Lin Bo Zhao,MD
Dae Chul Suh,MD,PhD Dong-Geun Lee,MD Sang Joon Kim,MD, PhD
Jae Kyun Kim,MD Seungbong Han,PhD Deok Hee Lee,MD,PhD Jong Sung Kim,MD, PhD
Correspondence to
Dr.Suh:
dcsuh@amc.oul.kr Association of pial venous reflux with hemorrhage or edema in dural arteriovenous fistula
ABSTRACT
Objective:We investigated whether pial venous reflux(PVR)is associated with hemorrhage or edema in dural arteriovenous fistula(DAVF).
Methods:We evaluated the association of hemorrhage or edema with the occurrence of PVR or cortical venous reflux(CVR)in222patients with DAVF.We determined whether angiographic findings of PVR or
CVR(more than Borden I or Cognard IIa)were associated with symptoms, lesion location,or brain lesion(hemorrhage or edema).We evaluated the lesion progression or the follow-up results after obliteration of the DAVF.
Results:Hemorrhage or edema developed in18%(40/222)of the patients with DAVF and55% (40/72)of the patients with PVR.There were2patterns of PVR associated with hemorrhage or edema:(1)PVR in any particular CVR territory(75%),and(2)direct PVR not via CVR(25%).The prence of brain lesion incread the odds of prence of PVR by4.09times compared to the group without brain lesion(95%confidence interval51.570–11.394,p50.004).Brain edema caud by PVR was reversible after obliteration of the fistula and may have progresd to hem-orrhage without proper patient management performed within veral weeks after the initial prentation.
Conclusions:Our results show that PVR is more cloly associated with the hemorrhage or edema than CVR in patients with DAVF.PVR can occur not only as a part of CVR but also directly in cer-tain types of DAVF.Neurology®2014;82:1897–1904
GLOSSARY
CVR5cortical venous reflux;DAVF5dural arteriovenous fistula;GK5gamma knife;mRS5modified Rank
菱形脸短发in Scale;PVR5 pial venous reflux;SAH5subarachnoid hemorrhage.
Current classifications of dural arteriovenous fistula(DAVF)are focud primarily on the pres-ence of cortical venous reflux(CVR)related to cerebral venous hypertension leading to cerebral infarction or hemorrhage.1–3CVR is known to be related to the so-called aggressive type of DAVF becau29%to46%of patients with CVR may develop cerebral hemorrhage.4–6How-ever,it has not been precily determined why hemorrhage or edema in certain brain areas is related to CVR.
Pial venous reflux(PVR),a part of CVR,has not been clearly identified or differentiated from CVR.7However,there have been only a few descriptions of the relationship of PVR to CVR and the location of their anatomical junction.
The aim of this study was to investigate the relationship of PVR vs CVR to hemorrhage or edema.To achieve this,we assd rial angiographic and cross-ctional imaging findings of CVR and PVR associated with hemorrhage or edema.We then prent a concept regarding how PVR occurring in patients with CVR is related to hemorrhage or edema.
METHODS We reviewed prospectively collected records of222concutive patients diagnod with DAVF at a single medical insti-tution(Asan Medical Center,Seoul,Korea)between July1998and Octob
er2012.We analyzed the patients’angiographic findings and
From the Department of Radiology and Rearch Institute of Radiology(L.B.Z.,D.C.S.,D.-G.L.,S.J.K.,D.H.L.)and Department of Neurology (J.S.K.),University of Ulsan,College of Medicine,and Department of Epidemiology and Biostatistics(S.H.),Asan Medical Center,Seoul,Korea; Department of Radiology(L.B.Z.),First Affiliated Hospital of Nanjing Medical University,Nanjing,China;and Department of Radiology(J.K.K.), Chung-Ang University,College of Medicine,Seoul,Korea.归来的爱
Go for full disclosures.Funding information and disclosures deemed relevant by the authors,if any,are provided at the end of the article.
©2014American Academy of Neurology1897
medical records to asss the patient demographics,the prence of brain lesions(hemorrhage or edema),shunt localization,and the prence of CVR or PVR.We excluded pial-type brain arteriovenous malformations with a dural supply.Selective angiography of the internal carotid artery,external carotid artery,and vertebral arteries was obtained using high-resolution, biplane,digital subtraction angiography(AXIOM Artis zee biplane angiography system;Siemens AG Medical Solution
s, Erlangen,Germany).
The clinical symptoms were parated , benign and aggressive.8The benign group consisted of an inci-dental diagnosis,nonspecific headaches,cranial nerve deficits, chemosis/proptosis,bruit or pulsatile tinnitus,mass lesions,and cardiac insufficiency.The aggressive group included izures, intracranial hemorrhage,motor or nsory deficits,visual field defects,aphasia,global neurologic deficits(dementia,delayed psychomotor development,macrocrania),and other nonhemor-rhagic neurologic deficits such as incontinence.We did not mea-sure the venous pressure either directly or indirectly.
Standard protocol approvals,registrations,and patient connts.The institutional review board approved the study, and written informed connt was obtained from each patient.
MRI/CT findings.Patients who prented with hemorrhage or edema en on MRI/CT obtained before treatment were analyzed and classified into3subgroups:(1)hemorrhage,defined as paren-chymal or subarachnoid hemorrhage(SAH)with little or no edema;(2)edema,defined as parenchymal edema with no evi-dence of hemorrhage;or(3)edema combined with hemorrhage, defined as both edema and hemorrhage,with the edema being disproportionate to the amount that would be expecte
d surround-ing a parenchymal hemorrhage.We correlated symptoms,lesion locations,and angiographic types.The patients who prented with acute neurologic deficits underwent an imaging study accord-ing to our acute stroke protocol,and which therefore included fluid-attenuated inversion recovery imaging(n528),diffusion-weighted imaging(n524),apparent diffusion coefficient imaging (n520),and perfusion imaging(n55).One patient who prented with a brainstem sign showed MRI findings mimicking brainstem tumor and thus underwent magnetic resonance spectroscopy.Becau the application of MRI/CT studies varied according to the attending physician or patient’s prenting symptom,analysis of imaging studies was bad on the neuroradiologist’s report and was additionally reviewed by connsus of2experienced neuroradiologists(S.J.K.and D.C.S.). Angiographic typing.Angiographically,benign and aggressive lesions were defined according to the abnce or prence of CVR9and were also grouped using the classification systems of Borden2and Cognard.1Borden I(sinus drainage only),Cognard I (antegrade sinus drainage without CVR),and Cognard IIa(retro-grade sinus drainage without CVR)were considered as“benign”DAVFs,whereas all of the higher grades that have cortical and spinal drainage with or without sinus drainage were grouped as“aggressive”DAVFs.10,11The main locations of DAVFs were categorized as the cavernous sinus,the transver-sigmoid sinus,the superior sagittal sinus,the ethmoidal roof,and the petrous area.We also identified a new type of DAVF lesion in the parietotemporal convexity and defined it as parietotemporal convexity DAVF.
CVR vs PVR.The prence of cortical and pial venous drainage was determined.Veins were defined as“cortical”when they courd along the cortical surface draining into the venous sinus and as“pial”when the fine and tortuous veins were within the brain or on the brain surface,as en on cerebral angiography (figure1E)and/or MRI.Prence of PVR was also decided by comparison with cortical veins in the venous pha of the ipsilat-eral internal carotid arteriogram(figure2,G and J).Compared with cortical veins,which are regarded as the main leptomeningeal veins draining into sinus,the fine pial veins or the intracortical veins beneath the pial membrane were regarded as having a corkscrew-like appearance or intraparenchymal cour,12which cannot be en on a routine normal angiogram(figures1E,2I,and3J).We did not apply any size criteria for the differentiation becau the pial vein is much smaller and more peripherally located than the cortical vein. In patients who underwent rial imaging studies,their prenting symptom pattern was compared with the development of a brain lesion according to the time interval.
Follow-up.Follow-up data for the222study patients were col-lected from the time of their admission until the end of2012.A complete history was obtained from each patient,and a neurologic examination was performed by independent neurologists who were not involved in the interventional procedure.If a patient was not followed up or the patient’s status was not exactly mentioned in an out
patient clinic,an experienced nur telephoned the patients to evaluate the possibility of any clinically relevant event.Functional outcome was assd with the modified Rankin Scale(mRS).13 Median clinical follow-up of all patients was15months (range1–178months),and final outcome was evaluated using the mRS,as shown in the table.The40patients with hemorrhage or edema were followed for a median of12months(range1–155 months).Treatment included embolization in23,gamma knife (GK)irradiation in6,surgical rection in5,and no treatment in 6patients.14Good(mRS score#2)vs poor(mRS score.2) outcome was compared for each treatment modality. Statistical methods.Cross-tabulations using patient x,age, angio-type(benign vs aggressive),clinical symptoms group (benign vs aggressive),lesion location,brain lesion(hemorrhage or edema),and the prence of CVR or PVR were performed. Statistical significance was calculated for each group using the Fisher exact test and t test for categorical variables and continuous variables,respectively.We conducted univariate and multivariable analys using variables that were significant in frequency or mean comparison between the prence and abnce of PVR compared with the prence of CVR without PVR.Becau lesion location was the cavernous sinus in62%of patients and the frequency of some category levels for the other lesion locations was small,we regrouped lesion location into a smaller number of categories(the cavernous sinus vs others).15Similarly,we regrouped135patients with the prence of CVR into prence or abnce groups of the brain lesion.The univariate and multivariabl
e logistic regression model propod by Firth was fitted for the binary outcome variable.This method can handle the paration problem occurring when some categorical levels have zero counts of brain lesion as in the patients with CVR but without PVR.16All statistical analys were performed using SPSS18software(SPSS Inc., Chicago,IL)and R software(R Foundation for Statistical Computing,Vienna,Austria;).The R package “logistf”was ud to fit the bias-reduced logistic regression model.17 Significance was determined at p,0.05.
We retrospectively computed the statistical power under some assumptions.Group sample sizes of42in group1with brain lesion and84in group2without brain lesion achieve90%power to detect a difference between the group proportions of0.3.The pro-portion in group1is assumed to be0.3under the null hypothesis and0.6under the alternative hypothesis.The proportion in group 2is0.3.The test statistic ud was the2-sided z test with pooled variance.The significance level of the test was targeted at0.05.
1898Neurology82May27,2014
RESULTS Baline characteristics.The baline clini-
cal and angiographic features of the 222patients with
intracranial DAVF are summarized in the table.
There were 134women (60%)and 88men (40%)
with a mean age at admission of 57years (range 14–
渡字组词
85years).The most common DAVF location was the
cavernous sinus region (137patients [62%])followed
by the transver and sigmoid sinus regions (38pa-
tients [17%]).Major prenting symptoms or signs in
patients who prented with hemorrhage or edema
were altered consciousness (n 511),orbital/ocular
symptoms related to the brain/brainstem (n 55),
neurologic deficit (n 511),izure (n 56),vere
headache (n 56),and dizziness (n 51).Seizure
developed in patients with edema in the parietal lobe
历史文学
due to the DAVF of the parietotemporal convexity
(n 55)or superior sagittal sinus (n 51)(figure 2).MRI/CT findings.Forty patients prented with hem-
orrhage or edema,as en on MRI/CT.Twenty-nine
patients revealed hemorrhage associated with (n 523)or
without (n 56)surrounding edema (figure 1).Eleven
patients only had edema without evidence of hemorrhage
(figure 2).Among the 29patients with hemorrhage,27
prented with parenchymal hemorrhage,one prented
with intracerebral hemorrhage followed by massive SAH,and one prented with massive SAH with
什么东西越洗越脏acute hydrocephalus.The location of the hemorrhage was lobar (n 518),the cerebellar hemisphere (n 56),and the brainstem (n 54).One patient who prented with a brainstem sign showed MRI findings mimicking brainstem tumor,but magnetic resonance spectroscopy did not reveal any evidence of tumor or ischemia (figure 3).CVR vs PVR.The distribution of CVR and PVR in
222patients is prented in the table.There was no CVR in 39%,CVR only in 28%,CVR and PVR in 28%,and PVR only in 5%.Prence of PVR in 72patients (32%)was associated with hemorrhage or edema (p ,0.001).Among 40patients (18%)who developed hemorrhage or edema,30patients (75%)revealed the prence of CVR and PVR (figure 1).Ten patients (25%)revealed direct filling of PVR not via CVR (figure 2).Univariate analysis revealed that the prence of brain lesion (hemorrhage or edema)incread the odds of the prence of PVR by 5.68times compared with the group without brain lesion (95%confidence interval 52.571–13.369,p ,0.001).Compared with the cavernous sinus location,other locations incread the odds of prence of PVR by 2.80
times.
Focal cerebral edema with development of subquent hemorrhage in a 66-year-old woman who prented with neurologic
deficit.A magnetic resonance fluid-attenuated inversion recovery image (A)shows localized high signal intensity in the right
parietal subcortical area.(B)CT imaging obtained 10days later showed focal hemorrhage surrounded by edema in the same
area of the right parietal lobe.Anteroposterior (C)and lateral (D)views of the right external carotid arteriogram show a dural
arteriovenous fistula in the superior sagittal sinus (SSS)supplied by the middle meningeal and superficial temporal arteries.
There is occlusion of the SSS (white arrows in D and E).Note the diffu corkscrew-like tortuous,fine pial venous engorge-
ment (black arrows)in the late venous pha (E).Her neurologic deficit remained after obliteration of the fistula by intrao-
perative coil embolization.
Neurology 82May 27,20141899
Moreover,aggressive symptoms incread the odds of
prence of PVR by 3.23times compared with the
benign symptom group.In the multivariable analysis,
after adjusting for location and aggressive symptoms,
prence of brain lesion was still significant and
incread the odds of prence of PVR by 4.09times
compared with the group without brain lesion (95%
confidence interval 51.570–11.394,p 50.004).
Follow-up results.During median 15months of
follow-up,there was no difference in good vs poor
outcome,likely becau the patients with aggressive
angio-type underwent active treatment while the
others did not (table).During the follow-up period,
there were 3patients who developed hemorrhage
(n 52)in patients with PVR and hydrocephalus
(n 51)in a patient with CVR.
A successful treatment outcome (mRS score #2)
was obtained in 33of the 40patients:20by emboli-
zation,5by GK irradiation,4after surgery,and 4who
received no treatment.18There was a poor treatment
outcome (mRS score .2,n 57)in 3patients who
underwent embolization,one who had surgery,one
after GK irradiation,and in 2patients with no treat-
ment.Of 29patients who prented with hemorrhage,
26were treated using endovascular techniques (n 5
21,transarterial or transvenous or both),DAVF-rection surgery (n 53),or by GK irradiation (n 52)as the first treatment option.Five patients under-went combined therapy becau of incomplete removal of the fistula using GK treatment (n 51)or surgery (n 51)followed by embolization or embolization fol-lowed by surgery (n 52)or GK treatment (n 51).The patients who had prented with hemorrhage showed complete resolution of the hemorrhage on follow-up imaging,and no patient revealed recurrent hemorrhage during the follow-up period.Of the 11patients who prented with brain edema only,8underwent endovascular treatment and 3were lost to follow-up after either GK treatment (n 52)or no treatment (n 51).The edema resolved completely in 7of the patients,as en on MRIs obtained 2months after treatment (figures 2and 3);edema decread in one patient after a follow-up period of 1month.Progression of brain lesions.Eight patients developed brain lesions during the follow-up period.Brain edema (n 52,both 3months after their initial diagnosis)or hemorrhage (n 52,1and 8months after the initial diagnosis)appeared after initial MRI studies were normal.In the patients who
prented
Localized cerebral edema in a 62-year-old man who prented with right-side myoclonus and tonic izure.A gradient echo image obtained at the time of the izure (A)shows a focal edema and dark signal along the left frontoparietal cortex.MRI obtained 3months later shows aggravated edema on T2-weighted image (B)and on T1-weighted image (C).Gadolinium-enhanced image shows slight enh
ancement along the cortical margin (D).T2-weighted image obtained 4years after embolization (E)shows normalized brain parenchyma without any other neurologic deficit.Note only a faint iron deposition along the cortical margin.Anteroposterior (F)and lateral (G)views of the external carotid angiogram show the superficial temporal artery supplying a dural arteriovenous fis-tula over the left parietal convexity via the emissary artery (thick,short arrows)into the pial veins (thick,long arrows).Note collateral filling of a remote pial vein (thin,long arrow in G –K)via the intracortical veins (thin,short arrows in G –K).Selective anteroposterior (H)and lateral (I)angiograms obtained at the emissary artery show pial venous reflux filling to the intracortical veins (thin,short arrows in G –K)as well as intraparenchymal collateral to the other pial vein (thin,long arrows in G –K).The venous pha of the internal carotid arteriogram (J),in contrast to pial venous reflux,shows no visible abnormality in the cortical venous drainage.Schematic drawing (K)shows a shunt filling the pial vein (thick,long arrow)and the other pial vein filling (thin,long arrow)via the intraparenchymal veins (thin,short arrows).Note cortical veins in the subarachnoid space (pink-colored space).The reason the fistular shunt flow remains in the pial venous system is suggested by thrombod disconnection (asterisk)of pial-cortical venous drainage.
1900Neurology 82May 27,2014
with brain edema,there was aggravation of the edema
(n 52,1and 3months after initial MRI)(figure 2),
development of hemorrhage (n 51,10days after
initial MRI)(figure 1),or even improvement with
some residual encephalomalacia (n 51,1.5years
after initial MRI).The locations of the lesions were
the parietotemporal convexity (n 54),cavernous sinus
(n 52),superior sagittal sinus (n 51),and transver-
sigmoid sinus (n 51).
DISCUSSION Our study suggests that PVR is more
cloly related to hemorrhage or edema.PVR was
associated with hemorrhage or edema in 75%of pa-
tients and was related to a certain brain area,whereas
CVR occurred in a wide vascular territory.Our study
also revealed that PVR was found without filling of建筑消防设施检测
the cortical vein in a certain type of DAVF in 25%
of patients with hemorrhage or edema.Therefore,
巨蟹座男生性格prence of PVR should be identified in addition to
the CVR,which is currently known as a risk factor
for hemorrhage in DAVF.19–21In addition,DAVF
diagnosis needs to be considered when there is
corkscrew-like pial venous engorgement in patients
who reveal brain lesion associated with izure or
neurologic deficit.In contrast to arterial ischemic infarction,many parenchymal abnormalities condary to venous con-gestion are reversible.22If venous hypertension can be relieved before cell death or intracranial hemor-rhage,the parenchymal changes may partially or com-pletely resolve.However,if venous pressure continues to increa,with a conquent reduction in arterial perfusion pressure,cell death may ensue.Our study revealed that edema after embolization was progres-sively completely resolved,although the edema re-mained during the initial short-term follow-up period.Three levels of cortical veins have been ,the main leptomeningeal veins,the fine pial net-work,and the intracortical veins.12The main lepto-meningeal veins are located in the pia matter on the surface of the cortex.Pial veins form a den superfi-cial network 23and they have been found to pass over sulci without entering them.24If the DAVF hemor-rhage is caud by rupture of the main leptomenin-geal veins,it should prent more frequently with SAH than with hemorrhage.25This anatomical aspect also demonstrates that it is the intracortical veins or pial veins rather than the main leptomeningeal veins that rupture condary to venous hypertension in pa-tients with cerebral DAVF.20The diameters of
the
A 49-year-old man prented with diplopia,dizziness,and mild dysarthria.A T2-weighted image (A)shows high signal intensities in the left cerebellar pedun-cle and pons.There are no definite signal changes on diffusion-weighted imaging (B)and slightly incread signal intensity on apparent diffusion coefficient image (C).Susceptibility-weighted imaging (D)shows the dilated petrosal vein in t
《中国古代寓言》he left cerebellopontine angle (long,white arrow)and intracortical venous engorgement (short,white arrow).A perfusion imaging study shows incread mean transit time (E),decread cerebral blood flow (F),and decread cere-bral blood volume (G)at the areas of round cursors on the high signal intensities on panel A.Perfusion curve (H)shows decread perfusion status in the brain edema area (red line)compared with the contralateral normal side (blue line).Single-voxel spectroscopy (I)obtained at the left middle cerebellar peduncle with marked gadolinium enhancement shows decread choline (Cho)and creatine peak and relatively prerved N -acetyl aspartate (NAA)peak with decread Cho/NAA ratio suggesting a nontumorous condition.Preembolization (J)and postembolization (K)external carotid angiograms show disappear-ance of a fistular shunt and the engorged petrosal vein (long arrow in J).Note fine corkscrew-like pial veins (short arrows).Fluid-attenuated inversion recovery image obtained 8months after embolization (L)shows normalized brain parenchyma without any other neurologic deficit.
Neurology 82May 27,20141901
