Findings Regarding an Intracranial Hemorrhage on the Phase Image of a Susceptibility-Weighted Image (SWI), According to the Stage, Location, and Size

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1 pissn eissn imri 2015;19: Findings Regrding n Intrcrnil Hemorrhge on the Phse Imge of Susceptiility-Weighted Imge (SWI), According to the Stge, Loction, nd Size Yoon Jung Lee 1, Song Lee 1, Jinhee Jng 1, Hyun Seok Choi 1, So Lyung Jung 1, Kook-Jin Ahn 1, Bum-soo Kim 1, Kng Hoon Lee 2 1 Deprtment of Rdiology, Seoul St. Mry's Hospitl, College of Medicine, The Ctholic University of Kore, Seoul, Kore 2 Deprtment of Rdiology, St. Pul's Hospitl, College of Medicine, The Ctholic University of Kore, Seoul, Kore Originl Article Received: My 18, 2015 Revised: June 11, 2015 Accepted: June 15, 2015 Correspondence to: Hyun Seok Choi, M.D. Deprtment of Rdiology, Seoul St. Mry's Hospitl, College of Medicine, The Ctholic University of Kore, 222 Bnpo-dero, Seocho-gu, Seoul , Kore. Tel Fx Emil: hschoi@ctholic.c.kr This is n Open Access rticle distriuted under the terms of the Cretive Commons Attriution Non-Commercil License ( y-nc/3.0/) which permits unrestricted non-commercil use, distriution, nd reproduction in ny medium, provided the originl work is properly cited. Copyright 2015 Koren Society of Mgnetic Resonnce in Medicine (KSMRM) Purpose: Susceptiility weighted imging (SWI) is new mgnetic resonnce technique tht cn exploit the mgnetic susceptiility differences of vrious tissues. Intrcrnil hemorrhge (ICH) looks drk looming on the mgnitude imges of SWI. However, the pttern of ICH on phse imges is not well known. The purpose of this study is to chrcterize hemorrhgic lesions on the phse imges of SWI. Mterils nd Methods: We retrospectively enrolled ptients with ICH, who underwent oth SWI nd precontrst CT, etween 2012 nd 2013 (n = 95). An SWI ws tken, using the 3-tesl system. A phse mp ws generted fter postprocessing. Cses with n intrcrnil hemorrhge were reviewed y n experienced neurordiologist nd trinee rdiologist, with 10 yers nd 3 yers of experience, respectively. The types nd stges of the hemorrhges were determined in correltion with the precontrst CT, the T1- nd T2-weighted imges, nd the FLAIR imges. The size of the hemorrhge ws mesured y one- directionl xis on mgnitude imge of SWI. The phse vlues of the ICH were qulittively evluted: hypo-, iso-, nd hyper-intensity. We summrized the imging fetures of the intrcrnil hemorrhge on the phse mp of the SWI. Results: Four types of hemorrhge re oserved: sudurl nd epidurl; surchnoid; prenchyml hemorrhge; nd microleed. The stges of the ICH were clssified into 4 groups: cute (n = 34); erly sucute (n = 11); lte sucute (n = 15); chronic (n = 8); stge-unknown microleeds (n = 27). The cute nd erly sucute hemorrhge showed heterogeneous mixed hyper-, iso-, nd hypo-signl intensity; the lte sucute hemorrhge showed homogeneous hyper-intensity, nd the chronic hemorrhge showed shrunken iso-signl intensity with the hyper-signl rim. All cute surchnoid hemorrhges showed homogeneous hyper-signl intensity. All prenchyml hemorrhges (> 3 mm) showed dipole rtifct on the phse imges; however, microleeds of less thn 3 mm showed no dipole rtifct. Lrger hemtoms showed heterogeneous mixture of hyper-, iso-, nd hypo-signl intensities. Conclusion: The pttern of the phse vlue of the SWI showed difference, ccording to the type, stge, nd size. Keywords: Intrcrnil hemorrhge; Phse mp; Susceptiility weighted imging; Mgnetic resonnce imging 107

2 Intrcrnil Hemorrhge on Phse Imge Yoon Jung Lee, et l. INTRODUCTION The development of n intrcrnil hemorrhge (nd its evolution) is dynmic process, depending on the physiologic nd mgnetic property of the hemogloin. Generlly, five stges of hemorrhge re widely ccepted y the sttus of hemogloin: hypercute (intrcellulr oxyhemogloin); cute (intrcellulr deoxy-hemogloin); erly sucute (intrcellulr met-hemogloin); lte sucute (extrcellulr met-hemogloin); nd chronic (ferritin nd hemosiderin) (1, 2). Differentition etween those stges of hemorrhge could e chieved y the comintion of the T1- nd T2-weighted imges (3). Grdient echo T2* weighted imges (GRE) were previously known to e sensitive, in the detection of intrcrnil hemorrhges. The recently pplied susceptiility-weighted imge (SWI) hs shown etter sensitivity nd specificity thn GRE, for detection of intrcrnil hemorrhges (4). Phse imging from the SWI is lso informtive, in regrd to differentiting the hemorrhge from clcifiction, y mens of the opposite direction of the phse vlue etween them (5-7). We hypothesized tht the findings of n intrcrnil hemorrhge on the phse imges would e different, ccording to the stge, loction, nd size, ecuse the phse vlue is proportionl to the prmgnetic property of the hemorrhge. To the est of our knowledge, findings of n intrcrnil hemorrhge on the phse imges hve not een evluted in ccordnce to its stge, loction, nd size. Therefore, the purpose of this study ws to ssess nd descrie the findings of intrcrnil hemorrhges on phse imges. MATERIALS AND METHODS Ptient Popultion The Institutionl Review Bord pproved this retrospective study, nd wived the ptient consent. Ptients with intrcrnil hemorrhges were serched, using n electronic medicl dtse, etween Mrch 2012 nd Decemer Among these, the numer of ptients who underwent oth n MRI (including SWI) nd computed tomogrphy ws 105. Ptients who hd previous history of hemorrhgic stroke, vsculr mlformtion, ruptured cererl neurysm, nd other cuses of intrcrnil hemorrhge were excluded from the nlysis (n = 5). Ptients with poor imge qulity of phse imges were excluded from the nlysis (n = 5). Finlly 95 ptients, with first onset intrcrnil hemorrhge, were included in this study. Acquisition of MRI nd Genertion of SWI nd Phse Imge Susceptiility-weight imges were tken using 3.0 T MR system (Verio, Siemens Medicl Solutions, Erlngen, Germny). SWI cquisition ws performed with 3-dimensionl grdient echo sequence, with FA = 15 ; TR/TE = 28/20 msec; FOV = mm; mtrix size = ; slice thickness = 2 mm; nd voxel size = mm. After otining oth the mgnitude nd phse imges, post-processing of the mgnitude nd phse imges were performed in n MR console. Briefly, phse imge ws generted fter unwrpping the phse imges y pplying high pss filter. Then, phse msk ws generted, nd multiplied to the fourth power with the mgnitude imge, to generte the SWI. The phse imge ws left-hnded system, where the hemorrhge presented hyper-signl intensity nd the clcifiction presented hypo-signl intensity on the phse imges. The cquisition time for the SWI took less thn 4 minutes nd 30 seconds. Conventionl sequences (T1-weighted imge nd T2-weighted imge) were cquired to clssify the stge of the hemorrhge. Clssifiction of Intrcrnil Hemorrhge Stges of hemorrhge The electronic medicl record ws reviewed y 3-yer trinee resident. The cute stge ws defined s occurring within 3 dys fter the symptom onset of intrcrnil hemorrhge. The erly sucute stge ws defined s occurring etween 4 to 7 dys fter symptom onset. The lte sucute stge ws defined s occurring etween 8 to 21 dys fter symptom onset. The chronic stge ws defined s occurring over 21 dys fter symptom onset. A neurordiologist with 10 yers of experience confirmed the hemorrhge y the drk looming lesion on the T2*- weighted grdient echo, nd correlted the stges of the hemorrhge y their chrcteristic ppernces on T1- nd T2-weighted imges (8). The signl intensity on the phse imges were descried y hyper-, iso-, nd hyposignl intensities, compred to tht of rin prenchym. A pre-contrst CT ws used to confirm whether the lesions on the phse imge were hemorrhges or clcifictions. Clcifiction ws defined y the hyperdense (Hounsfield unit > 140) lesion on the pre-contrst CT. The intervl etween the MRI nd the CT ws within 3 dys. 108

3 Loction of Hemorrhge The neurordiologist nd the trinee rdiologist, with 10 yers nd 3 yers of experience respectively, clssified them into 3 ctegories with consensus: surchnoid hemorrhge; prenchyml hemorrhge; nd sudurl hemorrhge or epidurl hemorrhge. Size of Hemorrhge Detection of the hemorrhge ws performed using the SWI, which is considered sensitive enough to identify tiny hemorrhges (presented s drk looming signl). After reviewing severl slices, ove nd elow the prenchyml hemorrhge, the longest dimeter of hemorrhge ws mesured using xil mgnitude imges. Mgnitude imges were considered most relile for mesuring the size of the hemorrhge, ecuse the voxel size of the mgnitude imge ws smller thn the T1- nd T2- weighted imges, nd less ffected y the susceptiility effect thn the SWI. The trinee rdiologist mesured the longest dimeter y mens of using one-directionl long xis on the PACS (picture rchiving communiction system). RESULTS Stge of Hemorrhge A totl of 95 ptients with intrcrnil hemorrhges were clssified into 4 groups: 34 cses were cute, 11 were erly sucute, 15 were lte sucute, 8 were chronic; in ddition, there were some stge-unknown microleeds (n = 27). All stges of hemorrhges were detected s drk signl intensity, with looming, on the SWI. In the cute Fig. 1. A cse of cute to erly sucute sudurl hemorrhge. The crescent sudurl hemorrhge, long the right cererl convexity, is shown y pre-contrst CT (), T1-weighted imge (), T2-weighted imge (c), nd phse imge (d). The sudurl hemorrhge ppers grdted nd hyperdense on pre-contrst CT (), isointense on T1-weighted imge (), grdted hypointense on T2-weighted imge (c), nd heterogeneously hyper-, iso-, nd hypo-signl intensities on phse imge (d). c d 109

4 Intrcrnil Hemorrhge on Phse Imge Yoon Jung Lee, et l. nd erly sucute stges, the middle of the hemorrhge slices were heterogeneously hyper-, iso-, nd hypo-signl intensities on the phse imges (Fig. 1). This heterogeneity of phse might come from heterogeneous distriution of oxy-, deoxy-, nd met-hemogloins. The upper nd lower slices of the hemorrhge were homogeneously hypersignl intensity; this phenomenon could e explined y the prmgnetic dipole rtifct (9). The lte sucute stge of the hemorrhges ws demonstrted y the homogeneous hyper-intensity on the phse imges, which could e explined y the homogeneously distriuted extrcellulr met-hemogloins (Fig. 2). The chronic stge of the hemorrhges ws depicted y shrunken iso-signl intensity with hyper-signl rim, which could e explined y the resolution of the hemorrhge with the hemosiderin rim. Loction of Hemorrhge 1. Surchnoid hemorrhge (SAH) All cses of SAH were due to the rupture of intrcrnil neurysms (n = 1), or trumtic rin injuries (n = 20). The findings of the SAH were oserved s eing sulcl or cisternl high density on the pre-contrst CT nd s drk signl on the SWI (10). Thin SAH ws expressed y homogeneous hyper-signl intensity on the phse imges (Fig. 3). However, thick portion of the SAH showed mixed hyper- nd hypo-signl intensities, due to n lising rtifct on the phse imges. Fig. 2. A cse of lte sucute sudurl hemorrhge (rrows). The crescent sudurl hemorrhges, long oth nterior cererl convexities, ppers hypodense on the pre-contrst CT (), hyperintense on T1-weighted imge (), hyperintense on T2-weighted imge (c), nd homogeneous iso- to hyperintense on phse imge (d). c d 110

5 Fig. 3. A cse of cute surchnoid hemorrhge (rrows). High density in the right prietl sulci on the pre-contrst CT (), not definitely delineted on T1- nd T2-weighted imges (, c), nd homogeneous hyper-signl intensity on phse imge (d). c d 2. Brin prenchyml hemtom The prenchyml hemtom were due to hypertension (n = 123), contusion (n = 22), or rupture of vsculr mlformtion (n = 1). There were no cses resulting from tumor leeding. Prenchyml hemtoms were demonstrted y three ptterns: heterogeneous hyper-, iso- nd hypo-signl intensity with dipole rtifct, homogeneous hyper-signl intensity with dipole rtifct, nd homogeneous hyper-signl intensity without dipole rtifct (depending on the size of hemtoms). 3. Sudurl hemorrhge (SDH) or epidurl hemorrhge (EDH) Sudurl hemorrhges (SDH) were found in 11 cses, nd epidurl hemorrhges (EDH) were found 2 cses. The signl intensities of the SDH nd EDH on the phse imges were found s eing of similr ppernce on the phse imges. The shpes of the SDH nd EDH hd extr-xil crescent nd iconvex ppernces, with stge-comptile signl intensities on the phse imges. Size of Hemorrhge A totl of 146 prenchyml hemorrhges were divided into 3 groups ccording to their size: those greter thn 5 mm (n = 56), those rnging from 3 mm to 5 mm (n = 36), nd those less thn 3 mm (n = 55). The slice thickness of the SWI ws 2 mm; therefore smller hemorrhges (< 3 mm) - compred to the slice thickness - showed homogeneous hyper-signl intensity (Fig. 4A). Lrger hemtoms showed heterogeneous mixture of hyper-, iso-, nd hypo-signl intensities. The signl intensity in the upper nd lower slices of the hemtom showed hyper-signl intensity, due to the 111

6 Intrcrnil Hemorrhge on Phse Imge Yoon Jung Lee, et l. Fig. 4. Prenchyml hemorrhge, ccording to size, on the phse imge. A 2 mm microleed in the left temporl loe (rrow) showing homogeneous hyperintense dot without dipole rtifct (). A 4 mm microleed in the left temporl loe (rrow), showing homogeneous hypointense dot surrounded y hyperintense rim t the mid-slice of the lesion (). prmgnetic dipole rtifct (11). The middle slices of the hemtoms showed homogeneous hypo-signl intensity (3-5 mm; Fig. 4B) nd heterogeneous mixture of hyper-, iso- nd hypo-signl intensity (> 5 mm). DISCUSSION SWI is very sensitive to lood products, nd cn provide dditionl phse informtion (12). A comintion of T1-, T2-, nd T2*-weighted imges cn e used to differentite etween the stges of hemorrhges. However, descriptions of the vrious intrcrnil hemorrhges on the phse imge hve not een reported previously. To the est of our knowledge, this study ws the first to descrie findings of the phse imge, ccording to the stge, loction, nd size of the intrcrnil hemorrhge. Ech stge shows different susceptiility to sequentil degrdtion of the hemogloin. Extrvsted oxyhemogloluin evolves to deoxy-hemogloin, met-hemogloin, nd hemosiderin in time (8). Theoreticlly, the evolution of hemogloin products results in higher susceptiility, so its signl on the phse imge cn e expected increse sequentilly. However, the inhomogeneous distriution of those hemogloin products mkes heterogeneous mixed hyper-, iso-, nd hypo-signl intensities in the cute nd erly sucute stges. The phse imges, post-processed y recent techniques might hve limittions ecuse the current dipole inversion of hemtoms is imperfect. In the lte sucute stge, homogeneous distriution of extrcellulr met-hemogloin cused more homogeneous high-signl intensities on the phse imges. In the chronic stge, the shrunken prenchym surrounded y hemosiderin ws demonstrted, s we expected. Conventionl MR sequences, such s the T1- nd T2-weighted imges, cn predict signl chnges in the prenchyml hemorrhge consistently. However, the prediction of the signl chnge is inconsistent for the EDH, SDH nd SAH on the conventionl MR sequences. Similr limittions were oserved on the phse imges. Recent studies on the phse imge of trumtic SAH showed heterogeneous lising pttern on the phse imge (10). Our study showed similr pttern on the phse imge, in the cse of thick portion of the SAH. However, most of the thin portion of the SAH showed homogeneous hyper-signl intensity on the phse imge, without lising. Alising cn lso e cused y other resons, such s onetissue interfces, ir-tissue interfces, nd the clcifiction of the tentorium or flx. Creful interprettion should e performed on hemorrhges ner the skull se, flx, tentorium, nd convexities. A dipole rtifct ws found in hemorrhges tht were 3 mm nd lrger thn 3 mm in size. The phenomenon could e understood s n imperfect dipole inversion of prmgnetic susceptiility (13). In our study, ecuse we used left-hnded phse imges, the upper nd lower slices of hemtoms showed hyper-signl intensities. If righthnded system ws used, the opposite hypo-signl intensity would e demonstrted on the phse imges. In contrst, smller hemorrhges (less thn 3 mm) showed reltively homogeneous hyper-signl intensity on phse imges (14). Our study hd severl limittions. First, this study is retrospective, in regrd to the nture of the nlysis. As for the SAH, ll of the cses were in the cute stge. Therefore, the evolution of SAH on the phse imge could not e ssessed on this study; s such, further study should e 112

7 undertken. Second, the dtes of the CT nd MR cquisition were different in most cses. It ws possile to chnge during the trnsition etween cute nd sucute stges, or erly nd lte sucute stges; however, the intervl etween the two modlities ws reltively nrrow (within 3 dys), nd hemtom evolution could only e reltively little during this short period. Third, the dipole inversion ws not performed on the post-processing of the phse imges. An ccurte dipole inversion could provide less lising of susceptiility, nd more quntittive phse informtion. In conclusion, ll hemorrhges showed looming drk signl on the SWI. However, the phse imges showed different ppernces, ccording to the stge, loction, nd size of the hemorrhges. These findings on the phse imges could provide more informtion out the vrious intrcrnil hemorrhges. REFERENCES 1. Prizel PM, Mkkt S, Vn Miert E, Vn Goethem JW, vn den Huwe L, De Schepper AM. Intrcrnil hemorrhge: principles of CT nd MRI interprettion. Eur Rdiol 2001;11: Brdley WG Jr. MR ppernce of hemorrhge in the rin. Rdiology 1993;189: Allkemper T, Tomch B, Schwindt W, et l. Acute nd sucute intrcererl hemorrhges: comprison of MR imging t 1.5 nd 3.0 T--initil experience. Rdiology 2004;232: Nndigm RN, Viswnthn A, Delgdo P, et l. MR imging detection of cererl microleeds: effect of susceptiility-weighted imging, section thickness, nd field strength. AJNR Am J Neurordiol 2009;30: Gupt RK, Ro SB, Jin R, et l. Differentition of clcifiction from chronic hemorrhge with corrected grdient echo phse imging. J Comput Assist Tomogr 2001;25: Hcke EM, Mittl S, Wu Z, Neelvlli J, Cheng YC. Susceptiility-weighted imging: technicl spects nd clinicl pplictions, prt 1. AJNR Am J Neurordiol 2009;30: Mittl S, Wu Z, Neelvlli J, Hcke EM. Susceptiilityweighted imging: technicl spects nd clinicl pplictions, prt 2. AJNR Am J Neurordiol 2009;30: Gomori JM, Grossmn RI. Mechnisms responsile for the MR ppernce nd evolution of intrcrnil hemorrhge. Rdiogrphics 1988;8: Deistung A, Ruscher A, Sedlcik J, Witoszynskyj S, Reichench JR. Informtics in Rdiology: GUIBOLD: grphicl user interfce for imge reconstruction nd dt nlysis in susceptiility-weighted MR imging. Rdiogrphics 2008;28: Wu Z, Li S, Lei J, An D, Hcke EM. Evlution of trumtic surchnoid hemorrhge using susceptiility-weighted imging. AJNR Am J Neurordiol 2010;31: Liu J, Liu T, de Rochefort L, et l. Morphology enled dipole inversion for quntittive susceptiility mpping using structurl consistency etween the mgnitude imge nd the susceptiility mp. Neuroimge 2012;59: Schelhorn J, Grmsch C, Deuschl C, et l. Intrcrnil hemorrhge detection over time using susceptiilityweighted mgnetic resonnce imging. Act Rdiol 2014 [Epu hed of print] 13. Liu T, Xu W, Spincemille P, Avestimehr AS, Wng Y. Accurcy of the morphology enled dipole inversion (MEDI) lgorithm for quntittive susceptiility mpping in MRI. IEEE Trns Med Imging 2012;31: McAuley G, Schrg M, Sipos P, et l. Quntifiction of punctte iron sources using mgnetic resonnce phse. Mgn Reson Med 2010;63: