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Perfusion Magnetic Resonance Imaging Review Article | Neuroimaging and Head & Neck http://dx.doi.org/10.3348/kjr.2014.15.5.554 pISSN 1229-6929 · eISSN 2005-8330 Korean J Radiol 2014;15(5):554-577 Perfusion Magnetic Resonance Imaging: A Comprehensive Update on Principles and Techniques Geon-Ho Jahng, PhD1, Ka-Loh Li, PhD2, Leif Ostergaard, MD, PhD3, Fernando Calamante, PhD4 1Department of Radiology, Kyung Hee University Hospital at Gangdong, College of Medicine, Kyung Hee University, Seoul 134-727, Korea; 2Wolfson Molecular Imaging Center, The University of Manchester, Manchester M20 3LJ, UK; 3Center for Functionally Integrative Neuroscience, Department of Neuroradiology, Aarhus University Hospital, Aarhus C 8000, Denmark; 4Florey Institute of Neuroscience and Mental Health, Heidelberg, Victoria 3084, Australia Perfusion is a fundamental biological function that refers to the delivery of oxygen and nutrients to tissue by means of blood flow. Perfusion MRI is sensitive to microvasculature and has been applied in a wide variety of clinical applications, including the classification of tumors, identification of stroke regions, and characterization of other diseases. Perfusion MRI techniques are classified with or without using an exogenous contrast agent. Bolus methods, with injections of a contrast agent, provide better sensitivity with higher spatial resolution, and are therefore more widely used in clinical applications. However, arterial spin-labeling methods provide a unique opportunity to measure cerebral blood flow without requiring an exogenous contrast agent and have better accuracy for quantification. Importantly, MRI-based perfusion measurements are minimally invasive overall, and do not use any radiation and radioisotopes. In this review, we describe the principles and techniques of perfusion MRI. This review summarizes comprehensive updated knowledge on the physical principles and techniques of perfusion MRI. Index terms: Perfusion; Perfusion MRI; Dynamic susceptibility contrast; Dynamic contrast-enhanced; Arterial spin-labeling INTRODUCTION at the level of the capillaries, and measures in units of milliliters per 100 gram per minute. Perfusion is closely Magnetic resonance techniques have been powerful in related to the delivery of oxygen and other nutrients to visualizing tissue perfusion in the brain and other parts the tissue. Perfusion is, therefore, an essential parameter; of body. Perfusion normally refers to the delivery of blood and for this reason, much effort has been put into its measurement. It is important to distinguish between Received May 8, 2014; accepted after revision July 5, 2014. perfusion and bulk blood flow, which occurs along major G.H.J. is supported by a grant of the Korean Health Technology arteries and veins. R&D Project, Ministry for Health, Welfare & Family Affairs, Republic Two main perfusion MRI approaches have been developed: of Korea (A092125). Corresponding author: Geon-Ho Jahng, PhD, Department of those with and without the use of an exogenous contrast Radiology, Kyung Hee University Hospital at Gangdong, College of agent. The first group of techniques includes dynamic Medicine, Kyung Hee University, 892 Dongnam-ro, Gangdong-gu, susceptibility contrast (DSC)-MRI and dynamic contrast- Seoul 134-727, Korea. • Tel: (822) 440-6187 • Fax: (822) 440-6932 enhanced (DCE)-MRI; while the second group relates to • E-mail: [email protected] arterial spin-labeling (ASL). DSC-MRI is used only in the This is an Open Access article distributed under the terms of brain for the clinical evaluation of perfusion in cerebral the Creative Commons Attribution Non-Commercial License ischemia and brain tumors. This technique involves the (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in rapid intravenous injection of a magnetic resonance any medium, provided the original work is properly cited. contrast agent and the serial measurement of signal loss 554 Korean J Radiol 15(5), Sep/Oct 2014 kjronline.org Perfusion MRI during the passage of the bolus through the tissue, using sensitive biomarkers to assess medical or surgical therapies. T2 or T2*-weighted images. DCE-MRI is another perfusion The objective of this review is to describe the basic MRI method that relies on the injection of a contrast physical principles behind these techniques. The review agent, but where T1-weighted magnetic resonance images discusses the following sections: 1) perfusion MRI methods are acquired dynamically before, during, and after bolus and sources of perfusion signals, 2) physical principles of injection of a contrast agent. The data can be interpreted perfusion MRI, 3) perfusion MRI protocols, 4) perfusion MRI in terms of physiological tissue characteristics by applying parameters, 5) perfusion signal dynamics, 6) quantifications the physical principles of tracer-kinetic modeling. This of perfusion MRI signals, 7) sources of error, 8) current method has become standard in many applications. In development issues, 9) outlines of clinical applications, contrast, ASL is a perfusion MRI method for quantitatively and 10) summary of perfusion MRI. This review summarizes measuring cerebral perfusion, which is also referred to as comprehensive updated knowledge of the physical principles cerebral blood flow (CBF), by taking advantage of using the and techniques of perfusion MRI. magnetically labeled blood itself as an endogenous tracer. ASL has been extensively performed in the research arena, Perfusion MRI Methods and Sources of and sporadically applied in diseases. Perfusion Signals Contrast-based perfusion imaging methods require a high temporal resolution to capture the pass of the bolus, Table 1 lists the three major types of perfusion MRI particularly when most of the contrast agent remains techniques, which are the DSC-MRI, DCE-MRI, and ASL intravascular. These perfusion-imaging methods allow the methods. estimation of several important hemodynamic parameters, which include blood flow, blood volume, and the mean Dynamic Susceptibility Contrast (DSC)-MRI transit time (MTT). So far, the major applications have been Dynamic susceptibility contrast-MRI is one of the in the assessment and management of patients with acute exogenous contrast-based methods, and relies on the stroke and tumors. Changes in hemodynamic parameters intravenous injection of a paramagnetic contrast agent, can precede abnormalities on conventional MRI, and such as those involving gadolinium (Gd) chelates, to knowledge of whether a lesion is associated with increased generate a well-defined bolus. Most of the Gd chelates, e.g., or decreased blood flow or blood volume can frequently Gd-diethylenetriaminepentacetate, are non-diffusible blood help narrow the differential diagnosis and aid patient pool tracers. This technique utilizes very rapid imaging management. Additionally, measurement of contrast agent to capture the first pass of the contrast agent, and it is permeability, such as a transport constant related to the therefore also known as bolus tracking MRI. After the bolus permeability–surface area (Ktrans) and the fractional volume of the contrast agent is injected, hemodynamic signals of the extravascular extracellular space (EES, ve), may be of DSC-MRI depend on the T2 or T2* relaxation time, and useful to evaluate diverse diseases. Given their relationship transiently decrease because of the increasing susceptibility with the underlying biology, they have been proposed as effect (1). Table 1. Three Types of Perfusion MRI Techniques DSC DCE ASL Full term Dynamic susceptibility contrast Dynamic contrast enhanced Arterial spin labeling Bolus handling Bolus tracking Bolus passage Bolus tagging Acquisition point First pass of contrast agent Accumulation of contrast agent Accumulation of tagged blood Exogenous or endogenous Exogenous method Exogenous method Endogenous method Contrast media Intravenous bolus injection of Intravenous bolus injection of Without contrast agent Gd-based contrast agent Gd-based contrast agent Tracer Non-diffusible blood pool tracer Flow or permeability-limited Diffusible tracer diffusible tracer Relaxation mechanism T2/T2* relaxation T1 relaxation Magnetic labeled blood T1 relaxation Effect Increased susceptibility effect T1 shortening effect Blood magnetization inversion Signal behaviors Decreased signal Increased signal Subtracted signal kjronline.org Korean J Radiol 15(5), Sep/Oct 2014 555 Jahng et al. Dynamic Contrast-Enhanced (DCE)-MRI normal or abnormal physiology and its variation with time. Dynamic contrast-enhanced-MRI is the other exogenous ASL requires the subtraction of two images, one in which contrast-based method. After the bolus of the contrast the incoming blood has been labeled and the other in agent is injected, hemodynamic signals of DCE-MRI depend which no labeling has occurred. The signal difference, which on the T1 relaxation time, and increase because of the is the ASL signal and which removes the static tissue signal, T1 shortening effect associated with the paramagnetic is approximately < 1%, which makes the signal-to-noise contrast agent (2). DCE-MRI uses rapid and repeated T1- ratio (SNR) of this method relatively low. The ASL difference weighted images to measure the signal changes induced by signal depends on the blood T1 relaxation time and the the paramagnetic tracer in the tissue as a function of time. labeling decays after a long delay time. In this method, the contrast agent is also intravenously injected to generate bolus. T1-weighting is not
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