Sulcal, ventricular, and white matter changes at MR imaging in the aging brain: data from the...

8/17/2019 Sulcal, ventricular, and white matter changes at MR imaging in the aging brain: data from the cardiovascular heal…

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N an cy C h a n g Y u e , M D { 1 4 9 } lic e M . A rn o ld , P h D

{ 149}

illiam T . L on gs tre th , Jr , M D , M P H

A llen D . E lster , M D { 149}h a rle s A . Ju n gre is , M D { 149}

an ie l H . O ’L ea ry ,

M D

V irg in ia C . P o ir ier , M D { 1 4 9 }R . N ick B ryan , M D , P h D

S u lc a l, V e n tr ic u la r , an d W h ite M a tte r

C h a n g es a t M R Im a g in g in th e A g in g B r a in :

D a ta fr o m th e C a r d io v a sc u la r H e a lth S tu d y ’

In d ex ter m s:

A g i n g ,

10 .91 , 10 .92

#{149}

r a in , a n a tom y, 1 0 .9 1 , 1 0 .9 2

#{149}

ra in , atr op h y, 10 .83

#{149}

r a i n ,

M R . 1 0.1 21 41 1

A b bre v ia tion : C H S = C ard iov asc u la r H eal th S tu dy .

R a d io log y 19 97; 202 :3 3-3 9

I

F rom th e D ep artm e n t of R a d io log y , T h e J oh n s H op k in s U n iv ers ity S c h oo l of M ed icin e, 60 0 N

W o lfe S t , B altim ore , M D 2 12 87-218 2 (N .C .Y ., R .N .B .); th e C ard iov ascu lar H e alth S tu d y C o ord in a tin g

C e n te r, S ea ttle , W a sh (A .M .A .); th e D ep a rtm en ts o f N eu rolo gy an d E p id em io log y , U n iv ers ity of

W a sh in g ton , S eattle (W .T .L .); th e D ep artm e n t of R ad io lo gy , B ow m a n G r ay S c h o ol of M ed icin e,

W a k e F o res t U n iv ers ity , W in sto n -S alem , N C (A .D .E .); th e N eu ror ad io lo gy D iv isio n , U n iver sity o f

P ittsburgh M edica l C en te r, P a (C .A .J .) ; the D ep ar tm en t o f R ad io logy , N ew E n gland M edica l C en te r,

B os ton , M ass (D .H .O .); a n d R egio n a l D iagn os tics , C le vela n d , O h io (V .C .P .). F r om th e 19 95 R S N A

scie n ti fic a ssem bly . R ec eiv ed M a y 6, 1 996 ; rev is ion re que ste d Ju ly 11; rev isio n r ece ive d A u g u s t 19 ;

acc ep ted A u gu st 26 . S u p p orted in p a rt b y th e N ation al H e art , L u n g, a n d B lood In stitu te con tr acts

N 01 -H C -8 50 79 , N 01 -H C - 8 508 0 , N 01 -H C -850 81 , N 0 1-H C -850 82 , N 01-H C -85 08 3 , N 0 1.H C -85 084 , N O l-

H C - 8 5 0 8 5 N 0 1 - H C - 8 5 0 8 6 , N 0 1-H C -15 103 . A d d re ss re p r in t r eq u ests to N .C .Y .

C R S N A , 1 9 9 7

S ee a lso th e a rtic les b y Y u e et a l (p p 41 -46 ) an d B ry an e t a l (p p

47-54)

a n d th e ed ito ria l b yjack (p p

17-19) in th is is sue .

33

N e u r o r a d io lo g y

P UR P OS E T o d eterm in e th e d istr i-

bu tion of changes in su lca l s ize , y en -

tr icu la r size, and w h ite

m atter sign a l

in ten sity d ep icted

o n cran ia l m ag -

n e tic reson a n ce (M R ) im ages, w ith

stratification ac cor d in g to ag e, r ace ,

a n d sex .

MATER IALS AND M ETHODS :

V en -

tr icu la r size, su lca l s ize , and

w h i t e

ma i l e r sig na l in ten sity ch an ges w ere

g ra d ed

on

cran ia l M R im ag es o f 3 ,660

com m un ity - liv ing , e lde r ly pa rtic i-

p an ts in th e C ard iova scu la r H ea lth

S tu dy . A h ea lth ier su b g ro u p w a s a lso

d e fin ed . S u m m ary sta tis tic s for b o th

g ro u p s w ere gen era ted fo r ag e, race ,

an d sex .

RESULTS : Regression m od e ls o f th e

en tire im aged cohor t show ed higher

grad es o f a ll var iab le s w ith increas-

in g a ge , an d h igh er v en tr icu la r a n d

su lca l g rad es in m en an d in n on b la ck

in d iv id u a ls . W h ite m atter grad e w as

gr eater in w om en a n d in b la ck m d i-

v id u a ls . R egressio n m od e ls o f th e

h ea lth ier su bg rou p sh ow ed s im ila r

assoc ia t ion s, excep t fo r a la ck of a sso -

c iatio n of su lca l an d ven tr icu la r size

w ith ra ce .

ON L US I ON

S u lca l w idth , yen -

tricu lar size , and w hite m atte r sig na l

in tensity change w ith ag e, se x , an d

race.

K n ow ledg e of th ese ch a ng es is

im p ortan t in ap propria te in te rp reta -

lion of M R im ag es o f th e e ld er ly .

M E A N I N G F U L in terp re ta tion o f neuro -

imag ing s tud ies o f th e eld er ly

req u ires a

know ledge o f a g e- r el at ed

chang es in th e b ra in . Sulca l en large-

m en t ,

ven tricu la r en la rg em en t, an d

hyperin tensi ty of p en ven tr icu lar an d

su bcortica l w h ite m a tter o n m agne tic

reson an ce (M R) images of th e b ra in ar e

tho ugh t to rep re sen t senescen t chang es

in n euro log ica lly in tac t elde rly ind iv idu -

als. T he p reva lence and ex ten t o f the se

changes as a func tion of age , sex , a n d

race in an e lde rly po pu la tion , h ow ev e r,

ar e in com ple tely d o cu m en ted .

A ltho ugh sev era l se ries (1 -4 ) h av e

addressed these a ge -d ep en den t ch an ges

as seen in the b rain a t c ran ia l co m puted

to m o grap h y (C T ) a n d M R imag ing ,

m o st o f th ese ser ie s com prised re lativ e ly

sm all nu m bers of in d iv id u a ls , an d so m e

h ad stro n g selec tio n b iases. T h e

purpose

o f th is study

w as to d e term in e th e d istr i-

bu tio n of chang es in su lcal s ize , y en -

tr icu la r size , an d w h ite m a tter d ep ic ted

on c ran ia l M R

im ages w ith stra tification

accord ing to age , sex , a n d ra ce .

M A T E R IA L S A N D M E T H O D S

P a rtic ipa n t S e lec tion

P artic ipan ts in th is stu dy w ere se lec ted

from th e co hort o f the C ard iovascu la r

H ea lth S tud y (C H S ), an ob serva tion al,

pop u la tion -based , long itud in al study of

card io vascu la r and ce reb ro vascu la r d is-

ease in adu lts ag ed 65 y ears and o lder.

C H S p artic ip an ts w ere recru ited in fo u r

co m m unities (Forsy th C ou n ty , N C ; P itts-

bu rgh , P a ; S ac ram en to C oun ty , C a lif;

W ash in g ton C o un ty , M d ) from M edica re

elig ib ility lis ts p rov ided b y the U .S . H ea lth

C are F inanc ing A dm in istratio n . P a rtic i-

pan ts w ere rec ru ited

with

ran dom sam -

p l ing to p rov ide eig h t sub group s stra tif ied

by ag e and sex . In d iv idua ls w ere exc luded

from the C H S if they w ere com m itted to

an in stitu tion tha t p reven ted p artic ipa -

lion ; h ad a te rm ina l illne ss; w ere u na b le

to w alk , com m unica te, o r g ive in fo rm ed

consen t ; or w ere lik e ly to m ove from th e

area du ring the 3 yea rs a fte r en try in to the

s tudy .

O f e lig ib le p erson s rec ru ited fo r the

C H S , 57 .6 % (5 ,888 of 10 ,22 2) agreed to p ar -

t ic ip ate an d

w ere en ro lled in th e stu dy .

T ho se w h o p artic ipa ted w ere m ore edu -

ca ted , yo ung e r, and m o re lik ely to be m ar-

n ed than tho se w h o d id no t. D e tails o f the

C H S design (5 ,6 ) an d rec ru itm en t

7

h av e

been desc rib ed els ew here.

M R Im agin g

M R im ag in g w as p erfo rm ed in 3 ,660

p art ic ip an ts; the se par tic ipan ts h ad

no

co n tra in d ications and gave consen t (8 ).

C on tra ind ica tion s inc luded m eta l ob jec ts

in the body su ch as m eta l fragm ents near


2/7

F igu re 1 . M R im ag es d em o n s tra te su lca l gra d e s 1-8 .

34 { 1 4 9 }

adio logy

January 19 97

th e e ye s, b ra in , o r sp inal c ord ; in tra cra n ia l

a neu rysm clips; p rosthet ic he art va lve s;

card iac pacem akcr;

or oth er in ternal dcc -

tr ic d ev ic es .

M R im aging

wa s

pe rform e d on 1 .5-T

im a gers (G E M ed ica l S y ste m s, M ilw au ke e,

W is ; P icke r, C le veland , O h io)

at th ree fie ld

c en ters a nd o n

o.35- r

im ag er (T osh ib a

A m eric an M edical S ystem s, D u lu th , G a )

at

the fourth . I h e im ag ing

p re)toco l in -

e lud ed stand ard sag itta l an d ax ial sp in-

e cho 1 1 -w e igh ted ( rep etit ion tim e m sec /

e cho tim e m sec, 500 15-25) , ax ial sp in-

de ns ity -w e igh ted (3 ,0 00 /20 -33 ), an d ax ia l

2 -ve ig l itcd (3 ,0 00 /70 - 1 00 ) im ag ing , a ll

with 5 - m m sect ion th ickn ess a nd no

ga ps ,

as detailed in the re por ts of th e p ilo t s tud y

5 ,8 ) . A x ial im ag ing w as p erfo rm ed p ar-

a lle l to a lin e be tw e en th e an terie )r a nd

po ste rio r e ’e)m rn lssure s. Im a gin g w as p er-

fo rn ie’d w ith ou t ad n iin istra tion o f co n trast

n ia te’ria I.

M R Im a gin g R ead in g C en ter

Th e acqu ired im age da ta w ere trans-

ferre d to m a gn etic tap e a nd d elivered to

the M R im ag in g read in g cen te r, w here a ll

96 im ages from each partic ip an t w ere d is -

p lay ed sim ultane ous ly on fo ur 1 ,024 x

1 ,0 24-p ix el w o rks ta tion m o nito rs w ith 2 56

gra y-scale in tens itie s. A ll im ag es w ere

read b y b oard-c erti fied ra d io log ists (in -

elu d in g N .C .Y .) w ith at lea st I ye ar of i ieu -

ro rad io logy fellow ship tra in ing and a fte r

com pletio n e )f an M R im agin g in terp reta -

tion tra in ing cou rse de sig ned

to

m e e t

spec ified reader rep roduc ib ility c rite ria .

M R im a gin g find ing s w ere e ntere d in a

com p ute r d a tabase by the read ers. R eaders

w ere b linded to a ll c lin ica l in fo rm ation , in -

e lud ing ag e, s ex , an d race .

G ra d ing S ystem s

T he su lca l p ro m inen ce, ve n tricu lar size ,

a nd w hite m at t e r

signa l in tensity ch an ges

in e ach ind iv id ual w e re a sse sse d o n a

se m iqua n ti ta tive 10 -po in t s cale (grade s o f

0 -9) b y usin g p red efin ed v isu al sta nda rds

from

atlases co m p ose d of 40 re fere nc e

c ases . P or tion s o f th ese atlase s ha ve bee n

p rev iou sly p ub lish ed (5), an d the m eth ods

d esc ribe d . S u lcal g rad es ran ged fro m v ery

sm all su lc i (g rade 0 ) to very larg e su lc i

(g rade 9) (F ig 1) . V entric u lar gra des cx -

te nd ed from sli tlik e v en tric les (g rad e 0) to

m ark ed ly e n la rge d ven tric les (g rad e

9) (F ig 2). “W hite m atter cha nge s” w ere

e stim ate d as th e to ta l ex te n t of p eriv en -

tricu la r and su bcortica l w hite m atte r s ig -

na l-in ten sity a bno rm ality o n sp in-d ens ity -

weigh ted ax ia l im ages; w hite m atte r

c han ges suc ces siv ely inc rea sed fro m no o r

b arely de tectab le cha ng e (gra des 0 a nd 1 ,

respec tiv ely ) to a lm ost all w h ite

matte r

in vo lve d (g rad e 9) (F ig 3) . F ro n ta l horn

w id th , in ner tab le d is tan ce, a nd c en tral

su lcu s w id th w ere m e asu red w ith an d cc-

tro n ic cu rso r. W hite m atter ch an ges

in

th e

b rain s tem w ere rec ord ed as no ne , m in i-

m a l, o r m odera te to severe . T he genera l

pat tern

of

sup rate n to ria l w h ite m a tte r

c han ges (per ive n tr icu lar cha ng es greater

than sub co rtica l ch anges, pe riven tricu lar

e qua l to su hco rtical ch ang es, o r per ive n-

tric u lar cha nge s less th an sub co rtic al

cha ng es) w as also reco rde d . A bn orm ali ties

in te rp reted as rep resen ta tive of a reas o f

la rge-v essel ce reb ra l in fa rc t o r sm all-vesse l

lac una r in fa rct w ere co ded sep ara te ly in

the da tabase as in fa rc tlike les ions . In fa rc t-

l ike lesions , foc al atro ph y , a nd o the r Ic-

sio ns w ere m ea sured and re corded and a re

d iscussed

in

separa te reports (9 ,10) .

T h e H ea lth ier S u b grou p

W e w er e a lso in te res ted in e xp lor in g th e

p oss ib le d iffe re nc e in t he a pp ea ra nc e on

cran ial M R im ages of ag in g in th e en tire

im aged C H S cohor t ve rsus ag ing in a

h ealth ie r subgro up . T he fo llow ing exc lu -

s ion c rite ria w ere used to d istingu ish th is

h ealth ie r sub grou p (so m e sub jec ts m et

m o re th a n on e e xclu sion c rite rio n ) from

the cohort o f 3 ,660 p artic ipan ts: (a ) 68 8

p artic ipan ts w ith in farcts g rea te r than 1 .5

cm in dia m e ter, fo cal bra in atroph y , p a-

ren chym al herna tom a, d iagno sis o f

“o ther” (inc lu d ing c lin ica lly im p ortan t

“ale rts” ), o r som e com bina tion o f these

f ind ing s on c ran ial M R im a ges ; (/‘) 328

p art ic ip an ts w ith self -rep orted clin ica l

trans ien t isch em ic a ttack or s troke prio r to

M R im aging ; (c ) 840 p ar tic ipan ts w ith

base line coronary ar te ry d isease (m yo car-

d ia l in fa rc t, ang in a, co ronary arte ry by pass

g ra ft , a ng io pl as ty );

(it)

14 4 par t ic ipan ts

w ith a m o dified M in i-M enta l S ta te exam i-

n ation sco re o f les s tha n 72 on a 1 00 -po in t

s cale (ie , 2 sta nd ard de v iat ion s be low the

m ea n); an d (c ’) 1 ,1 78 pa rtic ipa n ts w ith a

h isto ry o f com a, ce reb ra l p alsy , cancer,


3/7

F igu re 2 . M R im age s dem onstrate ve ntric u lar g r a d e s

1-8 .

.-

\

1

; :

; . L ,

5

6

7

8

V olu m e 2 02 { 1 4 9 }u m b e r I

Radio logy { 1 4 9 }5

F ig u re 3 . M R im a ges de m on stra te w h ite m atte r grades 1-8 . (R ep rin ted , w ith p e rm ission , from re fer en c e 5. )

b ra in tum or, b rain su rg ery , s eizu res , o the r

n eu ro lo g ic d ise ase s, lo ss o t

consc iousness

du e to head traum a, o r so n ic com b in ation

e)f th ese co n d itio n s .

T h e re m a in in g 1 ,488 p ar tic ip an ts w ere

inc luded

in

the hea lth ier sub group . T hese

include d 1 ,2 65 (85 % )

no nb lack an d 223

(15% ) black p art ic ip an ts, a ra cia l p ro po r-

tion iden tica l to th at o f the en tire M R

im a gin g C H S c oho rt.

S ta tist ica l A na ly ses

Sum m ary s ta tistic s from the M R im ag-

in g find ings of the en tire co hort and fro m

th e h ea lth ier su b g rou p w ere g en era ted for

5-y ear age g roups , race , and sex . B ivariate

corre la tions am on g the M R im aging v an -

ab les w ere ex am in ed . R egression m od e ls

w e re ge n er ate d fo r eac h of th e gra d e d

variab les and fo r the fron ta l h orn ra tio

and cen tra l su lcus w id th fo r the en tire co -

h o rt an d for th e h e alth ie r su b gro u p . T w o-

s tag e m od els w ere u sed , w hich a llow ed


4/7

T ab le I

In trarea d er an d

I nt er re ad er R elia bilit y

in a S u b se t o f M R Im a ge S e ts

In trare ade r A greem en t In traread er In terread er A g ree m e nt

In ter reader

V ar iab le w ith in O ne G ra de R ela xed K*

w ith in O ne G ra de

Relaxed K

Ve ntr ic le s 12 0/1 27 (9 4.4 %)

0 .89 2 32 /25 2 (92 .1% ) 0 .89

S ulci 11 4 /1 27 (8 9 .8 % )

0 .87 18 7/2 51 (74 .5’% )

0 .66

W hite m atte r

124 /128 (96 .9% ) 0 .96

2 15/25 1 (8 5 .7% ) 0.8 1

N ote -N um bers in pa rentheses a re perc enta ge s.

*

Th e

K

scor e is th e c h a n ce , ad ju ste d p er cen tag e ag ree m e n t scor e w ith th e fo llow in g q u alita tive d e -

sc rip to rs: ex cel len t (

>

0. 75) , fa ir to go od

(0 . 4 0 -0 . 7 5 ) , an d p o or ( <

0 .40) . ihe ‘relaxe d

K

h as the sam e d e-

sc rip to rs; how ev er, th e pe rce n ta ge ag ree m e nt of e xac tly m atc h in g g rad es is obv iou sly low er betw ee n

obse rve r s as a n a llow an ce o f ± o ne g rad e is p erm itted in th e s ta tistic al an aly sis (36) .

* D a ta a re m ean ± s tan d a rd d ev iation .

36 { 1 4 9 }

ad io lo gy Jan u a ry 1 997

ag e, sex , and race to en te r a t th e first stage ,

if s tatis tica lly sign ifican t, and o ther M R

im ag ing v ariab les to en ter at the se con d

stage . P o te n tia l in tera ctio ns be tw e en ag e

and sex and be tw een age and race w ere

tes ted .

E xam ina tion of

t he d is tr ib u ti on

of

residu als show ed adequa te m ode l fit, even

fo r the ca tegor ica l, g raded variab les. A ll

an aly ses w e re pe rfo rm e d w ith S P S S 6 .1

(S P S S , C h ica go , Ill ).

R E S U L T S

M R Im a gin g C o m p letion R ates

C ereb ral M R im ag ing w as corn -

p le ted in 3 ,66 0 of the C H S p artic i-

pan ts. T hese partic ipan ts inc lu ded

3 ,094 (85% ) nonb lack (w hite [n =

3 ,0731 an d o ther races [n

=

211 ) an d

566 (1 5% ) b lack coh ort m em bers.

T hree hund red th ree M R im ag e se ts

from the p ilo t stud y (8 ) com ple ted in

1992 w ere inc luded . T he rem ain in g

M R im age se ts w ere com ple ted in

years 5 and 6 (Jun e 19 92 to M ay 19 94).

M R im aging com ple tio n ra tes and

reasons fo r no ncom ple tio n are tab u-

la ted in a separa te report (9 ).

T he subgro up of partic ipan ts tha t

u nderw en t M R im aging w ere s ign ifi-

can tly m ore like ly to be you nger an d

less like ly to have hyp erten sion , d ia -

be tes , o r co ronary heart d isease than

w e r e tho se w ho d id n o t (11). T h ere

w as no sta tistica lly sign if ican t d iffe r-

ence in p ar tic ipa tion ra tes f rom th e

fou r s tudy site s .

R ep rod u c ib ility o f R esu lts

B linded d up lica te p rim ary read ings

w ere pe rfo rm ed w ith 384 (10 % ) of the

M R im age sets to assess in te r- and

in tra reader variab ility (8 ). In te r- and

in tna reader re liab ility based on “re laxed ”

K

s ta tis tic s (ag reem en t w ith in 1 grade)

a re p resen ted in T ab le 1 . T he stand ard

dev ia tion fo r in ter read er m easurem en ts

o f fron ta l h orn w id th , in ner tab le d is -

tance, an d cen tral su lcus w id th w ere 3 .0

m m , 3 .7 m m , and 1 .2 m m , respec tive ly .

Fo r w h ite m atte r loca tion (p er iv en tr icu -

Ian vs subcor tica l and bra in stem ), in te r-

reader and in tra read en

K

va lues w ere

0 .4 () and 0 .58 , respec tive ly .

S u lca l R a tin g in th e C oh or t

S u lca l grad e in the C H S cohort w as

independ en tly and s ign ifican tly in -

c reased w ith age P

<

.0 001) (T ab le

2) , m ale se x

P

< .0 00 1), an d n onb lack

race P

=

.(X )12) (F ig 4) . I t w as a lso sig -

nif ica n tly and p osi tive ly a sso ciated

w ith ven tricu la r size P

<

.00 01) bu t

no t w ith w hite m atter g rade befo re

ven tricu la r g rad e w as add ed to the

m o d e l P = .81 17). T h e s lo pe of th e

reg ress ion line o f su lca l g rad e w ith

ag e w as s im ila r fo r m en and w om en .

R egress ion m ode ls o f cen tra l su lcu s

w id th , m easured separa te ly , show ed

s im ila r a ss oc iatio ns.

V entr icu lar E n la rgem en t in the

C o h o rt

V entricu la r g rade w as s ign ifican tly

assoc ia ted w ith age

P

< .00 01 )

(T ab le

2 ) an d sex P

<

.0 001). H ig her yen-

tn icu la r g rades w ere foun d in m en

(F ig 5 ). V en tricu lar g rade w as s ign ifi-

can tly la rger in nonb lacks than in

b lacks P = .0068 ). V en tricu la r g rade

w as a lso independ en tly asso cia ted

w ith su lca l g rade P

<

.0001 ) an d

w hite m atte r g rade

P

< .00 01). P lan i-

m etric fron ta l h orn ra tio (th e ra tio o f

fron ta l h orn w id th to in ner tab le d is-

tan ce) a lso in c reased w ith age P <

.0001)andmalesex(P

<

.0001)bu t

d id no t s ig n ifican tly vary w ith resp ect

to race P = .0583) .

W h ite M a tter H y p er in ten sity in th e

C o h o r t

T he m ean w hite m atte r g rade a lso

inc reased w ith age

P

< .0 001 )

(Tab le

2). W hite m atter g rade w as g rea te r in

w o m e n P = .0064 ) (F ig 6). In ad d i-

tion , w hite m atte r g rade increased

m ore qu ick ly w ith ag e in w om en than

in m en . T he range w as narro w er in

th e young er ag e group s and broader

in the o lder g roups , as re flec ted by

th e increase in standard d ev ia tion

(T ab le 2 ). In co n trad is tinc tion to yen-

tr icu la r and su lca l g rades , w hite m at-

ten

grad e w as s ign ifican tly g rea te r in

th e b lack popu la tion P = .0 032) (F ig

6). T here w as a sign ifican t assoc ia tion

w ith ven tricu lar g rade P < .000 1) .

T here w as n o assoc ia tion w ith su lca l

g rade afte r v en tricu la r g rade w as

added to the m od el. A p prox im ate ly

34 ,7 (7 (1 ,2 60 of 3 ,6 28) o f the partic i-

pan ts had little o r no w h ite m atte r

changes , as re flec ted b y a grade o f 0

or 1 . T he d istribu tion w as predom i-

nan tly pen iven tn icu la r in 72 .7% (2 ,6 50

of 3 ,628 ) o f the participan ts , subcorti-

T a b l e

2

G rad ing of M R Im ag ing F ind ings in

D ifferen t A ge G rou p s

A ge (y) a t

M R Im ag in g

G rade*

S u l c a l

Al l

65-69

70-74

75-79

80 +

3 .4 ± 1.2

2 .9 ± 1 .0

3. 2 ±

1. 1

3.5 ±

1. 2

3. 9

±

1. 3

Ventr icu lar

Al l

65-69

70-74

75-79

80 +

3 .6 ± 1 .3

3 .0 ±

1.2

3. 4

±

1. 2

3. 7 ± 1. 2

4. 2 ± 1.3

W hite M atte r

Al l

65-69

70-74

75-79

80 +

2 .3 ± 1 .5

1.7 ± 1. 2

2. 0 ± 1. 3

2. 4 ±

1.4

2 .9± 1 .7

ca l in 4 .9 % (179 of 3 ,6 43) o f the partic i-

pan ts , and ba lan ced in 2 2 .3 % (81 4 of

3 ,643 ) o f the partic ipan ts . T he w h ite

m atter chang es w ere sym m etric in

9 5 .7% (3 ,489 of 3 ,645) o f the partic i-

pan ts . T h e b ra in stem show ed no

w hite m atte r ch an ges in 80 .9 % (2 ,94 8

of 3 ,645) o f the partic ipan ts, m in im al

changes in 15 .3% (55 9 of 3 ,645), and

m o dera te o r m arked ch an ges in 3 .8%

(138 of 3 ,6 45).


Iden tica l ana lyses w ere perfo rm ed in

the h ea lth ie r subgroup . A lth ough the

age an d sex assoc ia tions in th is su b-

g ro up w ere iden tica l to th ose in en tire

coho rt, race w as no longer s ign ifican tly

assoc ia ted w ith v en tricu la r

P

= .1514)

o r su lca l P

=

.11 61) g rade . Partic ip an ts

in the hea lth ie r sub group h ad , on av er-

age , a ven tricu la r g rade 0 .2 1 low er an d a

w hite m atte r g rade 0 .23 low er than p ar-

tic ip an ts in the rem a inde r o f th e coh ort


5/7

Entire C HS Coho rt

aM

N M B M

Entire C H S C ohort

4 . 5 . 6 .

F igu res 4-fl . G ra p h s o f M R im ag in g fin d in gs in th e C H S co h or t.

BF

= b lack f e ma l e ,

BM

= b lack m ale ,

NF

= n on b la ck fe m a le, NM = n o n b l a c k

male . (4 ) G raph sh ow s su lca l g rade a cco rd ing to se x , race , and ag e. (5 ) G rap h show s ven tricu lar g rad e acc ord ing to sex , rac e, an d age . (6 ) G rap h

sh ow s w hite m atte r g rad e ac cord in g to sex , rac e, an d ag e.

En tire C HS Coho rt

T a b le 3

D is t r ibu t ion of M R

Im ag in g F ind ings in th e H ealth ier

S u b g ro u p

65 -69 Y ears 7 0-7 4 Y e ars 7 5-7 9 Y ea rs 80 + Y ear s

W om en M en W o m e n M en W om en M e n W om en M e n

(% ) (% ) (% ) (% ) (% ) (% ) (% ) (% )

0 0 0 0 0 0 0 0

1 2 .1 2 .9 4 .0 0 .8 0 .9 0 .7 0 .8 0

46 .2 19 .1 3 2 .0 16 .3 24 .3 1 1 .4 1 5 .7 4 .6

78 . 0

63 .2 6 8 .6 51 .0 60 .4 41 .4 47 .5 20 .7

95 .5 8 6 .8 9 1 .9 86 .5 9 1 .4 76 .4 77 .9 56 .3

99 .2 98 .5 9 6 .1 94 .7 96 .9 92 .9 91 .0 85 .1

99 .2 10 0 .0 9 8 .7 9 8 .4 9 9 .6 98 .6 % .6 % .6

100 .0 N A 9 9.1 99 .6 1 00 .0

99 .3 99 .2

98 .9

N A N A 9 9.6 99.6 N A 10 0.0 100 .0 100 .0

N A N A

1 00 .0 1 00 .0

N A N A N A N A

0 0 0 0 0 0 0 0

6 .1 4 .4 2 .9 2 .0 3 .2 0 .7 1 .6 0

47 .7 26 .5 3 6 .9 2 0 .8 27 .5 15 .7 1 9 .7 8 .1

79 .6

7 0 .6 6 8 .1

54 .3

6 3 .5 53 .6 50 .0

26 .4

96 .2 91 .2 8 9 .7 8 2 .0 8 5 .6 80 .0 79 .5

60 .9

97 .7 97 .1 9 8 .9 9 5 .9 9 8 .2 95 .7 95 .1 8 7 .4

100 .0 100 .0 9 9 .6 9 9 .6 1 00 .0 99 .3 10 0 .0 96 .6

N A N A 1 00 .0 1 00 .0 N A 100 .0 NA 100 .0

N A N A N A N A N A N A N A N A

N A N A N A N A N A N A N A N A

8.3 11 .9 6 .8 6 .1 1 .4 4 .3 1 .6 1 .2

6 7 .4 5 5 .2 4 2 .4 47 .4 2 3 .9 37 .9 20 .2

23 .3

87.1 82.1 7 5 .9 78 .4 58 .1 70 .7 53 .2 53 .5

97 .0 97 .0 9 2 .9 9 1 .8 8 5 .1 85 .7 76 .6 74 .4

98 .5 98 .5 9 6 .3 9 7 .1 91 .4 95 .7 90 .3 8 0 .2

99 .2

100 .0 9 8 .2 9 8 .0 9 5 .1 97 .9

96 .8

89 3

100 .0 NA 9 9 .3 9 9 .2 96 .9 99 .3 99 .2 96 5

N A N A 9 9.6 100 .0 9 9 .6 1 00 .0 10 0 .0 97 .7

N A N A 100 .0

N A 99 .6 N A N A 9 8.8

N A N A N A N A 1 00.0 N A N A 1 00.0

Note -Numbe r s are cu m u la tive p er cen tag es. N A = n o t a p pl ic a bl e.

(ie, those ex clu ded from the h ealth ie r egories. T ab le 4 , a sum m ary of the

sub group ) a fte r ad justm en ts w ere m ad e in fo rm ation in T ab le 3 , lis ts on ly the

fo r sex , age , an d race . W hite m atte r p at- g rade ca tegory tha t con ta ins the 95 th

tern (pe riven tricu la r v s subcortical) an d pe rcen tile fo r su lca l, ven tr icu la r, and

brain s tem in vo lvem ent w ere sim ilar to w h ite m atte r g rades .

th ose seen in the w ho le group . S u lcal

g rade w as on ly m arg in ally d iffe ren t

(0 .08 low er in the hea lth ie r pop u lation ) .

T ab le 3 lis ts the d istribu tion s of each Su lca l E n la rg em en t

grad ed v ariab le and sh ow s the m ax i- W iden in g o f the su pe rf ic ial su lc i

m um va lue and the cu m ula tive pe rcen t- has long been n o ted (12 ) in the e l-

age a t each grade leve l fo r the age ca t- de rly b ra in a t g ro ss pa tho log ic in spec- a re con sisten t w ith d ata fro m ou r p i-

D I S C U S S I O N

V olu m e 202

{ 149}

u m b er 1

Radio logy { 1 4 9 }7

4. 5

4.0

3. 5

3.0

. 2.5

2.0

C,

1.0

0.5

0.0

G r a d e

V e n t r i c u l a r

0

2

3

4

5

6

7

8

9

Sulca l

0

2

3

4

5

6

7

8

9

W hite m atter

0

2

3

4

5

6

7

8

9

5.0

4 .5 4 .0

4 .0 3 .5

3 .5 3 .0

4 ) 3 .0

#{149 }0 2 .5

2.5 0

(

2.0

f

. 2. 0

1 .5 . ( 1 .5

1 .0 U # {1 49}0+ 1 .0

0 .5 7 5 .7 9 0 .5

0.0 .

_:_w

7 0 .7 4 5 )

o .o

N F B F 55 .69 4

All

tion

an d h as been attr ibu ted to w hite

m atte r lo s s becau se the co rtica l v o l-

u m e , in so m e stud ies (13 -1 5) , d id no t

seem to ch ange w ith age . T h is h as

been b orne o u t in m any large stud ies

(16 ,17 ) in w hich C T w as used to de -

sc r ibe d ila tatio n o f the su lc i af te r th e

6 th decad e. T h e chan ge in su lcal en -

la rgem en t m ay be a fun ctio n of age -

re lated d ec rease s in cereb ral b loo d

flow (18 ,1 9 ) .

In p rev iou s stu d ie s (17 ,20 ), su pe rf i-

c ia l su lca l s ize w as g raded w ith fo u r-

o r f ive -po in t sca le s , an d in te robse rve r

varia tion w as s im ila r to tha t o bse rv ed

in our s tu dy . T h is in te robse rver v ar ia -

lio n w as also ve ry sim ila r to th a t

n o ted in our p ilo t M R im ag ing stud y

(8 ) , a lth ough th e n um ber of readers

in creased fro m tw o to six and the

n um b er o f s tud ie s in creased ten -fo ld .

T he u se o f cen tra l su lcus w id th is

com plem en ta ry to th e sem iq uan tita -

f ive g rad ing sy stem . P rio r reports

h av e c ited d isp ro portion ate w iden in g

o f the supe rf ic ial su lc i (12 ) and an te -

n o r end s o f the sy lv ian fissu re s (1 4 ) in

th e fron tal lo bes w ith ag in g . W e chose

to m easu re the cen tra l su lcus b ecause

iden tifica tion is fairly accura te (21)

and m eth ods o f lo ca lizatio n a re w e ll

know n (22 ,23 ). T he cen tra l su lcus

w id th co rrela ted c losely w ith su lcal

grade .

T he c lear sex d iffe rence in su lcal

grad e (g rade in m en

g rea ter than

grad e in

w om en ) fo r bo th the coho rt

and th e hea lth ie r su bgrou p depa rts

fro m the re su lts o f p rev io us stud ies

(16 ) . O n c lose r exam ina tion , h ow eve r,

th e sub jec ts in th ose p rev ious stud y

groups w ere predo m inan tly fem ale .

In tw o stu d ie s (2 ,20 ) w ith a m ore

equ iva len t rep re sen ta tio n of m en and

w o m en , inc rea sed su lca l vo lum e in

m en w as reported .

R ac ia l d iffe rences in su lca l s ize have

been p oorly add re ssed in the litera -

tu re . O ur f ina l re su lts from the coho rt


6/738 { 1 4 9 }adio logyJanuary 1997

lo t stud y (5 ) (w hich con ta ined , by de-

s ign , a h ig h percen tage of partic ipan ts

w ith c lin ical trans ien t ischem ic a ttack

and s troke) and su gges t tha t no nb lack

race is sign ifican tly assoc iated w ith

inc reased ven tricu la r and su lca l g rade .

T h e racia l d iffe rences fo r ven tricu la r and

su lcal g rade d isappear in the hea lth ie r

subgro up . H o w ever, th is d isappearance

m ay b e partly a resu lt o f d ec re as ed

pow er du e to the sm alle r sam p le s ize

(1 ,488 in the hea lth ie r sub group vs

3 ,660 in th e en tire co hort). It is

no t

su rpr ising th at su lcal g ra de c orrela tes

w ith ven tricu lar g rade afte r co n tro l-

ling for ag e, s ex , an d ra ce, b eca use

b o th re flect cereb ra l a trophy .

V en tr icu la r E nla rgem en t

Inc reases in ven tricu la r vo lum e

w ith age are w ell know n from repor ts

o f h is to pa tho log ic (24 ,25 ) an d rad io -

log ic s tud ies (17 ,26 ,2 7). T he da ta a re

so m ew hat co nflicting , w ith the au-

thors of som e s tud ies (16) repor ting

th at the ven tric les en la rge w ith nor-

m al ag in g faste r than do th e su lc i and

o thers (26) s ta ting tha t d isp rop ortion -

a te v en tr icu la r en la rgem en t is com e-

lated w ith dem entia.

T he lite ra tu re is a lso d iv id ed m e-

gard ing sex d if fe rences in la te ra l yen-

tricu la r en la rgem en t; th e repo rted

d iffe rences range fro m n o sex d iffe r-

ence (16) to la rg er ven tric les in m en

(18 ,22) and an in crease in th e s lope of

th e reg ression line w ith age in m en

(14 ,23). So m e au thors (2 ) have sug-

gested th at fem ale sex h orm on es o t

o the r sex -spec if ic n eu ra l subs tra tes

m ay pro tec t the brain durin g ag ing .

T he resu lts o f u r p ilo t s tu dy (5 ) p re -

saged our fina l resu lts

of

grea te r yen-

tn icu la r size in m en in b o th the coh ort

an d the hea lth ie r subgro up afte r con -

tro lling fo r age .

N on b lack m ace w as assoc iated w ith

h igher v en tr icu la r g rade

in

the coh ort

(consisten t w ith d ata fro m the p ilo t

s tudy 1 5 1 ) bu t n o t in the hea lth ie r sub-

g roup . T h is d iffe rence be tw een da ta

from the hea lth ie r subg roup and d ata

from

our p i lo t study is a gain pro ba b ly

due to the se lection b ias

of

the p ilo t

stud y , w h ich include d hig h pe rcen t-

ages of perso ns w ith transien t isch -

em ic attack an d strok e.

T he use o f the fro n ta l h orn ratio as

a m easure of v en tricu la r en la rg em en t

w as fir st desc ribed , in 1976 , by H ahn

and R im (28), w ho used C T scans ;

th ey fou nd a rang e in vo lun tee rs and

pa tien ts (ag ed 10-8 1 years) o f 0 .19 -

0 .39 . O ur rang e w as 0 .1 9-0 .55 w ith a

m ean of 0 .33 . T he fron ta l horn ra tio

w as fo und to corre la te c lose ly w ith

ven tricu la r g rade .

W h ite M atter C h an g es

H ypen in tens ity o f pen iven tn icu la r

an d sub co rtica l w h ite m atte r h as a lso

been sho w n to increase w ith age in

m any prev iou s s tud ies (1 ,29 -31). P os-

tu la ted causes inc lude subepend ym al

g lios is (32) an d a troph ic pen ivascu la r

d em yelina tion (33) . P rev ious stud ies

(34 ) have a lso show n, as o ur stud y

d oes, tha t w hite m atte r chang es con-

re la te w ith ven tricu la r s ize; co rre la-

tions w ith su lca l s ize a re less p red ic t-

ab le . In our m od el, su lca l g rade is no

long er sign ifican tly assoc ia ted w ith

w hite m atte r g rade once ven tricu la r

g rad e is en te red in the m ode l. D esp ite

th is lack of asso cia tion , w hite m atte r

changes have been show n to be inde-

penden tly co rre lated w ith im pa irm en t

o f subcortico fron ta l func tions (4 ,1 1).

A lth ough prev iou s s tud ies (1 ,4 )

have show n som ew hat inc reased

w hite m atte r changes in w om en corn -

pared w ith m en , th ose d if fe rences

w ere no t sta tistically sign ifican t. In

ou r stud y , w om en h ad sign ifican tly

h igher w hite m atte r sco res in bo th

the en tire im aged C H S coh ort P =

.0 064) and the hea lth ier subg roup

P

= .000 8). T h is is in con trad is tin c-

tio n to the preva len ce of in fa rc tlike

lesions , w hich is h igh er in m en (9 ).

T hese sex d iffe rences in the p reva-

lence of w hite m atte r sign al in ten sity

changes and th at o f in fa rc tlike les ions

a re no t fu lly un derstoo d a t th is tim e

bu t a re p robab ly re la ted to subpo pu-

la t ions of in fa rc tlike les io n , pa rticu -

la rly m ajo r-vessel in fa rc tlike les io n ,

co rtical in fa rc tlike lesion , and sub cor-

tica l in fa rc tlik e les ion . T h e la tte r m ay

be m ore c losely re la ted to w hite m at-

tem signa l in tens ity ch an ges, a lthough

th is is specu la tio n.

It is in trigu ing tha t n onb lack race

is s ign ifican tly assoc ia ted w ith less

w hite m atter ch an ge in bo th th e co -

hor t P = .0032) and the h ea lth ie r su b-

g roup (P= .0 201).

T he preva len ce of w hite m atte r

ch anges (g rades 2 -9 ) in ou r e lde rly

co hort (65 .3% [2 ,368 of 3 ,628J) and in

oU r hea lth ie r sub group (60 .2% [884 of

1 ,469 ]) is h ig her than the preva lence

repo rted in tw o recen t po pu la tio n -

based s tu d ies (3 ,35) o f e ld e rly per-

sons, w h ich c ited a preva lence o f

ch anges in 27% an d 3 8% , resp ec-

tive ly , o f the ir sub jec ts. T h is d isc rep -

anc y is pro bab ly th e resu lt o f o ur use

of a m o re d isc re te g rad in g sys tem

an d a low er th resho ld fo r record in g

changes .


T ab le 4 m ay be used as a gu ide fo r

the c lin ic ian in de te rm in ing w here

T ab le 4

D istr ib u tion of M R im a gin g F in d in g s

a ccord in g to S ex an d A ge in th e

H ea lth ie r S ub gro up

65 -69 70 -74 75 -79

80 +

S ex Y e ars Y e ars Y e ars

Y e a r s

S uIc aI gra de

W om en 4

5

5 5

M en 5 5 5 6

V e n t r i c u l a r

gra de

W om en 4 5 5 6

M en

5 6 6

6

W hite m atte r

g r a d e

W om en 3 4 5

5

M en 3 4 4 6

N ote-N um bers are grade c ate gory co ntain -

in g the 95th pe rcen tile fo r th e gra de d va riab les .

any g iv en e lderly in d iv idua l’s M R

im ag in g find in gs lie in co m parison

w ith the find ing s in ou r hea lth ie r su b-

p opu la tion of com m u nity -liv ing peop le

o f s im ila r ag e and sex . F or exam ple , a

7 6-year-o ld w om an w ith a w hite m at-

ten grad e of 2 w ou ld b e near the m e-

d ian fo r h er age . A w hite m atte r g rade

of 5 w ou ld b e g rea ter th an tha t seen

in 9 5% of her p eers and m igh t sug-

gest causes o ther than in creas ing ag e.

H o w ever, w e cau tion aga ins t use of

the w ord

‘ ‘

abnormal’

‘

fo r g rades

above th is 95 th percen tile.

T h e C H S cohort o ffe rs an oppo rtu -

n ity to exam ine la rge num bers o f re la -

t ively

h ea lthy , e ldem ly ind iv idua ls. B y

u sing a s tand ard ized im ag ing pro to -

co l and read in g tech n ique , a la rge

d atabase h as been accum ula ted of the

M R im aging app earance of the bra in

in 3 ,660 persons ag ed 65 years and

o ld er . T he d is trib u tio n tab les p re-

sen ted fo r the hea lth ie r subgro up

(T ab les 3 , 4 ) can he lp de te rm ine the

c lin ica l im portance o f a troph y and

w hite m atte r sign al-in tens ity chang es

a t cran ia l M R im aging of an e lderly

asym ptom atic ind iv idua l. #{149}

A ck n o w le d g m e n ts : W e th an k th e p rin cip a l

staff at th e pa rtic ipa ting in stitu tio ns : G re gory L .

B urk e, W a lter H . E tt ing er, C u rt D . F u rbe rg , E d -

w ard H a po nik , G era rdo H eiss, D a lan e K itzrnan ,

H . S id ne y

K lo pfens te in , M a rgie L a m b, D a vid S .

L efk ow itz , M ary F . L y le’s , M a urice B . M itte l-

m a rk, C ath y N u nn, W a rd R ile y , G re the S . T e ll,

Jam es F . T oo le , B ev erly T u cke r, K ris C alho un ,

H arry C a lhou n, F a rid a R a utah arju , P e ntti R au-

ta har ju , L ora lee R o ber tson (B ow m a n G ray

S ch ool o f M edicin e, W ak e F o res t U n ive rsity ,

W inston -S ale m , N C ); W illia m B um m er, C ha rles

B ern ick , A nd rew D ux hury , M ary H aan , C alv in

H irsc h , P a ul K elle rm a n, L a w ren ce L aslet t, M a r-

shal l L ee, John R ob bin s, M arc S c hen ke r, N em at

B orh an i (U niv ers ity o f C a lifo rn ia-D av is, S acra-

m en to); M . Jan B usb y-W hiteh ead , Joyc e C hab ot,

G eo rge W . C om sto ck , L in da P . F ried , Jo el G .

H ill, S te ve n

J {149}

ittn er, S h irik i K u m a ny ika , D a vid

L e vin e, Joa o A . L irn a, N eil R . P o w e, T ho m as R .


7/7

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