.022.
[29]
KIM H, YONG S Y, OTGONBAATAR C, et al. Intravoxel incoherent motion diffusion-weighted MRI, fat quantification, and electromyography: correlation in polymyositis and dermatomyositis[J]. Tomography, 2024, 10(3): 368-377. DOI: 10.3390/tomography10030029.
[30]
ALCAN V, ZINNUROĞLU M. Current developments in surface electromyography[J]. Turk J Med Sci, 2023, 53(5): 1019-1031. DOI: 10.55730/1300-0144.5667.
[31]
CASEY P, ALASMAR M, MCLAUGHLIN J, et al. The current use of ultrasound to measure skeletal muscle and its ability to predict clinical outcomes: a systematic review[J]. J Cachexia Sarcopenia Muscle, 2022, 13(5): 2298-2309. DOI: 10.1002/jcsm.13041.
[32]
PARK J Y, PARK S M, LEE T S, et al. Radiopharmaceuticals for skeletal muscle PET imaging[J/OL]. Int J Mol Sci, 2024, 25(9): 4860 [2024-05-07]. https://pubmed.ncbi.nlm.nih.gov/38732077/. DOI: 10.3390/ijms25094860.
[33]
TANKISI H, BOSTOCK H, TAN S V, et al. Muscle excitability testing[J]. Clin Neurophysiol, 2024, 164: 1-18. DOI: 10.1016/j.clinph.2024.04.022.
[34]
NI M, YUAN H S. Opportunities and challenges of musculoskeletal imaging: achievements and prospects over the past decade in China[J]. Chin J Magn Reson Imag, 2022, 13(10): 18-22, 45. DOI: 10.12015/issn.1674-8034.2022.10.003.
[35]
POTCOVARU C G, FILIP P V, NEAGU O M, et al. Diagnostic criteria and prognostic relevance of sarcopenia in patients with inflammatory bowel disease-a systematic review[J/OL]. J Clin Med, 2023, 12(14): 4713 [2024-05-15]. https://pubmed.ncbi.nlm.nih.gov/37510827/. DOI: 10.3390/jcm12144713.
[36]
ALYAMI A S. Imaging of ulcerative colitis: the role of diffusion-weighted magnetic resonance imaging[J/OL]. J Clin Med, 2024, 13(17): 5204 [2024-10-07]. https://pubmed.ncbi.nlm.nih.gov/39274415/. DOI: 10.3390/jcm13175204.
[37]
MINNITI G, PESCININI-SALZEDAS L M, MINNITI G A D S, et al. Organokines, sarcopenia, and metabolic repercussions: the vicious cycle and the interplay with exercise[J/OL]. Int J Mol Sci, 2022, 23(21): 13452 [2024-03-17]. https://pubmed.ncbi.nlm.nih.gov/36362238/. DOI: 10.3390/ijms232113452.
[38]
OGURA A, SOTOME H, ASAI A, et al. Evaluation of capillary blood volume in the lower limb muscles after exercise by intravoxel incoherent motion[J]. Radiol Med, 2020, 125(5): 474-480. DOI: 10.1007/s11547-020-01163-5.
[39]
ADELNIA F, SHARDELL M, BERGERON C M, et al. Diffusion-weighted MRI with intravoxel incoherent motion modeling for assessment of muscle perfusion in the thigh during post-exercise hyperemia in younger and older adults[J/OL]. NMR Biomed, 2019, 32(5): e4072 [2023-09-13]. https://pubmed.ncbi.nlm.nih.gov/30861224/. DOI: 10.1002/nbm.4072.
[40]
YOON M A, HONG S J, KU M C, et al. Multiparametric MR imaging of age-related changes in healthy thigh muscles[J]. Radiology, 2018, 287(1): 235-246. DOI: 10.1148/radiol.2017171316.
[41]
GROSICKI G J, ZEPEDA C S, SUNDBERG C W. Single muscle fibre contractile function with ageing[J]. J Physiol, 2022, 600(23): 5005-5026. DOI: 10.1113/JP282298.
[42]
DELOREY D S. Sympathetic vasoconstriction in skeletal muscle: modulatory effects of aging, exercise training, and sex[J]. Appl Physiol Nutr Metab, 2021, 46(12): 1437-1447. DOI: 10.1139/apnm-2021-0399.
[43]
NYBERG M, JONES A M. Matching of O2 utilization and O2 delivery in contracting skeletal muscle in health, aging, and heart failure[J/OL]. Front Physiol, 2022, 13: 898395 [2023-10-28]. https://pubmed.ncbi.nlm.nih.gov/35774284/. DOI: 10.3389/fphys.2022.898395.
[44]
DIVITO B, MCLAUGHLIN M, JACOBS I. The effects of L-citrulline on blood-lactate removal kinetics following maximal-effort exercise[J]. J Diet Suppl, 2022, 19(6): 704-716. DOI: 10.1080/19390211.2021.1926392.
[45]
LEE S, CHOI Y, JEONG E, et al. Physiological significance of elevated levels of lactate by exercise training in the brain and body[J]. J Biosci Bioeng, 2023, 135(3): 167-175. DOI: 10.1016/j.jbiosc.2022.12.001.
[46]
MASTROPIETRO A, PORCELLI S, CADIOLI M, et al. Triggered intravoxel incoherent motion MRI for the assessment of calf muscle perfusion during isometric intermittent exercise[J/OL]. NMR Biomed, 2018, 31(6): e3922 [2023-08-21]. https://pubmed.ncbi.nlm.nih.gov/29637672/. DOI: 10.1002/nbm.3922.
[47]
JUNGMANN P M, PFIRRMANN C, FEDERAU C. Characterization of lower limb muscle activation patterns during walking and running with Intravoxel Incoherent Motion (IVIM) MR perfusion imaging[J]. Magn Reson Imaging, 2019, 63: 12-20. DOI: 10.1016/j.mri.2019.07.016.
[48]
NGUYEN A, LEDOUX J B, OMOUMI P, et al. Application of intravoxel incoherent motion perfusion imaging to shoulder muscles after a lift-off test of varying duration[J]. NMR Biomed, 2016, 29(1): 66-73. DOI: 10.1002/nbm.3449.
[49]
OHNO N, MIYATI T, FUJIHARA S, et al. Biexponential analysis of intravoxel incoherent motion in calf muscle before and after exercise: comparisons with arterial spin labeling perfusion and T2[J]. Magn Reson Imaging, 2020, 72: 42-48. DOI: 10.1016/j.mri.2020.06.003.
[50]
LI J, LU Z P, YUAN L, et al. Intravoxel incoherent motion imaging to assess the acute effects of moderate-intensity continuous training and high-intensity interval training on thigh muscles[J/OL]. NMR Biomed, 2024, 37(1): e5045 [2024-05-21]. https://pubmed.ncbi.nlm.nih.gov/37852945/. DOI: 10.1002/nbm.5045.
[51]
NGAMSOM S, NAKAMURA S, SAKAMOTO J, et al. The intravoxel incoherent motion MRI of lateral pterygoid muscle: a quantitative analysis in patients with temporomandibular joint disorders[J/OL]. Dentomaxillofac Radiol, 2017, 46(5): 20160424 [2023-12-20]. https://pubmed.ncbi.nlm.nih.gov/28332854/. DOI: 10.1259/dmfr.20160424.
[52]
SHAHIDI B, BEHUN J J, BERRY D B, et al. Intravoxel incoherent motion imaging predicts exercise-based rehabilitation response in individuals with low back pain[J/OL]. NMR Biomed, 2021, 34(12): e4595 [2023-12-26]. https://pubmed.ncbi.nlm.nih.gov/34327758/. DOI: 10.1002/nbm.4595.
[53]
FEDERAU C, KROISMAYR D, DYER L, et al. Demonstration of asymmetric muscle perfusion of the back after exercise in patients with adolescent idiopathic scoliosis using intravoxel incoherent motion (IVIM) MRI[J/OL]. NMR Biomed, 2020, 33(3): e4194 [2024-01-11]. https://pubmed.ncbi.nlm.nih.gov/31815323/. DOI: 10.1002/nbm.4194.
[54]
XU X Q, CHOI Y J, SUNG Y S, et al. Intravoxel incoherent motion MR imaging in the head and neck: correlation with dynamic contrast-enhanced MR imaging and diffusion-weighted imaging[J]. Korean J Radiol, 2016, 17(5): 641-649. DOI: 10.3348/kjr.2016.17.5.641.
[55]
TANG H, YU L, SUO S T, et al. Evaluation of skeletal muscle perfusion changes in patients with peripheral artery disease before and after percutaneous transluminal angioplasty using multiparametric MR imaging[J]. Magn Reson Imaging, 2022, 93: 157-162. DOI: 10.1016/j.mri.2022.08.001.
[56]
SHU D B, ZHANG C, DAI S Y, et al. Acute effects of foam rolling on hamstrings after half-marathon: a muscle functional magnetic resonance imaging study[J/OL]. Front Physiol, 2021, 12: 723092 [2023-11-25]. https://pubmed.ncbi.nlm.nih.gov/34690798/. DOI: 10.3389/fphys.2021.723092.
[57]
RIEXINGER A, LAUN F B, HÖGER S A, et al. Effect of compression garments on muscle perfusion in delayed-onset muscle soreness: a quantitative analysis using intravoxel incoherent motion MR perfusion imaging[J/OL]. NMR Biomed, 2021, 34(6): e4487 [2023-12-09]. https://pubmed.ncbi.nlm.nih.gov/33594766/. DOI: 10.1002/nbm.4487.

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