MRI of Short and Ultrashort T2 and T2* Components of Tissues, Fluids

The British Journal of Radiology, 84 (2011), 1067–1082 REVIEW The Agfa Mayneord lecture: MRI of short and ultrashort T2 and T2* components of tissues, fluids and materials using clinical systems G M BYDDER, FRCR Department of Radiology, University of California San Diego, San Diego, CA, USA ABSTRACT. A variety of techniques are now available to directly or indirectly detect signal from tissues, fluids and materials that have short, ultrashort or supershort T2 or T2* components. There are also methods of developing image contrast between tissues and fluids in the short T2 or T2* range that can provide visualisation of anatomy, which has not been previously seen with MRI. Magnetisation transfer methods can now be applied to previously invisible tissues, providing indirect access to supershort T2 Received 7 April 2011 components. Particular methods have been developed to target susceptibility effects Revised 29 April 2011 and quantify them after correcting for anatomical distortion. Specific methods have Accepted 30 June 2011 also been developed to image the effects of magnetic iron oxide particles with positive contrast. Major advances have been made in techniques designed to correct for loss of DOI: 10.1259/bjr/74368403 signal and gross image distortion near metal. These methods are likely to substantially ’ 2011 The British Institute of increase the range of application for MRI. Radiology It is a pleasure to thank the president and members extensively on neuroradiology, obstetrics and gynaecol- of the council of the British Institute of Radiology for ogy, as well as image perception. the opportunity to honour the memory of Professor During the first year of clinical MRI, only steady-state Mayneord, who had a pivotal role in founding medical free precession (SSFP), mobile proton density (rm) and T1 physics in the UK [1, 2]. He was prescient in suggesting weighted clinical images were available. Clinical heavily in 1945, a time when the use of magnetism in medicine T2 weighted spin-echo (SE) images arrived suddenly in was in disrepute, that the study of magnetic suscept- February 1982 and transformed the practice of MRI [15– ibility could yield both useful and interesting informa- 17]. These images showed abnormalities with high signal tion. This was published in the immediate aftermath of and contrast, and they rapidly became the mainstay of World War II in an issue of the British Medical Bulletin clinical diagnosis in the brain. Even with the subsequent celebrating the 50th anniversary of Roentgen’s discovery development of new types of sequences, such as fast spin of X-rays [3]. It was also a year before the discovery of echo [18], clinical diffusion weighted imaging [19] and nuclear magnetic resonance (NMR), 28 years before the fluid attenuated inversion recovery [20], detection of discovery of MRI, and over 40 years before the general signal from longer mean T2 relaxation components still use of susceptibility-weighted imaging (SWI) [4, 5] and remains the dominant form of MRI for diagnosis of the observation of the variation in bulk magnetic suscepti- parenchymal disease in the brain and much of the rest of bility of tendons, ligaments and menisci with orienta- the body. tion to the static magnetic field [6, 7]. However, even in 1981, low- or zero-level signals were It is also a pleasure to acknowledge the critical role of recognised in cortical bone by Smith [21] and Edelstein et Gordon Higson of the Department of Health in helping to al [22]. The appearance was attributed to short mean T2 fund the early development of X-ray CT by Sir Godfrey components in this tissue leading to undetectable signal Houndsfield and others at EMI and in supporting the early levels at the time of data acquisition. The lack of signal development of MRI partly from royalties derived from from normal tissue was useful in providing a dark CT [8]. This was a major contribution to the work done by background against which abnormalities in cortical bone, MR groups based in the UK in the late 1970s and led to with mean T2s sufficiently increased to provide detectable clinical imaging in 1980–1 [9–14]. A particular regret is the signal, could be recognised; however, the absence of death of Brian Worthington, a close collaborator with both signal meant that there was no possibility of measuring Bill Moore and Sir Peter Mansfield, and author of the first normal values of rm, T1 or T2, nor of studying normal MRI study on a series of patients [13]. Worthington wrote perfusion. In addition, there was no opportunity for active contrast manipulation, little or no distinction between T Address correspondence to: Dr Graeme Bydder, Department of adjacent short 2 tissues and no normal contrast enhance- Radiology, University of California San Diego, 200 West Arbor ment or effects from molecular imaging agents. As a Drive, San Diego, CA 92103-8226, USA. E-mail: [email protected] result, the study of cortical bone and other MR ‘‘invisible’’ The British Journal of Radiology, December 2011 1067 G M Bydder short T2 tissues, such as tendons, ligaments and menisci, zero mobile proton densities. This includes relaxation has been more limited than that of other tissues, such as agents (such as gadolinium chelates) and susceptibility brain, liver and muscle, where MR signals are readily agents (such as magnetic iron oxide particles, MIOPs). detectable with clinical systems. These materials may produce very large susceptibility In spite of these difficulties, there has been a differences in tissues and fluids, and can result in very proliferation of new approaches to imaging short T2 short T2*s. Many materials, including most plastics, also tissue components, including options for developing have short T2s. Other materials, such as contrast agents tissue contrast in the short T2 and T2* range, as well as and metals, may have no significant rm but can produce methods of imaging in the presence of metal. This has strong effects on surrounding tissues. included solutions and partial solutions to technical There is no precise definition of what constitutes a problems, some of which have appeared intractable for short echo time (TE) and what is an ultrashort TE (UTE), 20 years or more. and there is argument about how TE should be measured The theme of this paper is clinical MRI of ‘‘dark for tissues with short T2s [23–25]. For simplicity, a short matter’’ (i.e. tissues, fluids and materials that show little TE is taken to be less than 10 ms, and an ultrashort one or no signal with conventional imaging techniques). It less than 1 ms. It is also possible to define short T2/T2*s as includes direct and indirect imaging as well as spectro- less than 10 ms, ultrashort as less than 1 ms and super- scopy. As an initial step, some general principles under- short as less than 0.1 ms. This reflects the fact that, with lying this type of imaging are reviewed. older MR systems and conventional SE sequences, tissues with T2sorT2*s less than 10 ms produced little or no signal and were ‘‘invisible’’. With more recent systems General principles and gradient echo sequences, the cut-off is closer to 1 ms. Ultrashort pulse sequences can often directly detect signal The protons in rigid crystals or solids typically have in the 1–0.1 ms range, but indirect methods are usually very short T2s due to fixed field effects; however, in required to image supershort T2 (,0.1 ms) tissues. solution, motion of molecules leads to averaging of spin MR signals are usually spatially encoded using fre- interactions over time and much longer T2s. This gives quency and phase effects produced by linear applied rise to the concept of rm, representing more mobile tissue gradient fields. Susceptibility effects also include changes components with T2s that are long compared with those in the local field, and these may result in errors in locating of immobile components. The term ‘‘visible’’ can also be the position of the signal. In fact, the local susceptibility applied to the longer T2 components since they produce differences may be greater than those of the encoding detectable signal, and ‘‘invisible’’ can be applied to short gradient magnetic field and result in image distortion. T2 components, which do not result in detectable signal. This means that, in addition to shortening of T2 owing to It is important to distinguish between the T2 of the susceptibility effects, resulting in low signal, image tissue or fluid that reflects effects such as dipolar–dipolar distortion may be present with both loss of signal and interactions and chemical exchange, and the observed T2 local ‘‘pile up’’ (i.e. increase in signal where signals from (T2*) of tissues or fluids that also reflects local suscept- different regions are incorrectly superimposed on one ibility effects, chemical shift and J-coupling, as well as another). In general terms, phase encoding tolerates gross flow, magic angle and other effects. The dominant effect field distortion much better than frequency encoding both among these is often from susceptibility; this results in a for slice selection and spatial localization. shortening of T2* relative to T2 due to inhomogeneous Quantitation of tissue or fluid T2*s is made difficult by magnetic fields within voxels and intravoxel dephasing. the addition of other effects; this results in measured It is often useful to consider relaxivity, R2 or R2*, which values (T2*s) that include effects from local susceptibility 1 1 and other effects. Measurements may also be con- is the reciprocal of T2 or T2*, i.e. or , rather than the T2 T2Ã founded by distortion of the spatial encoding process transverse relaxation times. This is because relaxivities by susceptibility effects.

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