Scott W. Atlas, MD Vascular Alexander S. Mark, #{149} M AGNETIC resonance ing can rapidly vascular flow as high when sequential Aneurysm, was intracranial, the Department tal of the University Spruce St. Philadelphia, RIG.), of Radiology, of Pennsylvania, PA 19104 and the Department Hospi- 3400 (S.W.A., of Radiology, Uni- versity of California at San Francisco (A.S.M., E.K.F.). From the 1987 RSNA annual meeting. Received April 13, 1988; revision requested May 18; revision received June 1; accepted June 27. Address reprint requests to S.W.A. © RSNA, 1988 See also the article by Atlas et al (pp 449-453) and the editorial by Bradley (pp 574-575) in this issue. and define the Robert vessel in seven venous AND angioma invasion, both spin-echo (SE) Images time (TR) of 500-800 echo time (TE) 800/20) and with GRE images a short msec obtained were repetition and of 20 msec were a short (TR/TE in all 500- cases, as were long TR/short TE (2,500-3,000/2030) and long TR/TE (2,500-3,000/80) sequences. For 42 of 63 long TR SE images, first-order gradient moment nulling was employed for constant-velocity-flow compensation (3), which has been our stan- dard head imaging protocol since it became available. In all 63 cases, the sequential section acquisition technique gradient recalled state (GRASS) a TR of 150-200 msec, and a flip variables mize the intensity depiction and the nal and fluid stationary dient moment GRE of two section gap, images were to four X 128 to opti- flow as high of cerebrospi- fluid were as low in the obtained 256 malformation imgra- two without SE with the intersection X 256 matrix, a 20-cm field of view. The diagnosis was arteniovenous formation (AVM) in 23 cases, occult brovascular in- a 3-5-mm a 0-2.5-mm or other obtained technique. excitations, thickness, a 256 the 61 of 63 cases, GRE with first-order nulling; cases, GRE images this flow-compensation use selected of blood depiction (1,2,4,5). In was performed in of 50#{176}-60#{176}. These were tensity aging and acquisition (2) was employed, msec, a TE of 13-16 angle imaging in five occlusion, in neofive cases, and on thrombosis cases, and on a combination tomognaphic findings in in (CT), SE MR. 16 cases. The compared a retrospective, with the 17 of computed and SE GRE clinical MR images MR images nonblinded fashion. RESULTS Malformation METHODS Sixty-three patients, aged 1 1 weeks to 80 years, were examined with MR imaging at 1.5 T (Signa; General Electric Medical Systems, Milwaukee). In all patients, obtained. 11 cases, intracranial cases, aneurysm in 12 cases. These diagnoses were based on surgical and pathologic findings in cases, on angiognaphic findings in 30 were limitaMR imlesions. MD Applications MR Imaging’ cases, clini- I. Grossman, #{149} Arteriovenous PATIENTS Radiology From MD mangioma) plasm in acquisition cal applications and possible tions of gradient-echo (GRE) aging in vascular intracranial steady with 1988; 169:455-461 (MR) imagdepict intrasignal intensity section to evaluate 17.73 #{149} Arteniovenous malformations, cranial, 17.70 #{149} Brain neoplasms, MR studies, 10.36 #{149} Cerebral blood vessels, abnormalities, 17.70 #{149} Cerebral blood vessels, MR studies, 17.1214 #{149} Magnetic resonance (MR), pulse sequences I K. Fram, and gradient refocusing for echo formation are used (1,2). However, the role of this technique in clinical neurologic imaging has not yet been detenmined. The purpose of this study called terms: #{149} Evan Intracranial Lesions: of Gradient-Echo To investigate the role of the gradient-echo (GRE) technique in clinical intracranial magnetic resonance (MR) imaging, 63 patients with a variety of vascular intracranial lesions were examined at 1.5 T with the use of spin-echo (SE) and GRE sequences. In all cases, the sequential section acquisition technique called gradient recalled acquisition in the steady state (GRASS) was employed; a repetition time of 150-200 msec, an echo time of 13-16 msec, and a flip angle of 500_600 were used to optimize the depiction of blood flow as high intensity and the depiction of stationary fluid as low intensity. In 61 of 63 cases, gradient moment nulling was utilized to compensate for first-order flow effects. Although GRE images rapidly demonstrated flow in vascular intracranial lesions as high intensity, the vascular nature of these lesions was also clearly evident on SE images in most cases. In some cases, GRE images can be used to clarify the vascular nature of a lesion or to characterize a neoplasm. Other applications include the detection of vascular thrombosis, occult vascular malformations, and hemorrhagic complications of vascular lesions. Index MD (cavernous and malcemehe- In 21 of 23 cases of AVM, the lesions were clearly depicted by both SE and GRE imaging (Fig 1). In the other two cases, the GRE images were superior in defining flow in residual patent vessels after surgery or proton-beam therapy (Fig 2). In all 23 AVMs, the SE findings consisted of serpentine and mound areas of signal void (Fig 1). The GRE images varied in their depiction of these lesions. In i4 of 23 cases, the entire AVM, as seen on SE images, was depicted as high intensity on GRE images (Fig 1). In seven of 23 cases, large areas of the lesions depicted as signal void on SE images were also seen as signal void on GRE images obtained with gradient moment nulling (Fig 3). In one AVM, a substantial portion of the lesion was obscured by magnetic susceptibility-melated hypointensity antifacts due to its subfmontal location near the interface between the brain and the posterior ethmoid sinus (Fig 4). In one AVM, low intensity was seen in most of the lesion, presumably because no flow-compensation gradients were employed; in this case, the same regions were high intensity on GRE images obtained with the use of gradient moment nulling (Fig 5). In six AVMs, the GRE images were superior in depicting associated hemorrhage, seen as regions of marked hypointensity (Fig 6). 455 T. ‘ J#{149} Figure 1. MR images biguously depicted ages. (c) Axial GRE images. of AVM as round (150115) with ganglionic and serpentine image obtained and a. components. Large right ganglionic 2. demonstrate MR images linear between areas hemosiderin 15) image obtained of residual after of hypointensity from with AVM prior 50#{176} flip hemorrhage larger (open therapy. regions arrows) Axial of edema and short TR/TE (600/20) or encephalomalacia residual patent turbulent flow. vessel MR images (b) SE of left insular and Radiology is unam- (b) SE imvoid on SE (closed arrows) long TRITE occipital lobe. can be made (2,800/80) (b) SE images (c) Confident distinction only GRE (150/ on axial c. left frontal images clearly depict AVM as signal void. the lesion as high intensity (closed arrows), large nulling was employed. Persistence of signal void fects may also have contributed to this appearance. #{149} (a) and in left b. 3. AVM (2,800/80) as signal angle. a. Figure intraventnicular C. proton-beam within and short TR/TE (600/20) (a) and long TRITE high intensity in areas of flow depicted b. Figure 456 intraventricular regions of signal void on axial with 50#{176} flip angle demonstrates AVM with Axial short TR/TE (600/20) (a) and (c) Although axial GRE (150/15) image obtained with 50#{176} flip regions of patency remain as signal void (open arrows), even was presumably due to turbulence, although uncompensated long TR/TE (2,800/80) angle depicts some areas though gradient moment higher-order flow motion November of ef- 1988 7). In nine Occult Cerebrovascular Malformation In four of the 1 1 cases of occult cerebrovascular malformation, all internal signal characteristics seen on SE images were lost on the GRE images (ie, marked hypointensity was present throughout the lesion) (Fig cases, no evidence of flow- ing blood within the lesion was seen on GRE images. In two cases, high intensity was present within the lesion on the GRE images, which did not differentiate ty clot. pointense GRE flow In images, cases, two lesions which from Venous high-intensi- additional were identified were seen on SE images; these lesions sumably represented other occult rebrovasculam malformations. not hyon clearly prece- Angioma In three of the venous angiomas, five patients with the GRE images more more cleanly and specifically defined the nature of the lesion, when compared with the SE images (Fig 8). In two cases, no additional information GRE was obtained from the images. Aneurysm In one of the eurysms, the five patent men was more the GRE image. tensity was ages b. portions with portion of the anlu- clearly identifiable In two cases, high present in the patients on the thrombosed of the GRE and aneurysm on in- im- patent lumen, thereby making it virtually impossible to distinguish a high-intensity clot from blood flow on the GRE sequence alone (Fig 9). In two cases, there was no information imaging difference in diagnostic obtained techniques. with the two Neoplasm In three of the seven cases in which theme was a neoplasm, the GRE images were more specific than the SE images in delineating ence of large intratumoral Figure 4. MR images of subfrontal AVM. Sagittal short TR/TE (600/20) (a, b) and axial long TR/TE (2,800/80) (c) SE images clearly depict subfrontal AVM as regions of signal void (closed arrows). (d) On axial GRE (150/15) image obtained with 50#{176} flip angle, portions of the lesion are obscured by hypointensity (open arrows) due to diamagnetic susceptibility gradient-induced signal loss from nearby air-brain interface. one of these eas of signal cases, void the presvessels. In linear and focal amon SE images were thought to represent large intratumoral vessels rather than calcification on the basis of morphologic characteristics, but GRE images showed even tensity in magnetic more these profound areas, susceptibility-induced nal loss (Fig 10). found to represent ependymoma another patient the in an low which of vessels. GRE In fossa a vascular hemanbasis of CT finddemonstrated linear mass, Axial were at CT and surgery. with a posterior heterogeneous within sig- These areas calcification mass thought to be gioblastoma on the ings, the SE images tive hypoin- indicating intensity was images GRE (150/ sugges- failed 15) images to Figure 5. tamed draining tensity with 50#{176} flip angle. Enlarged vessel AVM (arrows) appears as low inon image obtained without gradient ob- moment nulling (a), even though sequential section acquisition gradient refocusing was used. High intensity is seen within this yessel ment Volume 169 Number 2 on image nulling obtained with gradient mo- (b). Radiology 457 #{149} show and high intensity an avascular found at surgery Vessel (Fig steady-state between areas, was 11). Patency In three med in these astrocytoma of the for patency 12 patients exam- of vessels at the base of the skull, GRE MR imaging clanfied the presence of thrombosis (Figs 12, 13). In two cases, large-vessel displacement and compression by mass lesions were more clearly seen on GRE images. In two cases, high the situation, signal the intensity imaging, difference of in- can signal be movement flowing spins and that of stationary spins is, to a great extent, related to the flip angle-the larger the flip angle, the greater the difference in signal intensities (1,2,5). 2. The nonselectivity of the refocusing mechanism with GRE imaging is also a factor. In conventional SE void at least from partially rapid flow ascribed of spins out of the to section between the excitation and refocusing pulses, both of which are section- selective (6,7). To emit a signal in SE imaging, both pulses must be expenienced by the spin. In GRE imaging, the refocusing case, reversal mechanism of the read-out (in this gradi- inten- sity was present in clotted vessels, which appeared as high intensity on SE images, thereby making flow indistinguishable from clot on the basis of GRE imaging alone. In five cases, no additional information was provided by the GRE sequence. I DISCUSSION Rapid MR ed flip angles imaging and for echo acquisition blood flow as high when the posed images, utilizing gradient can signal appropriate ables are used the depiction high intensity a. (1,2,4,5). of moving on GRE limit- reversal demonstrate intensity imaging ular (a) and 8, 9. nulling MR images of intraventniculan Intraventricular long TRITE AVM (2,800/80) image obtained more obvious siderosis is clearly seen (b) SE images. on with GRE from prior hemorrhage as signal (c) AVM 50#{176} flip angle. image, indicates void on is depicted Marked prior axial and intraventnicshort as high hypointensity intraventnicular TR/TE intensity lining right hemorrhage. (600/20) on axial ventri- van- on SE fea- a. Figure b. 7. MR images of right c. panietal occult cerebrovascular malformation. Focal high-in- tensity regions are depicted within areas of hemosidenin-related hypointensity on axial short TR/TE (600/20) (a) and long TRITE (2,500/80)(b) SE images. (c) Axial GRE (150/15) image obtained with 50#{176} flip angle depicts the lesion entirely as an area of hypointensity with no evidence of intralesional flow and without internal signal characteristics. 8b. Figures 6. AVM. GRE (150/15) cle (arrows), tunes of GRE imaging: 1. With the use of sequential section acquisition rather than an interleaved multisection technique, theme is inflow of unsaturated spins into every section (assuming that at least some component of flow is present along the section-select gradient). As a result, each section is like an “entry section”-that is, flow-related enhancement (6,7) is observed on every section in the acquisition (as long as the TR is long enough to avoid steady-state effects). In the non- ment Figure The basis of spins as images, as op- to the signal void seen lies in three important 8a. b. (8) MR images of subtle venous angioma. depicts lesion as area of slight hyperintensity 9a. (a) Coronal long TR/short due to misregistnation 9b. TE (2,800/30) of compensated SE image obtained with use of gradient moflow (arrow) in left frontal deep white matter. (b) Coronal GRE (150/15) image obtained with 50#{176} flip angle demonstrates more obvious and more extensive hyperintensity (arrows) in angioma, unambiguously indicating flow. (9) MR images of partially thrombosed left middle cerebral artery giant aneurysm depict both thrombosed (1) and patent (2) portions of lumen. (a) On axial short TRITE (600/20) SE image, thrombosed portion of lumen appears as high intensity, clearly distinguishable from patent portion of lumen, which is seen as signal void. (b) Axial GRE (150/15) image obtained with 50#{176} flip angle depicts both portions of the lumen as areas of high intensity. 458 Radiology #{149} November 1988 Figure 10. MR images depicting nal void (arrows) on axial short (c) On axial GRE (150/15) image compatible with CT-documented calcification TR/TE (600/20) obtained with calcification, in ependymoma. Right cerebellopontine angle mass contains linear and focal (a) and long TR/TE (2,800/80) (b) SE images, compatible with flow or dense 50#{176} flip angle, more profound hypointensity (arrows) in areas of signal void not flow, in patent vessels. regions of sigcalcification. on SE images is the convexities (Figs 1, 3). More subtle vascular lesions, such as small venous angiomas (Fig 8), may become more conspicuous on GRE im- ages. b. Figure showed (600/20) C. 11. MR images of avascular astrocytoma. marked enhancement consistent with (a) and long TR/TE (2,500/80) of hypointensity (arrows), possibly (150/15) image obtained with 50#{176} flip eas played hypointensity cytoma rather on SE images than 169 posterior fossa mass On axial short TR/TE is consistent with operative findings focal and irregular ar(c) On axial GRE in regions that dis- of avascular astro- hemangioblastoma. moment nulling for constant-velocity Volume large (b) SE images, lesion contains indicating extensive vascularity. angle, absence of high intensity ent) is not section-selective. Therefore, spins that originally are in the appropriate section for the application of the excitation radio-frequency pulse can still contribute signal, even if they have moved out of that plane during the intempulse time (TE/2), assuming that they have not left the volume subject to the application of the read-out gradient. The nonselectivity of refocusing in GRE imaging does not result in hypenintensity of incoming spins; it merely gives flowing spins the same signal intensity as stationary spins (if all other factors are the same) rather than signal void. 3. Another component of GRE imaging that contributes to the high intensity displayed by blood flow is the introduction of gradient pulses for correction of phase changes due to flow. We used the technique of gmadient sate On CT scans, hemangioblastoma. Number (3) 2 to compenflow only (first-order motion). Rephasing induced by this method of flow compensation cannot result in higher signal intensity for blood flow than for stationary fluid of the same composition. Extra gradient pulses were added to the section-select and read-out gradients in our GRE acquisitions. Our results indicate that the value of GRE imaging for vascular intracranial lesions is limited and often depends on the specific lesion in question. AVMs are usually easily diagnosable on the basis of the SE images alone. The enlarged vascular structunes were clearly seen as signal void in the vast majority of cases on short TR/TE and long TR/TE images. The high intensity of cemebrospinal fluid on long TR/TE SE images often was very useful in highlighting lesions that contained regions of signal void, especially when the abnormal vessels were intraventnicular or located over In two patients who had under- gone proton-beam radiation therapy for AVMs, GRE images allowed confident distinction between small megions of residual patent vascular channels and hypointensity of penlesional hemosidenin seen on SE images (Fig 2). Treated AVMs therefore may necessitate adjunctive GRE imaging emphasizing flow for complete noninvasive evaluation. The appearance of large tumor yessels was more specific on GRE images. In these cases, the initial interpretation of hypointensity on SE images as due to vascular flow void was verified or disproved on the basis of the GRE images. For example, in a surgically proved, partially calcified ependymoma, the sensitivity of GRE acquisition to magnetic-susceptibility differences allowed a confident specific diagnosis of intratumomal calcification, rather than blood flow in yessels, as the cause of SE signal voids (Fig 10). In another case, a surgically proved avascular posterior fossa astrocytoma, thought initially to represent a hemangioblastoma on the basis of CT findings, was depicted as being without large vessels on the GRE image (Fig 11). Adjunctive GRE imaging of intracranial neoplasms for possible vasculamity therefore seems to be another indication for this technique, both as a means of improving the specificity of MR imaging in brain tumors and perhaps as a means of assessing the degree of malignancy. GRE imaging was often helpful in ascertaining whether ambiguous intravascular SE signal-intensity pattemns represented patent or thrombosed lumina (Figs 12, 13). The diag- Radiology 459 #{149} a. b. Figure 12. MR images of thrombosed right internal ies (closed arrows) all demonstrate signal void ular vein (open arrow) shows moderate intensity ther slow flow or thrombosis. (c) High-intensity (open arrow) can be differentiated unambiguously a. on vein. Normal left internal jugular 13. MR images of thrombosed basilar artery (600/20) (a) and long TR/TE (2,500/80) (b) SE images seen on both SE images. (c) Axial GRE (150/15) image thrombosis rather than slow Radiology and left and right internal carotid arter- Right internal (b), indicating jugular vein jugei- C. (arrow). could Ambiguous indicate obtained signal-intensity relatively with slow 50#{176} flip angle pattern seen flow or thrombosis. depicts definite in basilar Left artery pontine low intensity on axial short infarction in basilar TRITE is clearly artery, indicating flow. nosis of vascular occlusion and the clarification of patency in partially thrombosed giant aneurysms were often possible on these images, due to the depiction of blood flow as high intensity. It has been clearly shown that certain SE sequences may depict vascular flow as variable intensities under certain conditions, mainly due to the phenomena of flow-related enhancement and evenecho rephasing (6,7). Furthermore, the recent implementation of flowcompensation techniques, such as gradient moment nulling (3), in moutine head imaging (on long TR SE images) often results in high intensity within or adjacent to patent yessels. There are several pitfalls in evalu- #{149} vein axial short TR/TE (600/20) (a) and long TR/TE (2,800/80) (b) SE images. on short TRITE image (a) and increased intensity on long TR/TE image patent vessels (closed arrows) and low-intensity thrombosed right internal on axial GRE (150/15) image obtained with 50#{176} flip angle. b. Figure 460 C. jugular ating nique. blood The GRE imaging flow major with this limitation to discriminate GRE techof using flow from thrombus lies in cases in which a hypemintense subacute clot of methemoglobin is present. Methemoglobin appears as high intensity on GRE images obtained with the use of imaging variables (relatively large flip angle and short TE) selected to demonstrate flow as high intensity (Fig 9), since the contrast in these images is relatively Ti dependent (4). Furthemmore, even though flow may be present, GRE images can still demonstrate low intensity in certain cases. When GRE images are obtained without gradient moment nulling (on with inadequate compensation for higher-order flow effects), flow is not consistently tensity, even variables bulent sity depicted as high in- though other imaging are unchanged (Fig 5). Turflow is also seen as low inten- due to irretrievable random spin dephasing (8); in approximately onethird of the AVMs in our series, substantial areas of patency were depicted as low intensity on GRE images, presumably due to turbulence (Fig 3). In-plane flow and extremely slow flow (5,9) can theoretically fest as low intensity although in practice be mani- on GRE images, these have not been problematic in our experience. Hemorrhagic complications of vascular lesions are often more obvious on GRE sitivity breakdown images. of GRE This heightened sen- imaging to bloodproducts has been reportNovember 1988 this Table 1 Uses of GRE Imaging Intracranial Lesions in Vascular Small vascular malformations with abnormal flow Venous angiomas Residual AVMs after therapy Vascular malformations without abnormal flow (eg, cavernous Neoplasm tibility (10) pointensity blood flow from blood flow from calcification Differentiating hemosiderin Intravascular ty. thrombosis subacute (except when complications specific for all are associated on GRE images. In most cases, of vascular of signal with however, is due investigators to local (10-12) and magnetic-susceptibility differences from paramagnetic tionary stages of hemorrhage. evoluThese susceptibility changes result in the static local magnetic field pentunbations that shorten T2*, an effect that is compensated for by the 180#{176} radio- frequency pulse used Therefore, hemorrhage AVM on a hemorrhagic in SE imaging. from an occult cere- brovasculam malformation seen on GRE images when can the be SE im- ages fail to depict the lesion (Fig 6). In one of our cases, however, an AVM was partly obscured on the GRE image by a diamagnetic susceptibility gradient-induced hypointensity artifact due to its proximity to air-brain be noted T2* interfaces that the effects seen be associated with chronic hemorrhage. Volume 169 GRE both Number images acute and Furthermore, 2 hy- void. 6. In a limited tions of vascular lesions, number the 7. on SE images. of Haase A, Frahm FLASH imaging: AVMs 8. #{149} ing flip low angle pulses. J Magn 9. 10. 11. us- 1986; 67:258-266. 2. Wehrli F, Hecker Prost distinguishing properties called acquisition (GRASS) (abstr). can 1987; 3. Pattany Motion (MAST) Tomogr J, Roberts F. The of gradient-re- flow imaging. effects in magnetic AJR 1984; 143:1157- Evans A, Herfkens R, Spritzer CE, et al. of turbulent flow on MRI signal intensity using gradient refocused echoes. In: Book of abstracts: Society of Magnetic Resonance in Medicine 1987. Vol 1. Berkeley, Calif: Society of Magnetic Resonance in Medicine, 1987; 354. Fram E, Karis J, Evans A, et al. Fast imaging of CSF: the effect of CSF motion. In: Book of abstracts: Society of Magnetic Resonance in Medicine 1987. Vol 1. Berkeley, Calif: Society of Magnetic Resonance in Medicine, 1987; 314. Edelman RR, Johnson K, Buxton R, et al. MR of hemorrhage: new approach. AJNR 1986; 7:751-756. Mills TC, Ortendahl DA, Hylton NM, Crooks LE, Carlson JW, Kaufman L. Partial flip angle MR imaging. Radiology 1987; 12. Reson Blood The effects detec- J, Matthaei D, et al. rapid NMR imaging 154:443-450. L. 1166. References 1. Axel resonance tion of occult cerebrovascular malfonmations and lange-vessel thrombosis (unless the clot is in the high-intensity methemoglobin stage), and chamactenization of intracranial neoplasms visualized as heterogeneous signal loss Buxton RB, Edelman RR, Rosen BR, et al. Contrast in rapid MR imaging: Tl- and T2-weighted imaging. J Comput Assist Tomogr 1987; 11:7-16. Fram E, Hedlund L, Dimick R, Glover G, Herfkens R. Parameters determining the signal of flowing fluid in gradient refocused imaging: flow velocity, TR and flip angle. In: Book of abstracts: Society of Magnetic Resonance in Medicine 1986. Vol 1. Berkeley, Calif: Society of Magnetic Resonance in Medicine, 1986; 84-85. Bradley WG Jr. Waluch V. Blood flow: magnetic resonance imaging. Radiology 1985; the vascular naby the presence with an equivocal appearance on the SE examination, the GRE technique can clarify the vascular nature of the area in question. Other useful applications of this technique include the diagnosis of hemorrhagic complica- (Fig 4). It should hypointensity from on 5. SE images cases (Table 1), such as treated and small vascular malformations ed by many 4. in- GRE images can be to successfully demflow in vascular intraas high signal intensi- cleanly demonstrate ture of these lesions clot is present) Hemorrhagic lesions is not In summary, rapidly obtained onstrate blood cranial lesions hemangiomas) characterization Differentiating appearance tracellular blood by-products, since calcification (13), turbulent flow (8), chemical shift, and the boundary of regions differing in magnetic suscep- 13. 162:531-539. Atlas SW, Mark AS, Grossman RI, Gomori JM. Intracranial hemorrhage: gradientecho MR imaging at 1.5 T-comparison with spin-echo imaging and clinical applications. Radiology 1988; 168:803-807. Atlas SW, Grossman RI, Hackney DB, et al. Calcified intracranial lesions: detection with gradient echo acquisition rapid MR imaging. AJNR 1988; 9:253-259. in the steady state Magn Reson Imaging 5(suppl 1):l05. PM, Phillips JJ, Chiu LC, et al. artifact suppression technique for MR imaging. J Comput Assist 1987; 11:369-377. Radiology 461 #{149}