Sulcal Hyperintensity on Fluid-Attenuated Inversion Recovery MR Images in Patients Without Apparent Cerebrospinal Fluid Abnormality

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1 Toshiaki Taoka 1,2 William T. C. Yuh 1 Matthew L. White 1 Jerome P. Quets 1 Joan E. Maley 1 Toshihiro Ueda 1 Received pril 25, 2000; accepted after revision ugust 10, Department of Radiology, Magnetic Resonance Imaging Center, University of Iowa College of Medicine, 200 Hawkins Dr., Iowa City, I Present address: Department of Radiology, Nara Medical University, 840 Shijo, Kashihara, Nara, Japan. ddress correspondence to T. Taoka. JR 2001;176: X/01/ merican Roentgen Ray Society Sulcal Hyperintensity on Fluid-ttenuated Inversion Recovery MR Images in Patients Without pparent Cerebrospinal Fluid bnormality OJECTIVE. Failure to suppress cerebrospinal fluid (CSF) signal intensity (sulcal hyperintensity) on fluid-attenuated inversion recovery (FLIR) images has been reported in patients with abnormal CSF, such as those with meningitis and subarachnoid hemorrhage. Our study investigates the clinical history and MR findings associated with sulcal hyperintensity on FLIR images in patients without apparent CSF abnormality. SUJECTS ND METHODS. Three hundred consecutive MR imaging examinations were prospectively screened for patients with sulcal hyperintensity on FLIR images. Nine patients with clinical, CT, or laboratory evidence suggesting abnormal CSF were excluded. The distribution of sulcal hyperintensity on FLIR images and associated abnormal enhancement were evaluated. The presence of the dirty CSF sign (mild increase in CSF signal on unenhanced T1-weighted images or mild decrease on T2-weighted images) in the corresponding hyperintense sulcus was also assessed. RESULTS. Twenty-six (8.9%) of the 291 patients had sulcal hyperintensity (16 focal, 10 diffuse) associated with 18 masses (6.1%) and eight vascular abnormalities (2.7%). Sulcal hyperintensity was frequently associated with the dirty CSF sign (69.2%) and abnormal contrast enhancement (overall, 96.2%; 88.5%, leptomeningeal; 53.8%, vascular enhancement). CONCLUSION. Our study shows that sulcal hyperintensity on FLIR imaging can occur in patients without apparent CSF abnormality. Its frequent association with mass effect, vascular disease, abnormal vascular enhancement, and dirty CSF sign suggests that an increase in blood pool, a small amount of protein leakage, and the flow-entering phenomenon of the congested blood may contribute to sulcal hyperintensity on FLIR images. ecause of the ability to increase lesion contrast, suppress normal cerebrospinal fluid (CSF) signal intensity, and acquire images with a relatively short acquisition time with fast imaging techniques, fluid-attenuated inversion recovery (FLIR) imaging has mostly replaced proton density weighted imaging for the evaluation of supratentorial brain disease [1 10]. When compared with T2-weighted and proton density weighted imaging, FLIR imaging has been reported to be superior in the evaluation of acute stroke and parenchymal lesions near CSF [8, 11]. In addition, FLIR imaging has been advocated as a sensitive MR technique (up to 100%) in the detection of subarachnoid hemorrhage [12, 13]. Therefore, the presence of sulcal hyperintensity on FLIR imaging has generally been considered suggestive of abnormal CSF, such as in meningitis and subarachnoid hemorrhage. Our project was initiated after observing sulcal hyperintensity on FLIR imaging in several patients with acute stroke who had no clinical, CT, or laboratory evidence of subarachnoid hemorrhage. Our purpose was to prospectively investigate whether sulcal hyperintensity can occur in patients without apparent CSF abnormality and to correlate the presence of sulcal hyperintensity with clinical history, underlying pathophysiology, and associated MR findings. In addition, we propose several possible mechanisms to explain sulcal hyperintensity on FLIR imaging in patients without CSF abnormality. Subjects and Methods We prospectively screened for sulcal hyperintensity on FLIR imaging in 300 consecutive patients undergoing contrast-enhanced and unenhanced brain MR imaging. When charts were reviewed, nine patients with apparent clinical, laboratory, or CT evidence to suggest abnormal CSF (such as meningitis, subarachnoid hemorrhage, or seeding of metastasis) were excluded. The underlying diseases of patients with sulcal hyperintensity on FLIR imaging were classified into two groups: those with mass effect and JR:176, February

2 Taoka et al. those with vascular abnormality. Two neuroradiologists retrospectively and independently reviewed the MR images of all patients with sulcal hyperintensity on FLIR images. Sulcal hyperintensity on FLIR imaging was defined as hyperintensity in the CSF space of one or more cortical sulci or cerebellar sulci and as normal CSF hypointensity on the remaining sulcal or ventricular spaces. Hyperintensities on the surface of the cortex were carefully excluded by comparing T1-weighted and T2-weighted images. We also excluded artifact from dental material, which shows typical MR characteristics and geometric patterns overlapping anatomic structures. Discrepancies between reviewers interpretations were resolved by consensus. On FLIR images, the pattern of the sulcal hyperintensity was further classified as focal or diffuse. Sulcal hyperintensity limited to a single lobe of the brain was considered focal, whereas more widespread abnormality involving two or more lobes was considered diffuse. In the cerebellum, the focal group was defined as sulcal hyperintensity that did not extend across the great horizontal fissure or across the midline. The sulci with hyperintensity on FLIR imaging were also evaluated for the presence of mild hyperintensity on unenhanced T1-weighted images or mild hypointensity on T2-weighted images ( dirty CSF sign) [14]. The presence and pattern of abnormal enhancement in the corresponding sulcal space with sulcal hyperintensity on FLIR were also assessed. Patterns of abnormal enhancement included leptomeningeal enhancement, sheetlike enhancement located deep in and along the sulci, and vascular (linear or tubular) enhancement. MR imaging was performed with either a 1.5-T Signa MR imaging system (General Electric Medical Systems, Milwaukee, WI) or a 1.5-T Vision MR imaging system (Siemens, Erlangen, Germany). Unenhanced MR examinations included FLIR images (TR/TE eff range, 8000/80 130; inversion time, 2000 msec; echo train length, 8), fast spin-echo T2-weighted images (8000/90 100; echo train length, 8), and spinecho T1-weighted images (TR range/te range, /16 20), with the axial plane; section thickness, 5 mm; matrix size, ; field of view, cm; and a head coil. ll FLIR images were obtained before the administration of contrast medium. Contrast-enhanced T1-weighted images with parameters identical to unenhanced T1-weighted images were obtained after the IV injection of 0.1 mmol/kg of gadopentetate dimeglumine (Magnevist; erlex Laboratories, Wayne, NJ). Results Twenty-six (8.9%; age range, 2 88 years; 14 males and 12 females) of the 291 patients showed sulcal hyperintensity on FLIR images. Eighteen mass lesions included six meningiomas (Fig. 1), five metastatic brain tumors, Fig year-old woman with large meningioma., Unenhanced fluid-attenuated inversion recovery image (TR/TE eff, 8000/108; inversion time, 2000 msec; echo train length, 8) shows hyperintensity (arrows) in sulcal space of both hemispheres, whereas cerebrospinal fluid in lateral ventricle shows hypointensity., Contrast-enhanced MR image (TR/TE, 500/20) shows some linear enhancement (arrows ) along gyri, which suggests leptomeningeal enhancement. C Fig year-old man with acute middle cerebral artery stroke (main lesion of infarction is not shown)., Unenhanced fluid-attenuated inversion recovery image (TR/TE eff, 8000/108; inversion time, 2000 msec; echo train length, 8) shows hyperintensity (arrow) in sulcal space of left frontal lobe., Contrast-enhanced MR image (TR/TE, 500/20) shows linear enhancement (arrow) along surface of gyri, which occupy almost entire sulcal space. C, T2-weighted image (TR/TE eff range, 8000/90 100; echo train length, 8) shows slight hypointensity (arrow) in corresponding sulcus. (Fig. 2 continues on next page) 520 JR:176, February 2001

3 MR Imaging of Sulcal Hyperintensity Fig. 2. (continued) 77-year-old man with acute middle cerebral artery stroke (main lesion of infarction is not shown). D, Unenhanced T1-weighted image (TR/TE, 500/20) shows relatively slight hyperintensity (arrow) in corresponding sulcus compared with other sulci. E, Gradient-echo T2*-weighted image (250/15; flip angle, 20 ) shows mild hypointensity (arrow) in involved sulci. This is likely caused by focal magnetic inhomogeneity from content (deoxyhemoglobin) of blood pool due to alteration of hemodynamics and suggests venous congestion. one astrocytoma, two subdural hematomas, two cases of hydrocephalus, and two subcortical hematomas. Eight patients had vascular abnormalities, including six patients with ischemic stroke (Fig. 2), one patient with venous thrombosis (Fig. 3), and one patient with dural arteriovenous fistula (Fig. 4). The pattern of sulcal hyperintensity on FLIR imaging limited to one lobe (focal pattern) was found in 15 patients and extended to two or more lobes (diffuse pattern) in 11 patients. lthough there was no statistical significance, patients with mass effect, 12 (66.7%) of 18 patients, were more likely to have a focal pattern of sulcal hyperintensity, whereas patients with vascular abnormalities, five (62.5%) of eight patients, were more likely to have a diffuse pattern. bnormal contrast-enhancement pattern was frequently seen, occurring in 25 (96.1%) of 26 patients with sulcal hyperintensity. Leptomeningeal enhancement in the corresponding area was the most frequent pattern observed, occurring in 23 (88.5%) of 26 patients with sulcal hyperintensity and associated with all cases of vascular abnormality (100%) and 15 (83.3%) of the 18 cases of mass effect groups. bsence of leptomeningeal enhancement occurred in only three (11%) of 26 small mass lesions (meningioma, subcortical hematoma, and metastatic brain tumor). Vascular (arterial or venous) enhancement was seen in 14 (53.8%) of 26 patients. The dirty CSF sign (mild hyperintensity in the sulcus on T1-weighted images) corresponding to sulcal intensity on FLIR images was seen in 18 (69.2%) of 26 patients with sulcal hyperintensity on FLIR images (Fig. 2). The dirty CSF sign was more prevalent in six (75%) of eight patients in the vascular group, whereas the sign was seen in 12 (66.7%) of 18 patients in the mass effect group. Discussion Sulcal hyperintensity is a term describing the failure to suppress the CSF signal on FLIR imaging. It has been described in the past as hyperintense CSF, leptomeningeal hyperintensity, or hyperintensity within the subarachnoid space [12, 15 18]. Such findings have been reported extensively in patients with abnormal CSF, such as those with subarachnoid hemorrhage and meningitis [1, 12, 13, 16]. Our study was initiated after observing sulcal hyperintensity on FLIR imaging in several patients who had no clinical, CT, or laboratory evidence to suggest abnormality in the CSF. Our preliminary results suggest that the findings could be observed consistently in a larger patient population. Our findings are not rare and are reproducible. These findings confirm our opinion that sulcal hyperintensity on FLIR imaging does not always indicate CSF abnormality such as in subarachnoid hemorrhage or meningitis. To investigate possible mechanisms causing sulcal hyperintensity on FLIR imaging in patients without apparent CSF abnormality, we evaluated several characteristic MR findings that may reflect the underlying pathophysiologies. These included the distribution (focal versus diffuse) of sulcal hyperintensity on FLIR imaging, association of abnormal vascular enhancement (leptomeningeal and vascular), and corresponding CSF signal changes (dirty CSF sign) on the D unenhanced conventional T1- and T2- weighted images. These findings were then correlated with the underlying pathophysiologies (mass effect or vascular disease) of the patients. The distribution pattern of sulcal hyperintensity on FLIR imaging may reflect the spatial relationship between the lesion and sulcal hyperintensity. The frequent association of an abnormal vascular enhancement pattern may reflect the alteration of underlying hemodynamics associated with various vascular diseases or with breakdown of the blood brain barrier. The dirty CSF sign in the sulcus may reflect a similar mechanism causing the sulcal hyperintensity on FLIR imaging. Our findings show that sulcal hyperintensity on FLIR imaging caused by vascular disease in patients without apparent CSF abnormality tended to be more diffuse and extensive than sulcal hyperintensity caused by mass effect. In patients with vascular abnormalities, sulcal hyperintensity was always associated with abnormal vascular enhancement and suggested that the alteration of the underlying hemodynamics in the involved sulcal space may play a role in the failure of nulling the normal CSF signal (Figs. 2 4). Sulcal hyperintensity on FLIR imaging in patients with mass effect tended to be limited to those compressed sulcal spaces immediately adjacent to the mass. In this group of patients, sulcal hyperintensity was again frequently associated with focal vascular enhancement particularly associated with large masses. Therefore, sulcal hyperintensity on FLIR imaging associated with mass effect in patients without apparent CSF abnormality may also be caused by the alteration of E JR:176, February

4 Taoka et al. regional hemodynamics due to sulcal and vascular compression by the mass itself. bnormal enhancement suggests that the breakdown of the blood brain barrier and leakage of the protein (serum) into the local sulcus may exist concurrently. The dirty CSF sign was frequently seen in our patients in the corresponding sulcal spaces with sulcal hyperintensity, but not in the remaining sulcal spaces distant to or on the contralateral side of the brain (Fig. 2). The dirty CSF sign has been reported in cases of subarachnoid hemorrhage [14], presumably because of the paramagnetic effect from the blood product and high protein concentration in the CSF itself. lthough the cause of the shortening of the T1 and T2 relaxation times of the CSF in the sulcal space is unknown, in our patients, it is unlikely that it originates from the CSF D Fig year-old woman with sagittal sinus thrombosis., Unenhanced fluid-attenuated inversion recovery image (TR/TE eff, 8000/108; inversion time, 2000 msec; echo train length, 8) shows hyperintensity in superior sagittal sinus due to venous thrombosis. lmost all cortical sulci of both hemispheres show hyperintensity especially in right occipital region (arrows)., Contrast-enhanced MR image (TR/TE, 450/20) shows gyral enhancement in right occipital region (arrows). C, T2-weighted image (TR/TE eff, 8000/90; echo train length, 8) shows hyperintensity in superior sagittal sinus (arrows) likely due to venous thrombosis D, Unenhanced T1-weighted image (TR/TE, 450/20) shows relative hyperintensity in corresponding cortical sulci (arrows) compared with that shown in lateral ventricles. alone because no evidence suggests abnormality in the CSF. The mechanism causing changes in the sulcal signal on FLIR images and unenhanced T1- and T2-weighted imaging (dirty CSF sign) may be similar in patients without CSF abnormality. Several mechanisms have been proposed to explain the failure of the nulling of CSF signal intensity (sulcal hyperintensity) on FLIR imaging, mostly involving patients with CSF abnormality [12, 17, 19]. In patients with abnormal CSF, it is generally accepted that the failure to suppress CSF on FLIR imaging is caused by the shortening of T1 relaxation of the protons in the CSF due to blood products and higher protein concentration in the CSF [12, 15]. In our study, patients with sulcal hyperintensity on FLIR images had no apparent clinical, laboratory, or CT evidence of abnormal CSF. However, on the basis of the frequent association of abnormal enhancement to sulcal hyperintensity on FLIR images, local breakdown of the blood brain barrier may be another cause of sulcal hyperintensity [20, 21]. Local serum leakage may cause local higher protein concentration of CSF, which does not reflect overall CSF findings as in subacute stroke. Local CSF with higher protein concentration may show reduced T1 relaxation time causing hyperintensity on FLIR imaging. ecause some instances show sulcal hyperintensity on FLIR imaging without evidence of blood brain barrier breakdown as in venous abnormality or mass effect, local protein leakage may not be the only cause of sulcal hyperintensity on FLIR imaging. nother possible mechanism is the flow-entering phenomenon of CSF flow because C 522 JR:176, February 2001

5 MR Imaging of Sulcal Hyperintensity FLIR imaging applies an inversion pulse. With the flow-entering phenomenon, the protons of the CSF outside the imaging plane that have not experienced inversion pulses may have a higher signal than those protons that remain in the imaging plane on FLIR images. However, CSF flow effect should differ from section to section, and the signal of the entry section should be the highest. lthough we cannot completely exclude the CSF flow-entering phenomenon, this mechanism was not readily appreciated in our study. lthough this effect is prevalent in the basal cisterns in which CSF pulsation can be a significant factor, it is uncommon over the convexities of the brain where CSF motion is diminished. In addition, signal changes caused by turbulent CSF flow tended to be more inhomogeneous, whereas by visual examination, sulcal hyperintensity was generally seen diffusely in the sulcal spaces in our patients. On the other hand, the flow-entering phenomenon of the vessels should be taken into account. Fig year-old man with dural arteriovenous fistula., Unenhanced fluid-attenuated inversion recovery (FLIR) image (TR/TE eff, 8000/108; inversion time, 2000 msec; echo train length, 8) before treatment shows slight sulcal hyperintensity in right temporal lobe (arrow )., Contrast-enhanced MR image (TR/TE, 500/20) before treatment shows multiple serpentine hypointense structures in right temporal lobe as compared with contralateral side before embolization, most likely representing high-flow vasculature of arteriovenous shunt. C, Unenhanced FLIR image (TR/TE eff, 8000/108; inversion time, 2000 msec; echo train length, 8) after treatment shows that sulcal hyperintensity becomes more extensive after embolization (arrows). D, Contrast-enhanced MR image (TR/TE, 500/20) after treatment shows enhanced vessels suggesting slow-flowing blood vessels. Hypointense vessels on contrast-enhanced MR image () before treatment become hyperintense with vascular enhancement after embolization (arrows), suggesting alteration of hemodynamics. The blood from outside the imaging plane will have high signal intensity on FLIR images. CSF signal changes on FLIR have been reported in one case of moyamoya disease [19], in which engorged pial vasculature from leptomeningeal anastomoses was the proposed cause of the sulcal hyperintensity as seen in our patients (Figs. 2 4). In our study, abnormal enhancement patterns including leptomeningeal and vascular enhancement were frequently associated with hyperintense CSF on FLIR images. Leptomeningeal enhancement extended into the depths of the sulci and reflected the vascular hemodynamic changes at pial-to-arachnoid (arterial capillary and venous) levels. lthough slow flow in leptomeningeal collaterals has been proposed and pathophysiologically correlates with vascular enhancement [22], other factors including arterial, venous, perivascular, and leptomeningeal contrast medium accumulation may also cause intravascular enhancement [23 27]. ll cases of hydrocephalus, subdural hematoma, and large mass showed diffuse CSF hyperintensity on FLIR imaging and diffuse leptomeningeal enhancement. In these cases, intracranial pressure is expected to be elevated and again leads to more extensive venous congestion as compared with those cases of small focal lesions. Our data cannot reveal why the abnormal enhancement pattern has a high association with CSF hyperintensity on FLIR imaging or how its mechanism contributes to the high signal intensity. However, these findings appear to show, at least in part, that the alteration of the regional vascular dynamics such as congestion, inflammation, or slow flow can play a role in the presence of CSF hyperintensity on FLIR imaging in patients with normal CSF. The expansion of the blood pool in the corresponding sulcal space causing failure of the nulling of the CSF signal may be a possible mechanism. The sulcal space consists primarily of the CSF and, to a much lesser extent, the blood vessels consisting of arteries, arteriocap- C D JR:176, February

6 Taoka et al. illary bed (leptomeningeal), and venous network. In a normal sulcus, the relatively small volume and oxygenation status of the blood pool in the vascular structure has a minimal effect on the local magnetic field and signal intensity of CSF protons. Therefore, in the healthy patient, the signal intensity of the sulcal space on FLIR imaging is low because of a successful suppression of the dominant CSF signal in the sulci. However, the blood pool can become more influential in patients with an alteration of the underlying hemodynamics. The blood pool effect can theoretically increase when the relative volume ratio of CSF blood in a voxel is decreased (as with a decrease in sulcal CSF space or an increase in intravascular volume caused by mass effect or vascular disease). Diffuse sulcal hyperintensity on FLIR images was seen in our patients with evidence of an increase in venous pressure and blood pool such as in a case of dural sinus occlusion (Fig. 3) and in another case of pre- and posttreatment of dural arteriovenous fistula (Fig. 4). The congested venous blood pool increases in volume and contains a higher concentration of deoxyhemoglobin compared with the normal state. This condition can cause shortening of T2* relaxation time due to the paramagnetic effects of deoxyhemoglobin. In our study, we obtained gradient-echo T2*-weighted images in a stroke patient. In this patient, the area corresponding to the sulcal hyperintensity on FLIR images and congested vasculature on the T2*- weighted images showed mild hypointensity suggesting an increase in local field inhomogeneity (Fig. 2). These cases again suggest that alteration of hemodynamics causing increased blood pool may play a role in sulcal hyperintensity on FLIR imaging. Our study had several limitations. Our preliminary data cannot prove or disprove the mechanism explaining the sulcal hyperintensity on FLIR imaging in patients without apparent CSF abnormality. In addition, we only prospectively screened 300 MR images to recruit patients for retrospective review. Only those cases with MR images that contained unenhanced and contrast-enhanced T1- weighted and T2-weighted FLIR images were included. Therefore, incidence and sensitivity of detecting sulcal hyperintensity and its associated pathophysiology and other MR findings were biased. Finally, the proposed mechanisms in this study are speculative and are based indirectly on the MR imaging and clinical findings without definitive proof. Sulcal hyperintensity on FLIR is a nonspecific finding and occurs frequently in patients without CSF abnormality. Therefore, caution should be taken in interpreting such findings particularly in the emergency treatment of central nervous system diseases that requires information to avoid potential hemorrhagic complications. With the frequent association of vascular disease, mass effect, abnormal vascular enhancement, and dirty CSF sign, we speculate that alteration in vascular hemodynamics with slow flow, increased blood pool, and a small amount of protein leakage may be the cause for the failure in suppression of the CSF signal (sulcal hyperintensity) in patients without apparent CSF abnormality. References 1. Kates R, tkinson D, rant-zawadzki M. Fluidattenuated inversion recovery (FLIR): clinical prospectus of current and future applications. Top Magn Reson Imaging 1996;8: Essig M, Hawighorst H, Schoenberg SO, et al. Fast fluid-attenuated inversion recovery (FLIR) MRI in the assessment of intraaxial brain tumors. J Magn Reson Imaging 1998;8: Tourbah, Deschamps R, Stievenart JL, et al. 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