Neonatal Intracranial Ischemia and Hemorrhage

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Neonatal Intracranial Ischemia andHemorrhage :Role of Cranial Sonography and CT

ScanningImran Ahmad Khan, M.D.,1Shagufta Wahab, M.D.,1Rizwan Ahmad Khan, M.S., M.Ch.,2Ekram Ullah, M.D.,1Manazir Ali,

M.D.3Department of Radiodiagnosis,1 Division of Pediatric Surgery,2 Department of Pediatrics,3 JNMCH, M!, "igar#, $ndia J Korean Neurosurg Soc 47 : 89-94, 2010!"ecti#e : To evaluate the role of cranial sonography and computed tomography in the diagnosis ofneonatal intracranial hemorrhage andhypoxic-ischemic inury in an !ndian set-up"$ethods : The study included 100 neonates #ho under#ent cranial sonography and computed tomography$%T& in the 'rst month of life forsuspected intracranial ischemia and hemorrhage" T#o o(servers rated the images for possi(le intracraniallesions and a )appa statistic forintero(server agreement #as calculated"

Results : There #as no signi'cant di*erence in the )appa values of %T and ultrasonography $+& for thediagnosis of germinal matrixhemorrhage.intraventricular hemorrhage $/.!& and periventricular leucomalacia $3& and (oth sho#edgood intero(server agreement"+, ho#ever detected more cases of /.! $24 cases& and 3 $19& cases than %T $22 cases and 1cases of ! and 3, respectively&" %Thad signi'cantly (etter intero(server agreement for the diagnosis of hypoxic ischemic inury $!!& in terminfants and also detected more cases$55& as compared to + $18&" %T also detected cases of extraaxial hemorrhages as compared to 1detected (y +"Conclusion : + is (etter modality for imaging preterm neonates #ith suspected ! or 3" o#ever, +is unrelia(le in the imaging of term ne#(orns #ith suspected !! #here %T or magnetic resonance image scan is a (etter modality"10"5540.)ns"2010"46"2"89

K%& 'R(S : ypoxic ischemic inury 7 +ltrasonography 7 %T-scan"

Clinical )rticle%opyright 2010 The orean eurosurgical ocietyrint ! 200;-5611 <n-line ! 1;98-686

INTR(*CTINeonatal intracranial hemorrhagic and hypoxic lesionscan (e divided as those occurring in the preterm and in theterm infants" !n the preterm, the maor lesions are germinalmatrix hemorrhage $/&.intraventricular hemorrhage$!& and periventricular leucomalacia $3&15,18&" !n theterm infants the maor pro(lems are hypoxic-ischemic encephalopathy.inury $!!& and intracranial hemorrhage1,11&"!ntracranial hemorrhage is uncommon in term infants and#hen it occurs is generally unrelated to the germinal

matrix21&

" +ltrasonography $+&, computed tonography$%T& and magnetic resonance image $/=!& are (eingroutinely used to screen the neonate for pro(a(le intracranialpro(lems1;,16,19,24&" >et, only fe# studies have attemptedto compare the role of various imaging modalities in thesetting of speci'c neuroimaging 'ndings vi?" hemorrhagicand ischemic lesions in preterm and term infants" The purposeof our study #as to compare the relative role of cranialsonography and %T in the diagnosis of hemorrhagic and



ischemic events in preterm and term infants@ and there(yattempt to determine #hich modality is (etter suited fordetection of a particular lesion" Ae did not include /=! inour comparative study as /=! is not availa(le in most of the !ndian setup, especially at the periphery" Blso, most of the neonates are too sic) to (e investigated (y /=!" Curthermore,

cost concerns preclude the use of /=! in many cases" The advantages of + are that it is easily availa(le, cheap,Duic) and easy to perform and can (e done at the (edside"Blso, it does not use ioni?ing radiation" o#ever, sonographydoes not di*erentiate su(arachnoid from su(duralhemorrhages and it is also unli)ely that a small corticalhemorrhage #ill (e detected12&" !t is relatively insensitive toalteration in (rain tissue perfusion and to acute !!5,22&"E =eceived : /arch 2;, 2009 E =evised : ovem(er 14, 2009E Bccepted : Fecem(er 29, 2009E Bddress for reprints : =i?#an Bhmad han, /"", /"%h"Fivision of ediatric urgery, Fepartment of ediatrics, G/%, B/+,4.816-C, " " agar, agla =oad, Bligarh, +"", !ndia

Tel : H91-9410210281, Cax : H0;61-2621126I-mail : drri?#anahmad)hanJyahoo"co"in

+,online /3 %omm

The advantages of %T include its easy availa(ility and highspatial resolution" %T provides excellent anatomic resolutionof the entire (rain parenchyma" Blso, it is not operatordependent, relatively cheaper and can (e more rapidlyperformed as compared to /=!" %T can relia(ly distinguish(et#een su(dural and su(arachnoid (leed, #hich isdiKcult on sonography12&" o#ever in premature infantsthe role of %T for the documentation of acute hypoxicischemic(rain inury is limited" igh #ater content of thepremature (rain precludes the use of decreased attenuation

as an index of cere(ral edema" %T contri(utes signi'cantlyto total radiation dose derived from medical imaging inchildren" Bt present, the (est radiologic modality to evaluatethe (rain in infants and children is /=!" There are no)no#n (iological ha?ards and no ioni?ing radiation, and itproduces exDuisite anatomic detail of the central nervoussystem $%&" /=! has greater sensitivity and speci'cityfor the detection of perinatal !! than either ultrasound or%T" Thus, early T2 prolongation on standard /=! #ithin12 to 18 hours after inury appears to correlate #ith edema,#hereas T1 shortening after 5 days and T2 shortening after-6 days correlates #ith permanent (rain damage10,24&"$)T%RI)-S )N( $%TH(S<ur study #as conducted from Ganuary 200; to Fecem(er200, in the Fepartment of =adiodiagnosis, G""/edical %ollege and ospital, B/+ on 150 neonatesreferred from the eonatal +nit of our hospital #ith clinicalsuspicion of intracranial ischemia or hemorrhage" !nformedconsent #as o(tained from the parents of thepatients included in the study" %ranial sonography and %T#ere then performed #ithin 48 hours of each other" <f



these %T could not (e performed in 1; patients and in 14patients the interval (et#een %T and + #as more than48 hours due to various reasons and so they #ere excluded"<f the remaining 101 infants #e chose 100 as the studysi?e, for the ease of calculations" The study included ;4preterm and 4 term infants" There #ere ; males and 44

females" !maging #as performed at 10-14 days of age, asrecommended (y Loal et al"4& B detailed clinical evaluation#as done including general physical examination andneuro-logical examination" %linical data included estimatedges-tational age $LallardMs&, (irth #eight, 1 and ; minuteBpgar scores, mode of delivery, age at imaging and time(et#een sonography and %T" The relevant la(oratoryinvestigations li)e serum electrolytes, arterial (lood p andp<2, and serum (iliru(in #ere carried out #henever reDuired"

The follo#ing exclusion criteria #ere ta)en into account :1& atients #ith )no#n congenital % malformations"2& atients #ith meningitis"5& atients in #hom sonography and %T could not (eperformed #ithin 48 hours of each other"Imaging%ranial sonography #as performed #ith a Toshi(a Camio8 mart +ltrasound machine using multifreDuency 4 /?and /? electronic curvilinear array pro(es" Iight /?and 12 /? linear high freDuency pro(es #ere also usedto detect any possi(le extraaxial Nuid collections" tandardimages in sagittal and coronal planes #ere o(tained throughthe anterior fontanelle" osterior sagittal and coronalvie#s #ere o(tained via the posterior fontnelle, #heneverreDuired" on-contrast %T #as done using iemens omatomLalance single slice helical scanner using the seDuence

mode at 120 )e, 120 mBs, and 1"; second scan time peracDuisition@ ; O ; mm contiguous axial scans #ere o(tained"=educed tu(e current settings #ere used20& to reduce meanradiation dose to the patient"Image analysisBll sonograms and %T images #ere separately and independentlyrevie#ed (y t#o senior radiologists #ho #ere(linded to patient history and previous radiology reports"

The images #ere assessed for the follo#ing a(normalities :germinal matrix hemorrhages $/&-rades ! through !,including intraventricular hemorrhages $!& and parenchymalextension $I& $Lurstein apile et al"6& classi'cation#as used&@ non-matrix related hemorrhages including intraparenchymalhemorrhage $!& and extraaxial $su(dural.su(arachnoid.epidural& hemorrhage@ !! of the cortex,(asal ganglia, (rainstem, thalamus or cere(ellum@ and earlyand late $cystic& 318&" Iach a(normality #as scored on ascale of 1-; $1 P de'nitely not present, 2 P pro(a(ly notpresent, 5 P indeterminate, 4 P pro(a(ly present, ; P de'nitelypresent&" Bn a(normality #as considered present if thecollective score of the t#o o(servers #as at least 8"Statistical analysis



Cor each techniDue, possi(le 'ndings from the examinationsof the participants #ere rated as one of 've categories1 to ; (y the t#o o(servers" The )appa statistic for multipleratings per participant #as used to measure intero(serveragreement8,25&" appa #ith linear #eighting #as used insteadof un#eighted )appa as used erroneously (y previous o(servers;,&"

ypothesis tests #ere evaluated as statistically signi'cant#hen p values #ere less than 0"0;" %omparison of )appa statistics (et#een imaging techniDues #as conductedusing the ? test" Ahen t#o techniDues #ere compared, thetechniDue #ith statistically higher )appa value #as consi-

J Korean Neurosurg Soc 47 .February 2010

,/dered to (e more accurate for the detectionof a speci'c imaging 'nding"R%S*-TS

T#enty-four cases of germinal matrix.intraventricular hemorrhages, 10 casesof non-matrix related intracranial hemorrhages,

55 cases of !! in term infants and 19 cases of !! in preterm infants $3& #ere o(served as per Ta(le 1"0reterm infants<ut of the ;4 preterm infants, 24 su*ered from germinalmatrix.intraventricular hemorrhages $Cig" 1&, 19 su*eredfrom 3 and patients had extra-axial hemorrhages, 2patients of 3 also su*ered from intraparenchymal hemorrhages#hich #ere not related to germinal matrix"

T#enty of the 24 cases of ! $85Q& and 15 of the 19 casesof 3 $8Q& #ere seen in preterm infants of R 52 #ee)sof gestational age" + detected 24 cases of /.!#hile %T detected 22 cases@ 2 cases of grade ! ! (eing

missed on %T $Ta(le 2&" Blthough the )appa values of %T$0"8;44& #ere found to (e higher than + $0"6864&, thedi*erence #as not statistically signi'cant" There #ere 15cases of early 3 and cases of cystic 3 $Cig" 2-;&"+ detected 19 cases of 3 #hile %T detected only 1"Loth %T and + ho#ever detected all the cases of cystic3" The )appa values of + #ere found to (e higherthan %T particularly for early 3" The di*erence #asho#ever, not signi'cant" Thus the sensitivity of %T relativeto + for the diagnosis of ! and 3 #ere 91"6 and82"6;Q respectively" + #as una(le to detect only 1 of the cases of extra-axial hemorrhages #hich #ere revealed(y %T, indicating that sonography has poor sensitivity in

the detection of extra-axial hemorrhages $"2Q&" Curthermore,t#o small intra-parenchymal hemorrhages of thesi?e a(out 1 cm #ere missed on + and #ere detectedonly on %T"Term infants+ revealed 18 cases of !! as compared to 55 detected(y %T $Ta(le 5&" Bdditionally, + diagnosed seven falsepositive cases #hich #ere reported as de'nitely negative on%T, thus the sensitivity and speci'city of + relative to



%T #ere only ;;";Q and 62Q respectively" /oreover,)appa values of %T $0"662& #ere signi'cantly higher thanthe corresponding values of + $0";594& for the diagnosisof !! $ p R 0"01&" T#o cases of intracranial (leed #ereseen in term infants in our study, #hich #ere relia(ly diagnosed(y (oth %T and +"

(ISC*SSINLla)en(erg et al";& had previously compared the eKcacyof + relative to %T and /=! for the diagnosis of ischemiaand hemorrhages" o#ever, their study #as small $n P46& and there #as no adeDuate representation of pretermImaging in Neonatal Intracranial Ischemia . IA Khan, et al.

,1Ta!le 12 Spectrum of findings" no" Cindingsum(er of cases detected on%ranial sonography %%T head1 /.! 24 222 on-matrix hemorrhages 5 105 eriventricular leucomalacia 19 1

4 ypoxic-ischemic inury 18 55/.! : germinal matrix hemorrhage.intraventricular hemorrhage

3ig2 12 Ultrasonography and computed tomography of a neonate showing

B/L grade III germinal matrix and intraventricular hemorrhage with

hydrocephalus.

Ta!le 2 CT and USG of intracranial bleed in preterm infantsCinding of o" of patients detected (y/.! onography %%Trade ! 05 01rade !! 09 09rade !!! 09 09rade ! 05 05/.! : germinal matrix hemorrhage.intraventricular hemorrhage

3ig2 2 Early periventricular leucomalacia : ultrasonography shows increased

echogenicity in B/L frontal and left parietal region.

infants in their study" Ae had ;4 preterm and 4 terminfants in our study and #e #anted to compare the eKcacyof + relative to %T in each su(group" !n preterm neonates,out of the 54 cases of intracranial hemorrhages, 24#ere germinal matrix related" /aority of the cases of !$85Q& #ere seen in the preterm neonates of less than 52#ee)s gestational age" + fared #ell in the diagnosis of /.! and detected more cases than %T $24 as against22 detected (y %T&" This 'nding #as also seen (y previouso(servers;,&" The t#o cases that #ere missed (y %T #ere of unilateral grade ! /" Blso, (oth %T and + sho#edexcellent intero(server agreement in the diagnosis of grade !to ! !, #ith )appa values of %T $) P 0"8;44& (eingslightly greater than + $) P 0"6864&" The di*erence,ho#ever, #as not statistically signi'cant" Thus, + should(e the preferred modality for the screening of ! o#ing toits (etter and excellent intero(server agreement"%T #as found to (e more sensitive in detecting extraaxialhemorrhages, and detected cases of su(dural (leed ascompared to only 1 detected (y +" This 'nding #asalso noted (y previous o(servers2,;,,14&" %T #as also (etter



in detecting non-matrix related intraparenchymal hemorrhagesand detected 4 of them" + sho#ed poor sensitivityand #as una(le to detect 2 of these cases #here hemorrhage#as less than 1 cm in si?e" Thus, our study sho#s that+ is not relia(le in the detection of non-matrix relatedhemorrhages"

!n preterm neonates, 19 cases of periventricular leucomalacia#ere o(served in our study, cases #ere of cystic3 and 15 of early 3 $L.3 periventricular echogenicityon +&" Ae found it diKcult on %T to di*erentiate lo#attenuation due to 3 from normal lo# attenuation seenin premature (rain" Bs a result, %T had lesser $though notstatistically signi'cant& )appa values than + for thediagnosis of 3, particularly early 3 $Ta(le 2&" There#ere three such cases #here the diagnosis #as missed on%T-scan $early 3&" onography on the other hand sho#edgood sensitivity and intero(server agreement for thediagnosis of early 3" Bll the cases of cystic 3 #ere,ho#ever diagnosed relia(ly (y (oth modalities" ence,sonography should (e the imaging modality of choice forthe detection of early 3" o#ever, once cystic changesdevelop after 1-5 #ee)s, (oth modalities can diagnose 3#ith eDual precision"!n term neonates, cranial sonography detected only 18cases of hypoxic ischemic inury out of 55 detected (y %T"Cocal ischemic lesions appeared on + as locali?ed areasof varia(ly increased echogenicity" o#ever, interpretationof this increased echogenicity #as relatively su(ective and anum(er of cases $6 cases& #ere reported as having suspiciousareas of increased echogenicity #hich #ere termed asde'nitely negative (y %T $false positive&" !t #as particularly

diKcult to diagnose on + cases #here there #as a generali?edincrease in echogenicity of (ilateral cere(ral hemispheres$glo(al ischemia&" Blso + #as not a(le to detect

J Korean Neurosurg Soc 47 .February 2010

,Ta!le 52 USG and CT findings in cases of hypoxic ischemic injury in

term infants" no" Cindings + %T1 Cocal./ultifocal cere(ral infarcts 9 1;2 lo(al ischemic changes 1 45 %ystic encephalomalacia 4 44 %ere(ellar infarcts 0 2; Lasal ganglia !nfarcts 5 4 Thalamic infarcts 1 26 Lrainstem infarcts 0 2+ : ultrasonography

3ig2 42 Computed tomography of a patient showing cystic periventricular

leucomalacia.

3ig2 62 Ultrasonography of same patient showing cystic periventricular

leucomalacia.

3ig2 52 Early periventricular leucomalacia: computed tomography of the

above patient shows low attenuation of white matter in B/L frontal and

parietal regions. A small focus of bleed is seen in right frontal region.

any of the cases of (rainstem and cere(ellar infarcts $Ta(le



5&" The intero(server agreement of + $) P 0";594& #assigni'cantly lo#er than %T $) P 0"662& $ p R 0"01& in diagnosisof !! in term neonates" The di*erence (et#eenultrasound and %T for the detection of cortical !! couldnot (e explained (y progressive evolution of ischemicinury (ecause there #as a narro# #indo# of time (et#een

the performance of each examination $#e performedcranial sonography and %T #ithin 48 hours of each other&"

Thus, + faired poorly in the diagnosis of !! in termneonates" The superiority of %T for the detection of !!has (een suggested (y several investigators2,14&" The study#ith +-pathology correlation has demonstrated lo#sensitivity $28Q& in the detection of pathologically proven!!-associated lesions in neonates" o#ever, 9 infants #ithstrong clinical evidence of !I $lo# 1 and ; min Bpgarscores& turned out to (e normal at the time of %T scan, implyingthat presence of normal scan at %T and sonographydoes not entirely rule out neurological insult in the a*ectedneonate" <ther imaging techniDues such as functional anddi*usion-#eighted /= imaging, positron emission tomography,single photon emission computed tomography and/= spectroscopy may prove to (e more useful in the detectionof regional cere(ral (lood No#.perfusion or meta(olicdistur(ances to precisely de'ne the extent of inury andthus predict future neurodevelopment outcome"<ur study did not address the issue #hether serial +examinations could provide the same diagnostic informationas %T" The changes associated #ith the evolution of /.! and !! that have (een o(served at serial +examinations can (e useful diagnostically" o#ever, thisaspect ignores the additive costs of multiple + examinations

and possi(le delay in diagnosis" Curther studies needto (e conducted to compare (oth conventional and ne#erneuroimaging techniDues #ith respect to cost (ene't issues"CNC-*SIN%ranial + examination provides a relatively sensitiveand highly speci'c means of detecting ! and should (eemployed in screening preterm neonates for ! and theintero(server agreement of %T is higher than + for thedetection of !, and can detect extra-axial hemorrhages#hich are li)ely to (e missed on +" /oreover, cranialsonography has greater sensitivity and intero(server agreementthan %T in the diagnosis of 3 $!! of premature(rain& and therefore should (e the preferred modality forimaging 3" !n term neonates, + fair poorly in thedetection of !! i"e", it has poor sensitivity, speci'city andintero(server agreement as compared to %T" Curthermore,%T is fairly precise modality for detecting !! of termneonates and should (e the mainstay in the imaging of term neonates, #here cost concerns or non-availa(ility precludesthe use of /=!"

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Neonatal Intracranial Ischemia and Hemorrhage