j neurosurgery - a proposed grading system for arte rio venous malformations

8
J Neurosurg 65:476-483, 1986 A proposed grading system for arteriovenous malformations ROBERT F. SPETZLER, M.D., AND NEIL A. MARTIN, M.D. Divisio n of Neurologi cal Surgery, Barrow Neurolo gical In stitute, Phoenix , Ariz ona v- An important factor in making a recommendation for treatment of a patient with arteriovenous malfor- mation (AVM) is to estimate the risk of surgery for that patient. A simple, broadly applicable gradi ng system that is designed to predict the risk of morbidity and mortality attending the operative treatment of specific AVM 's is proposed . The lesion is gr aded on the basis of size, pattern of venous drainage, and neurological eloqu ence of adja cent brain. All AVM's fall into one of six grades. Grade I m alform ations are small, superficial, and located in non-eloquent cortex; Grade V lesions are large, deep, and situated in neurologically critical areas; and Grade VI lesions are essentially inoperable AVM's. Retrospectiv e application of this grading scheme to a series of surgically excised AVM's has demonstrated its correlation with the incid ence of postoperative neurological complications. Th e application o f a standardized grading scheme will enable a comparison of results between various clinical series and between different treatment techniques, an d will assist in the process of m anage ment decisi on-maki ng. KEY WORDS 9 arteriovenous malformation 9 grading system 9 surgical resection prognosis T HE surgical treatment of arteriovenous mal- formations (AVM's) of the brain is primarily intended to eliminate the continued risk of disastrous intracranial hemorrhage. The decision to recommend surgery rests on an objective comparison of the long-term risks presented by an untreated AVM, with the more immediate risks of operative treatment. Clearly, the individual patient with an AVM is bene- fit ed only if his operation is accomplished without mor- tality or disabling morbidity. As there is now infor- mation on the long-term risks or natural history of untreated AVM's, educated surgical decision-making requires an objective method -- a grading system -- for predicting the risks of operation in individual cases of AVM's. An ideal grading system would define, for each spe- cific AVM, the degree of difficulty involved in safely removing the malformation. Such a grading system should provide a reasonably accurate estimation of operative morbidity and mortality, and be simple yet comprehensive enough to be readily applied to all cere- bral AVM's. Previously proposed grading schemes, which have been based only on AVM size or on the number and distribution of feeding arteries, are simple enoug h to be easily applicable. 8 These fail, however, to consider such impo rtant variables as anatomic location, degree of vascular steal, eloquence of adjacent brain, and pattern of venous drainage. Other systems are so complicated that they are difficult to be applied easily and rapidly.ll In order to correct these shortcomings a simple system that weighs the important features of an individual AVM, and thus grades the lesion according to its degree of surgical difficulty, is proposed. Description of Grading System Graded Variables The major factors important in determining the dif- ficulty of resecting an AVM include: size, number of feeding arteries, amount of flow through the lesion, degree of steal from surrounding normal brain, loca- tion, surgical accessibility, eloquence of adjacent brain, and pattern of venous drainage. A grading system based on all of the above variables would be too cumbersome for practical use. However, experience with the man- agement of AVM's has established that many of these factors are interrelated, allowing us to simplify the grading process. By reducing the graded variables to three generalized features of AVM 's, the scheme can be simplified without ignoring critical factors. The three variables considered are: 1) size of the AVM; 2) pattern of venous drainage; and 3) neurological eloquence of the brain regions adjacent to the AVM. 4 7 6 J. Neurosurg. / Volume 65/October, 1986

Upload: ingnes

Post on 09-Apr-2018

233 views

Category:

Documents


1 download

TRANSCRIPT

Page 1: J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

8/8/2019 J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

http://slidepdf.com/reader/full/j-neurosurgery-a-proposed-grading-system-for-arte-rio-venous-malformations 1/8

J Neurosurg 65:476-483, 1986

A proposed grading system for arteriovenousmalformations

ROBERT F. SPETZLER, M .D., AND NEIL A. MARTIN, M.D .

Division of Neurological Surgery, Barrow Neurological Institute, Phoenix, Arizona

v- An impo rtant factor in making a recommendation for treatment o f a patient with arteriovenous malfor-ma tion (AVM ) is to estimate the risk of surgery for that patient. A simple, broa dly applicable grading systemthat is designed to predict the risk o f m orbidity and m ortality attending the operative treatment of specificAVM 's is proposed . The lesion is graded on th e basis of size, pattern o f venous drainage, and neurologicaleloqu ence of adja cent brain. All AVM's fall into o ne of six grades. Grade I m alform ations are small, superficial,

and located in non-eloquent cortex; Grade V lesions are large, deep, and situated in neurologically criticalareas; and Grade VI lesions are essentially inoperable AVM's.

Retrospectiv e application of this grading scheme to a series of surgically excised A VM 's has dem onstratedits correla tion with the incid ence of postoperative neurological complications. Th e application o f a standardizedgrading scheme will enable a comparison of results between various clinical series and between differenttreat me nt technique s, an d will assist in the process of m anage men t decision-making.

KEY WORDS 9 arteriovenou s malforma tion 9 grading system 9 surgical resectionprognos is

THE surg ica l t r ea tment of a r te r iovenous ma l-

f o r ma t io n s ( A V M' s ) o f t h e b r a in i s p r ima r i l yin t e n d e d t o e l imin a t e t h e c o n t i n u e d r i sk o f

d isas t rous in t rac ran ia l hemor rhage . The dec is ion tor e c o mme n d su r g e r y r e s t s o n a n o b j e c t i v e c o mp a r i so no f t h e l o n g - t e r m r isk s p r e se n t e d b y a n u n t r e a t e d A V M,w i th t h e m o r e im me d i a t e r i sks o f o p e r a t i v e t re a tme n t .C lea r ly , the ind iv idua l pa t ien t wi th an AVM is bene -f i te d o n ly i f h i s o p e r a t i o n i s a c c o mp l i sh e d w i th o u t mo r -ta l i ty or d isab l ing morbid i ty . As the re i s now infor -ma t io n o n t h e l o n g - t e r m r i sk s o r n a tu r a l h i s t o r y o funt rea ted AVM's , educa ted surg ica l dec is ion-makingr e q u i r e s a n o b j e c t i v e me th o d - - a g r a d in g sy s t e m - -

for p red ic ting the r i sks of ope ra t i on in ind iv idua l caseso f A V M ' s .

An idea l g rad ing sys tem would de f ine , fo r each spe -c i f ic AVM, the degree of d i f f icu l ty involved in sa fe lyr e mo v in g t h e ma l f o r ma t io n . S u c h a g r a d in g sy s t e msh o u ld p r o v id e a r e a so n a b ly a c c u r a t e e s t ima t io n o fo p e r a t i v e mo r b id i t y a n d mo r t a l i t y , a n d b e s imp le y e tc o mp r e h e n s iv e e n o u g h t o b e r e a d i l y a p p l ie d t o a l l c er e -bra l AVM's . P rev ious ly proposed grad ing schemes ,w h ic h h a v e b e e n b a se d o n ly o n A V M s i z e o r o n t h enumber and d is t r ibu t ion of f eed ing a r te r ie s , a re s impleenoug h to b e eas ily appl icab le . 8 These fai l, however , toc o n s id e r su ch imp o r t a n t v a r i ab l e s a s a n a to mic l o c a t i o n ,

degree of vascu la r s tea l , e loquence of ad jacent b ra in ,a n d p a t t e r n o f v e n o u s d r a in a g e . O th e r sy s t e ms a r e socompl ica ted tha t they a re d i f f icu l t to be appl ied eas i lyand rap id ly . l l In orde r to cor rec t these shor tcomings as imple sys tem tha t we ighs the impor tan t f ea tures of anind iv idua l AVM, and thus grades the le s ion accord ingto i t s degree of surg ica l d i f f icu lty , is p ropo sed .

Descript ion of Grading System

Graded Variables

T h e ma jo r f a c to r s imp o r t a n t i n d e t e r min in g t h e d i f -f icu l ty of r e sec t ing an AVM inc lude : s ize , number offeed ing a r te r ie s , amount of f low through the le s ion ,

degree of s tea l f rom sur rounding normal bra in , loca -t ion , surg ical accessib i li ty , e loq uence of ad jacent b ra in ,and pa t te rn of venous dra inage . A grad ing sys tem basedo n a l l o f t h e a b o v e v a ri a b le s w o u ld b e t o o c u mb e r so m efor prac t ica l use . However , expe r ience wi th the man-a g e me n t o f A V M' s h a s e s t a b l i sh e d t h a t ma n y o f t h e sefac tor s a re in te r re la ted , a l lowing us to s impl i fy the

grad ing process . By reduc ing the graded va r iab les tothree gene ra l ized fea tures of AVM 's , the schem e can bes impl i f ied wi thout ignor ing c r i t ica l f ac tor s . The th reeva r iab les cons ide red a re : 1 ) s ize of the A VM ; 2) pa t te rnof venous dra inage ; and 3) neuro logica l e loquence ofthe bra in r eg ions ad jacent to the AVM.

476 J. Neurosurg. / Volume 65/October, 1986

Page 2: J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

8/8/2019 J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

http://slidepdf.com/reader/full/j-neurosurgery-a-proposed-grading-system-for-arte-rio-venous-malformations 2/8

Grading system for arteriovenous malformations

Size of the A VM. The s ize of the AVM is de te r -min e d b y me a su r in g o n a n g io g r a ms t h e l ar g es t d i a me te ro f t h e n id u s o f t h e ma l f o r ma t io n . W h e n ma g n i f i e dangiographic v iews a re cons ide red , a cor rec t ion for themagnif ica t ion fac tor i s r equi red . The s ize of the AVMis d e t e r min e d t o b e sma l l ( < 3 c m) , me d iu m ( 3 t o 6cm) , o r la rge (> 6 cm) , and the AVM is scored appro-pr ia te ly.

T h e s iz e o f th e m a l f o r ma t io n i s re sp o n sib l e f o r mu c ho f t h e t e c h n i c a l di f f ic u l t y i n r e mo v in g A V M ' s . T h el a rg e r a n A V M, t h e l a r ge r t h e a m o u n t o f n o r ma l a d j a -cen t neura l t i ssue tha t i s exposed to in jury dur ingmic rosurg ica l r e sec t ion of the n idus . La rge AVM'sma n d a t e l o n g e r o p e r a ti n g t ime , t h e r e b y i n c r ea s in g t h er i sk of anes thes ia - re la ted compl ica t ions . Fur the rmore ,the c r i te r ion of s ize encompasses seve ra l o f the o the rimpor tan t f ac tor s tha t de te rmine the degree of surg ica ld i f f icu l ty . In gene ra l the s ize of an AVM de te rmines ,or i s c lose ly r e la ted to , the n um be r o f f eed ing a rte r ies ,

the am ou nt of f low, and the degree of s tea l.Pattern of Venous Drainage. T h e c o u r se o f t h e

d r a in in g v e in s is d e t e r min e d f r o m th e a n g io g ra m. T h evenou s pa t te rn i s cons ide re d supe r f ic ia l i f a ll the dra in-age f rom the AVM is th rough the cor t ica l venous sys-t e m. T h e v e n o u s p a t t e r n i s c o n s id e r e d d e e p i f a n y o ra l l o f the dra inage i s th rough deep ve ins ( such asin te rna l ce rebra l ve ins , basa l ve ins , o r p recent ra l ce re -be l la r vein) . In the pos te r ior fossa , on ly ce rebe l la r hemi-spher ic ve ins tha t d ra in d i rec t ly in to the s t r a igh t s inusor t r ansve rse s inus a re co ns ide red to be supe r f icia l ve ins .

C lea r ly , the pa t te rn of venous dra inage i s c lose lyre la ted to the surg ica l access ib i l i ty of an AVM. Deep

v e n o u s d r a in a g e , n o ma t t e r h o w sma ll , f u r t h e r c o mp l i -ca te s AVM exc is ion . Of ten the vas t ma jor i ty of anA V M w i l l h a v e b e e n s e p a r a t e d f r o m th e su r r o u n d in gbra in when the sma l l a r te r ia l ized subependymal ve inso f t h e d e e p c o mp o n e n t a r e e n c o u n te r e d . T h e se v e in sa re f r iab le , r e s i s t b ipo la r coagula t ion , and have thed a n g e r o u s p r o p e n s i t y t o r e t r a c t a n d b l e e d i n to t h ep a r e n c h y ma o r v e n t r ic l e w h e n d i s r u pt e d .

Eloquence of Adjacent Brain. E lo q u e n t b r a in r e -g ions a re de f ined a s those tha t speak to r ead i ly iden t i -f iab le neuro logica l func t ion and , i f in jured , r e su l t in ad isab l ing neuro logica l de f ic i t . For the purpose of th isgrad ing scheme , the fo l lowing a re cons ide red e loquentareas (Fig. 1) : the sensorimotor , language, and visualc o r t ex ; t h e h y p o th a l a mu s a n d t h a l a mu s ; t h e i n t e r n a lcapsu le ; the bra in s tem; the ce rebe l la r pedunc les ; andthe deep ce rebe l la r nuc le i . Areas wi th mu ch mo re subt leneuro logica l func t ion , o r a reas in which in jury does no tcause pe rmanent d isab l ing de f ic i t ( such as the an te r iorpor t ion of the f ron ta l o r tempora l lobes , o r the ce rebe l -la r cor tex) a re cons ide red non-e loquent . To prese rves impl ic i ty , i t i s a ssumed tha t e loquent cor t ica l r eg ionso c c u p y t h e i r n o r ma l a n a to mic l o c a t io n . F o r t h e p u r p o seof grad ing , Wada te s t ing or e lec t rophys io log ica l map-p ing techniques des igned to prec ise ly loca l ize e loquentcor tex a re no t r equi red . Da ta f rom these techniques , i f

FIG. 1. The anato mic areas consid ered neurologically el-oquent for the purposes of the grading system are indicated.The deep eloquent areas (hypothalamus, thalamus, brainstem, and cerebellar peduncles) are highlighted in the uppe rimage. The eloquent regions of the cerebral cortex (sensori-motor areas, language areas, and primary visual area) areidentified on the lower image.

ava ilab le , can eas i ly be used for g rad ing bra in e loquen cein t h i s s c h e me . T h e r e mo v a l o f A V M' s a d j a c e n t t oe loquent a reas ca r r ie s a much grea te r r i sk of d isab l ingneuro logica l morb id i ty than does exc is ion of these le -sions f rom less cr i t ica l regions. The brain that is adja-

cen t to the AVM is l iab le to exper ience dama ge du r ingsurge ry f rom AVM dissec t ion and re t r ac t ion , and a f te rsu r ge r y f r o m p o s to p e r a t i v e h e mo r r h a g e o r e d e ma .

Determination of Grade

In orde r to ass ign an AV M grade , the s ize , the veno usdra inage , and the e loquence of the ad jacent b ra in a red e t e r min e d f r o m a n g io g r a ph y , c o mp u te r i z e d t o mo g r a -p h y ( C T ) , a n d /o r ma g n e t i c r e so n a n c e ima g in g ( MR I ) .Pa r t icu la r ly wi th deep supra ten tor ia l o r pos te r ior fossama l f o r ma t io n s , C T a n d MR I a r e h e lp f u l i n d e l in e a t in gth e t o p o gr a p h i c al r el a t i o n ship o f t h e A V M to e lo q u e n treg ions . A numer ica l va lue i s a ss igned for each of the

J. Neurosurg. / Volume 65/October, 1986 477

Page 3: J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

8/8/2019 J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

http://slidepdf.com/reader/full/j-neurosurgery-a-proposed-grading-system-for-arte-rio-venous-malformations 3/8

R. F. Spetzler and N. A. Martin

FIG. 2. Carotid angiograms, lateral view (left) and antero-posterior view (right), showing a Grad e I ar teriovenous mal-formation (AVM). This AVM is less than 3 cm in diameter(small: 1 point) , located i n the a nterior fron tal lobe (non-eloquent: 0 points) , and drains through cortical veins (arrows)(superficial drainage: 0 points).

FIG. 4. Carotid angiograms, lateral view (left) and antero-posterior view (right), showing a Grade I I arter iovenous mal-formation (AVM). The AVM is less than 3 cm (small : 1point) , located in the dominant hemisphere adjacent to thereceptive language area (Wernick e's area) (eloquent: 1 point) ,and has exclusively superficial venous drainage (arrow) (su-perficial drainage: 0 points).

T A B L E 1

Determination of arteriovenous malformation (A VM) grade*

Graded Feature Points Assigned

size of AVMsmall (< 3 cm) 1medium (3-6 cm) 2large (> 6 cm) 3

eloquence of adjacent brainnon-eloquent 0

eloquent 1pattern o f venous drainagesuperficial only 0deep 1

* Grade = [size] + [eloquence] + [venous drainage]; that is (1, 2,or 3) + (0 or 1) + (0 or 1).

ca tegor ie s ( Tab le 1 ). The g r ade o f the l e s ion i s de r ived

b y s u m m i n g t h e p o i n t s a s s i g n e d f o r e a c h c a t e g o r y . T h e

l o w e s t g r a d e p o s s i b l e i s G r a d e I ; s u c h a l e s i o n w o u l d b e

s m a l l ( 1 p o i n t ) , l o c a t e d i n a n o n - e l o q u e n t r e g i o n s u c h

a s t h e a n t e r i o r f r o n t a l l o b e ( 0 p o i n t s ) , a n d h a v e e x c l u -

s ive ly supe r f i c ia l d r a inage ( 0 po in t s ) ( F igs . 2 and 3 ) .

C o m p l e t e s u r g i c a l e x c i s i o n o f s u c h a n A V M w o u l d

p r e s e n t r e l a t i v el y m i n o r t e c h n i c a l d i f fi c u l ti e s a n d w o u l d

e n t a i l v e r y li t tl e r is k o f r e s u l t a n t m o r b i d i t y o r m o r t a l i t y .

T h e h i g h e s t g r a d e w i t h i n t h i s s c h e m e i s G r a d e V ; a n

A V M o f t h is t y p e w o u l d b e l a rg e r t h a n 6 c m ( 3 p o in t s ) ,l o c a t e d w i t h i n o r i m m e d i a t e l y a d j a c e n t t o e l o q u e n t

b r a i n ( 1 p o i n t ) , a n d a p o r t i o n o f t h e d r a i n a g e w o u l d

e m p t y i n t o t h e d e e p v e n o u s s y s t e m ( 1 p o i n t ) ( F i g s . 7

FIG. 3. Vertebral angiograms, lateral view (left) and an-teroposterior view (right), showing a Grade I ar ter iovenousmalformation (AVM). This cerebel lar AVM is less than 3 cmin diam eter (small: 1 point) , lo cated superficially on the cere-bel lar cor tex (non-eloquent: 0 points), an d d rains only throughsuperficial cerebellar hemispheric veins (arrows) (superficialdrainage: 0 points) .

FIG. 5. Carotid angiograms, lateral view (left) and antero-posterior view (right), showing a Grade I I I ar ter iovenousmalformation (AVM). The AVM is less than 3 cm (small: 1point), located adjacent to the thalamus (e loquent: 1 point) ,and drains into the galenic venous sys tem (arrow) (deepdrainage: 1 point) .

4 7 8 J. Neurosurg. / V olum e 65 /Octob er, 1986

Page 4: J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

8/8/2019 J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

http://slidepdf.com/reader/full/j-neurosurgery-a-proposed-grading-system-for-arte-rio-venous-malformations 4/8

Grading system for arteriovenous malform ations

FIG. 6. Carotid angiograms, lateral view (left) and anteroposterior views, arterial phase (center) and venousphase (right), showing a Grad e IV arterioven ous malfo rmatio n (AVM). This AVM is slightly less than 6 cm

in diameter (m edium: 2 points), located in the dom inant parietal lobe adjacent to Wernick e's area (eloquent:1 point), and drains in part in to the galenic system (arrow) (deep drainage: 1 poin t).

and 8) . A Grade V l e s ion i s a s soc ia t ed w i th s ign i f i can t

r i s k o f s u r g i c a l m o r b i d i t y a n d m o r t a l i t y . T h e s e l a r g e ,

c r i t i ca l ly loca t ed ma l forma t ions requ i re ex tens ive d i s -

s e c t i o n i n c l o s e p r o x i m i t y t o i m p o r t a n t b r a i n r e g i o n s ;t h e i r r e m o v a l m a y b e c o m p l i c a t e d b y d i f f i c u l t i e s w i t h

cont ro l l i ng f rag i l e deep ve ins . Obl i t e ra t ion of t he l a rgeA V M s h u n t p r e s e n t s s u r r o u n d i n g n o r m a l v e s se l s w i t h

a sudden inc rease in pe r fus ion tha t may re su l t i n vaso-g e n i c e d e m a o r e v e n h e m o r r h a g e ( a p h e n o m e n o n t h a t

h a s b e e n t e r m e d " n o r m a l p e r f u s i o n p r e s s u r e b r e a k -th rough " ) . ~3 Var io us com bin a t io ns o f l e s ion s i ze , l oca -

t i o n , a n d v e n o u s d r a i n a g e p a t t e r n r e s u l t i n t h e i n t e r -

med ia t e g rades o f AV M (F igs . 4 to 6) . A schem at i c

r e p r e s e n t a t i o n o f a l l 1 2 p o s s i b l e c o m b i n a t i o n s o f t h egraded c r i t e r i a i s foun d in F ig . 10.

T h e r e a r e c e r t a in l e s i o ns t h a t s h o u l d n o t c u r r e n t l y b e

c o n s i d e re d f o r s u rg e r y. W i t h i n t h i s g r o u p a r e e x t r e m e l yla rge d i f fuse AVM's tha t a re d i spe rsed th rough c r i t i ca l

n e u r o l og i c a ll y e lo q u e n t a r e a s, o r m a l f o r m a t i o n s w i t h a

d i f fuse n idus tha t encompasses c r i t i ca l s t ruc tures such

as the hypotha lamus or b ra in s t em (F ig . 9 ) . As surg ica l

r e s e ct i o n o f s u ch l e s io n s w o u l d a l m o s t u n a v o i d a b l y b e

as soc ia t ed w i th a t o t a l ly d i s ab l ing de f i c i t o r dea th , t heseA V M ' s f a l l i n t o a s e p a r a te c a t e g o r y t h a t c a n b e t e r m e d" G r a d e V I " o r , m o r e s i m p l y , " i n o p e r a b l e . "

FIG. 7. Carotid angiograms, arterial phase (left) and ve-nous phase (right), showing a Grade V arteriovenous malfor-mation (AVM). This AVM is larger than 6 cm in its greatestdiameter (large: 3 points), located in the co rpus callosum witha deep thalamic comp one nt (eloquent: 1 point), and drainspredominantly into a hugely dilated internal cerebral vein(arrow) (deep drainage: I point).

FIG. 8. Vertebral angiograms, anteroposterior view (left)and lateral view, venous phase (right), showing a Grade Varteriovenous malformation (AVM). This posterior fossaAVM is larger than 6 cm (large: 3 points), located in thecerebellar hemisphere with extension into the inferior cere-bellar peduncle and region of the deep cerebellar nuclei (elo-quent: 1 point), and drains prima rily into the galenic system(dee p drainage: 1 point) .

J. Neurosurg. / Volume 65/O ctob er, 1986 47 9

Page 5: J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

8/8/2019 J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

http://slidepdf.com/reader/full/j-neurosurgery-a-proposed-grading-system-for-arte-rio-venous-malformations 5/8

R. F. Spetzler and N. A. Martin

TABLE 2

Correlation of A VM grade with surgical results*

GradeMinor Major

No. of No Deficit Deficit Deficit DeathCases (%)

No. % No. % No. %

I 23 23 100 0 0 0 0 0

II 21 20 95 1 5 0 0 0III 25 21 84 3 12 1 4 0IV 15 11 73 3 20 1 7 0V 16 11 69 3 19 2 12 0

total 100 86 86 10 10 4 4 0

* See also Fig. 11. AVM = arteriovenous malformation.

FIG. 9. Vertebral angiograms, anteroposterior view (left)and lateral view, arterial phase (right), showing an inoperable(Grade VI) arteriovenous malformation (AVM). This AVMis fed by multiple vessels from the rostral basilar artery,encircling and infiltrating the mesencephalon. The diffuseinvolvement o f the brain stem renders this lesion inoperable.

A p p l i c a t i o n o f th e G r a d i n g S c h e m e

In order to test the predictive value of this system,

100 consecutive AVM's completely resected by one ofus (R.S.) were retroactively analyzed. The lesions weregraded on the basis of their radiographic studies, andthe complications of surgery for the malformations in

each grade were tabulated and presented in numericaland graphic form (Table 2 and Fig. 11). The compli-cations were broken down into the categories of minor

deficit, major deficit, and mortality. Temporary neu-rological deficits lasting less than 3 days are not in-

cluded. There was no mortality. The specifics of mor-bidity are listed in Table 3. The results indicate that the

correlation between AVM grade and the incidence ofneurological complications is good. Grade I and II

lesions were resected with very low incidence of surgi-

cally induced neurological deficit, while surgery forGrade IV and V AVM's was accompanied by a signifi-

cant nu mber of neurological complications.In order to test the reliability and consistency of the

grading system, 25 angiograms of patients with AVM'swere graded independently by one of the authors and

by two other neurosurge ons. There was complete agree-ment amo ng all the observers in 23 of the 25 cases, and

in 24 of 25 cases between one of the authors and aneurosurgeon. In two cases the grades varied by one; in

each instance the presence or absence of eloquence wasin question. In one case an AVM was situated in the

anterior portion of the dominan t t emporal lobe, and inthe other the AVM was situated in the periventriculararea of the left frontal horn. Even in retrospect the

jud gmen t is difficult. Thus, there is excellent correlationbetween indep endent observers in grading AVM's basedon this system.

The need for all three variables becomes quickly

apparent when the operative difficulty is comparedbetween an AVM of 2 cm located in the frontal pole

TABLE 3

Details of instances of deficit

Minor Deficit

1. very mild increase in brain-stem deficit2. temporary increase in visual field deficit3. temporary increase in aphasia and weakness4. mild increase in aphasia (resolved 90%) only detectable

with rapid speech5. temporary mild increased weakness6. increase in trigeminal nerve deficit (anticipated)7. mild temporary increase in hemiparesis8. mild residual ataxia9. temporary mild dysphasia

Major Deficit1. hemiparesis2. increase in aphasia3. homonymous hemianopsia (anticipated)4. severe neurological deficit (presumed normal perfusion

pressure breakthrough) with major aphasia and hemi-paresis

and a similarly sized AVM located in the thalamus. Byjust using size, both AVM's would be considered as

Grade I; however, by including both eloquence anddeep venous drainage the AVM's are, respectively, inGrades I and III, assessing correctly the expected mor-

bidity and mortality in the surgical management ofeach lesion.

D i s c u s s i o n

Simply put, surgical removal of an A VM is indicatedif the risk of operation is less than the risk determined

by the natural history of the AVM. As more data haveaccumulated, it has become apparent that the long-term prognosis for patients with AVM's is grim. The

ongoing risk of intracranial hemorrhage from an AVMis 2% to 3% per year, and the risk for recurrent hem-orrhage is higher than this, at least temporarily, after an

AVM has bled. 4,5 The risk o f de ath associated with

initial AVM rupture is approximately 10%, and themortality rate increases with each subsequent hemor-

rhage? ~2 The incidence of neurological deficit is ap-proximatel y 50% for each episode of hemorrhage. 16 In

480 J . Neurosurg. / Volume 65/O ctob er, 1986

Page 6: J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

8/8/2019 J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

http://slidepdf.com/reader/full/j-neurosurgery-a-proposed-grading-system-for-arte-rio-venous-malformations 6/8

Grading system for arteriovenous malformations

FIG. 10. Diagrammatic representation of the combinations of graded variables (size, eloquence, and venousdrainage) that are possible for each grade of arteriovenous malformation. There is one combination each forGrades I and V, three combinations each for Grades I I and IV, and four possible combinations for Grade III.

addition to the complications of intracranial hemor-

rhage, patients with AVM's face the lesser risks ofdeveloping flow-related symptoms, such as ischemicdeficit due to steal.

An estimation o f the risk that confr onts an individual

patient with an A VM requires specific consideration ofcertain characteristics of both the AVM itself and thepatient harboring the AVM. For instance, untreated

AVM's located in the posterior fossa appear to have aparticularly poor prognosis, 4 and small AVM 's seem to

J. Neurosurg. / Vo lume 65 /Oc tob er, 1986 481

Page 7: J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

8/8/2019 J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

http://slidepdf.com/reader/full/j-neurosurgery-a-proposed-grading-system-for-arte-rio-venous-malformations 7/8

20% -

m MAJORDEFICIT

[~ MINOREFICIT

10%

0% ~ JI I I I l l I V V

GRADES

FIG. 11. Correlation of arteriov enous malform ation gradeswith surgical results. See also Tab le 2.

have a grea te r p ropens i ty to b leed spontaneous ly thando la rge m a lforma t ions . 5 Chi ldren face a grea te r dangerthan d o adul t s in tha t they have be fore them the pe r iodof l ife of highest r isk for AVM rupture (ages 15 to 40years) / '~2 Patient-specif ic character ist ics such as thesemust be cons ide red in the formula t ion of p rognos is foreach case . Recent ly publ i shed rev iews provide a mo redeta iled analysis of the c l inical features that inf luenceth e b e h a v io r o f i n d iv id u a l A V M' s a n d o f t h e n a tu r a lhistory of these lesions as a group. 7'~6

There i s less ava i lab le in form a t ion tha t can be ap pl iedto a de te rmina t ion of the r i sks tha t a t tend surg ica l

remova l o f an ind iv idua l AVM. In the pas t , th is e s t i -ma t io n h a s b e e n d e p e n d e n t o n t h e k n o w le d g e a n dpersona l expe r ience of the surgeon involved in the case ,and has of ten been imprec ise and nonsy s temat ic . I t hasbeen diff icult to apply the surgical results as reporte d inthe l i te ra ture because the AV M's in these r epor ts havebeen inco mp lete ly character ized . 2'~~

As d iscussed above , ca tegor iza t ion of AV M's accord-ing to s ize or num ber of f eed ing a r te rie s on ly i s insuf -f ic ient . For these reasons this grading system was con-structed. I t is simple , easy to learn, and easy to apply.No re la t ively simple grading system will accurate lyc la ss i fy a l l the va r ia t ions of such complex vascu la r

le sions. For ins tance , r e la t ive ly sma l l AV M's may havemore or le ss d i rec t a r te r iovenous con nec t ion s r e su l t ingin ve ry h igh f lows - - a f ea ture tha t cons ide rab ly com-pl icate s the i r surg ica l t r ea tment . This sys tem m ay assignan inap prop ria te ly low grade to such a lesion, since sizera the r than f low is scored . The loca t ion and organiza -t ion o f e loquen t a reas , pa r t icu la rly those ad jacent to anA V M, ma y v a r y f r o m th e n o r m a n d t h u s b e a n o th e rpoten t ia l source of e r ror . This may re su l t in un der - o rove res t ima t ion o f the r i sk of caus ing s ign i f icant neu-rological def ici t in a specif ic case . In spite of occasionalinappropr ia teness o f the a ss igned grade , we be l ieve tha tthe s impl ic i ty of the sys tem is an advantage . In orde r

R . F . S p e t z l e r a n d N . A . M a r t i n

to t a k e i n to c o n s id e r a t i o n e v e r y p o s sib le a n a to m ic a n dp h y s io lo g ic a l p e r m u ta t i o n o f A V M' s , t h e s c h e me w o u ldhave to be so comp lex as to be imprac t ica l .

This g rad ing sys tem has demonst ra ted a r e la t ionsh ipto the technica l d i f f icu l ty of r emoving ind iv idua l

AVM's . Vir tua l ly a l l the Grade I and I I AVM's wererem oved wi th out m uch d i f f icu lty in s ing le - s taged pro-cedures . The Grade IV and V le s ions , however , o f tenr e q u i r ed p r e - a n d i n t r a o p e r a t i v e e mb o l i z a t i o n a n d mu l -t istaged surgical resection.

This grad ing sys tem is des igned to be pred ic t ive ofthe r e su l t s o f com ple te surg ica l r e sec t ion of AVM 's .T h i s r e ma in s t h e "g o ld s t a n d a r d " f o r t h e t r e a tme n t o fAVM 's , a s i t i s the o n ly me t hod t ha t v i r tua l ly e l imina testh e r i sk o f f u tu r e h e mo r r h a g e . L o n g - t e r m f o l l o w - u pr e v ie w o f p a t i e n t s w h o se A V M' s w e r e c o mp le t e ly e x-c ised has conf i r med tha t they a re a lmost fu l ly pro tec tedf rom reb leed ing . 3 Incom ple te surg ica l r e mov a l andfeeding a r te ry l iga t ion do no t p reve nt la te r b leed ing , z3

I n c o mp le t e o b l i t e r a t i o n o f t h e A V M b y e mb o l i z a t i o na lso fa i l s to provide pro tec t ion f rom subsequent hem-or rhage. 9 Even in cases tha t show com ple te angio-graphic ob l i te ra t ion a f te r embol iza t ion , the re i s no a s-su r a n ce t h a t h e m o r r h a g e c a n n o t o c c u r in t h e f u tu r e . Insu c h t h o r o u g h ly e mb o l i z e d c ases , t h e n id u s o f t h e A V Mnever the le ss r ema ins in the bra in and the poss ib i l ity ford e l a y ed r e c a n al i z a t i o n o f p o r t i o n s o f t h e m a l f o r ma t io nthroug h co l la te ra l channe ls ex is t s.

S te reo tax ica l ly d i rec ted rad ia t ion the rapy i s anothe rtechniq ue ava i lab le for the t r ea tm ent of AVM 's . 6'~5 Ou rgrad ing sys tem may be appl ied to le s ions t r ea ted e i the rb y r a d i a ti o n t h e r a p y o r b y e mb o l i z a t i o n f o r t h e p u r p o seof comp ar ing the r e su l t s o f these techniques wi th thoseof surgical excision. I t is , however , quite possible thatth is sys tem wi l l no t accura te ly pred ic t the r e su l t s o fembol iza t ion or r ad ia t ion the rapy , a s the compl ica t ionsof these types of t r ea tm ent d i f f e r f rom tho se of surgery .

A prospec t ive appl ica t ion of th is g rad ing sca le inAVM cases i s cur ren t ly underway. I f th is sca le in i t ss impl ic i ty proves to pred ic t ope ra t ive morbi d i ty in o th e rse ries , i t wi ll p rov ide a use fu l too l for dec is ion-ma kingin t h e ma n a g e me n t o f p a t i e n t s w i th A V M' s . A s afur the r bene f i t , i t wi l l f ac i l i ta te compar ison of AVMtrea tm ent r e su l ts be tween se r ies or be tween techniques .

Acknowledgments

The authors w ould like to than k M arjorie Medina, R.N.,and Drs. Issam Awad and Daniele Rigamonti for independ-ently assisting in grading the A VM's.

References

1. Celli P, Ferrante L, Palm a L, et al: Cerebral arterioveno usmalfo rmatio ns in children. Clinical features and ou tcom eof treatment in children and in adults. Surg Neurol 22:43-49, 1984

2. Drake CG: Cerebral arteriovenous malformations: con-siderations for and experience with surgical treatment in166 eases. Clin Neuro surg 26:145-208 , 1979

482 J. Neurosurg. / Volum e 65 /Octob er, 1986

Page 8: J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

8/8/2019 J Neurosurgery - A Proposed Grading System for Arte Rio Venous Malformations

http://slidepdf.com/reader/full/j-neurosurgery-a-proposed-grading-system-for-arte-rio-venous-malformations 8/8

Grading system for arteriovenous malform ations

3. Forste r DMC, Ste iner L, Hfikanson S: Arte r iovenousmalform at ions of the bra in . A long-te rm c l in ica l s tudy. JNcurosurg 37:562-570, 1972

4. Ful ts D, K el ly DL Jr : Natur a l h istory of a r te r iovenousmalfor mat ions o f the bra in : a c l in ica l s tudy. Neurosurgery15:658-662, 1984

5. G raf C J , Perre t GE, T orner JC: Bleeding from cerebra la r te r iovenous malformat ions as par t of the i r na tura l h is-tory. J Neu rosurg 58:331-337 , 1983

6. Kje l lberg RN, Han amu ra T, Davis KR, e t a l: Bragg-peakp ro to n -b e a m th e ra p y fo r a r t e rio v e n o u s ma l fo rma t io n s o fthe brain. N Engi J M ed 309:26 9-274, 1983

7. Luessenhop A J: Natura l h istory of cerebra l a r te r iovenousmalformat ions, in Wilson CB, Ste in BM (eds) : Intracra-nial Arteriovenous Malformations. Bal t imore : Wil l iams& Wilkins, 1984, pp 12-23

8. L uessenhop A J, Gennar e l l i TA: A natom ica l grading ofsupra tentor ia l a r te r iovenous malformat ion s for de te rmin-ing operabi l i ty . Neurosurgery 1 :30-35, 1977

9. Luessenhop AJ, Presper JH: Surgica l embol iza t ion ofcerebra l a r te r iovenous malformat ions through in te rna lcaro t id and ver tebra l a r ter ies . Long-te rm resul ts . J Neu-

rosur g 42:443-4 51, 197510. Parkinson D, Bachers G: Arte r iovenous malformat ions.

Sum mary of 100 consecutive supra tentor ia l cases. J N eu-rosurg 53:285-299, 1980

11. Pellettieri L, Carlsso n CA, Grev sten S, et al: Surgicalversus conserva t ive t rea tment of in t racrania l a r te r iove-

nous m alformat ions. A s tudy in surgica l dec ision-making.Acta Neuroehir Suppl 29:1-86, 1980

12. Perre t G, Nishioka H: Report on the Coopera t ive Studyo f In t r a c ra n ia l A n e u ry sms a n d Su b a ra c h n o id H e mo r -rhage . Sec t ion VI. Arte r iovenous malformat io ns. An ana l-ysis of 545 cases of c ranio-cerebra l a r te r iovenous m alfor-

mat ions and f is tu lae reported to the Coopera t ive Study.J Neurosu rg 25:467-49 0, 196613. Spe tz le r RF, Wilson CB, Weinste in P, e t a l : Normal

perfusion pressure breakthrough theory . Cl in Neurosurg25:651-672, 1978

14. Ste in BM, W olper t SM: Arte r ioven ous malform at ions ofthe bra in . I. Current concepts and t rea tment . Arch Neurol37:1-5, 1980

15. Ste iner L: Trea tment of a r te r iovenou s malform at ions byradiosurgery , in W ilson CB, Ste in BM (eds) : IntracranialArteriovenoas Ma l fo rma t io n s . Ba l t imo re : Wi l l i a ms &Wilkins, 1984, pp 295-314

16. Wilk ins RH: Natura l h istory of in t racrania l vascular mal-format ions: a review. Neurosurgery 16 :421-430, 1985

Man uscr ipt received July 3, 1985.Accep ted in final form A pril 10, 1986.Address reprint requests to: Robert F . Spe tz le r , M.D.,

Edi tor ia l Off ice , Barrow Neurologica l Inst i tu te , 350 WestThomas Road, Phoenix , Arizona 85013.

J. Neurosurg. / Volume 65 / October, 1986 4 8 3