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Safety of Cerebral Digital Subtraction Angiographyin Children

Complication Rate Analysis in 241 Consecutive DiagnosticAngiograms

Ingrid M. Burger , BS; Kieran J. Murphy , MD; Lori C. Jordan , MD; Rafael J. Tamargo ,MD; Philippe ailloud , MD

+ Author Affiliations

1. From the Division of Interventional Neuroradiology (I.M.B., K.J.M., P. .!, the De"artment of Bioethi#s (I.M.B.!, the Division of Pediatri# Neurology ($.%.J.!, and the Division of %ere&rovas#ular Neurosurgery ('. .!, Johns )o"*ins +niversity, Baltimore,

Md.!. Corre"ponden#e $o Philippe ailloud, MD, Di%i"ion of In$er%en$ional&euroradiology, John" 'op(in" S#hool of Medi#ine, John" 'op(in" 'o"pi$al,)** & +olfe S$, Bal$imore, MD ! - . /0mail phg12hmi.edu

&e3$ Se#$ion

Abstract

Background and Purpose Catheter-based cerebral angiography remains an important

diagnostic tool in the pediatric population, particularly considering the currently growing interestin diagnosing and treating cerebrovascular disorders in children. There are no recent estimates of the complication rate associated with modern diagnostic digital subtraction angiography (D A!in the pediatric population. The purpose of this study was to estimate the rate of complicationsoccurring during cerebral angiography in children.

Methods Data from "#$ consecutive pediatric cerebral angiograms performed at a singleinstitution were entered into an institutional review board%approved database. &nformation on

patient demographics, D A indication, neurovascular diagnosis, and intra procedural and postprocedural complications was collected.

Results 'ur population included $$ boys and )* girls, with age ranging from $ wee to $years (mean D, $" years!. All angiograms were technically successful. o intraproceduralcomplication was noted/ in particular, there was no occurrence of iatrogenic vessel in0ury(dissection! and no transient or permanent neurological deficit secondary to a thromboembolicevent. 'ne child with a comple1 dural arteriovenous fistula e1perienced a fatal intracranialrehemorrhage secondary to a posterior fossa vari1 rupture 2 hours after completion of anuneventful diagnostic angiogram. The rates of intraprocedural and postprocedural complications
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were therefore *.*3 () 3 C&, *.*3 to $.#3! and *.#3 () 3 C&, *.*$"3 to ".")3!,respectively.

Conclusions The rate of immediate complications occurring during diagnostic cerebralangiography in children is very low. o intraprocedural complication was documented in the

reported series. D A performed by e1perienced angiographers is a safe procedure that can provide critical diagnostic information.

Key +ord"4 #a$he$er05a"ed angiography , #hildren , #ompli#a$ion"

4ecent advances in noninvasive neurovascular imaging techni5ues, including magneticresonance angiography (64A! and computed tomography angiography (CTA!, have reduced thenumber of catheter-based cerebral angiograms performed for purely diagnostic reasons. Digitalsubtraction angiography (D A! remains, however, the most accurate imaging techni5ue for evaluation of the cerebrovascular system. $ As such, D A continues to be widely used tocomplement partial or 5uestionable information obtained by noninvasive imaging means. &n

addition, new angiographic techni5ues, such as 2-dimensional D A, 2-dimensional digitalangiography, and 2-dimensional fusion D A, have further enhanced the diagnostic accuracy of D A. "% &n parallel with these technical advancements, constant improvements in angiographicdevices, such as wires and catheters, combined with the development of safer contrast agents,have continued to reduce the already low ris of complications associated with catheter-basedangiography. 7,8

The assumption remains, however, that catheter-based angiography is more challenging or dangerous in children. As a result, angiography is fre5uently delayed9if obtained at all9in thisage group, despite the fact that the information it would provide might be invaluable for timelyand accurate diagnosis and decision ma ing. The ris of an intraprocedural complication such as

stro e is obviously $ of the principal reasons preventing referring physicians from re5uestingcatheter cerebral angiography for their patients, along with the cost and availability of trained pediatric angiographers. This concern is, of course, legitimate and needs to be addressed by publication of the actual rates and types of complications associated with cerebral D A in the pediatric population. Availability of such information to both referring physicians andneuroradiologists is particularly important at the time of decision ma ing and parent counseling.Although earlier studies have already reported low complication rates for pediatric cerebralangiography, no estimation of the complication rate for modern diagnostic cerebral D A iscurrently available. This study e1amined the complication rate observed in a series of "#$consecutive diagnostic cerebral angiograms performed in "* pediatric patients at a singleinstitution between :anuary $))) and 6ay "**7.

Patients and Methods

Patient Population

This report is based on analysis of a pediatric neurovascular database approved by ourinstitutional review board (&4;!. The data selected for this review consisted of "#$ consecutivecerebral angiograms performed in "* children (age $ or less! at a single institution ( Table $ !.
http://stroke.ahajournals.org/search?fulltext=catheter-based+angiography&sortspec=date&submit=Submit&andorexactfulltext=phrasehttp://stroke.ahajournals.org/search?fulltext=children&sortspec=date&submit=Submit&andorexactfulltext=phrasehttp://stroke.ahajournals.org/search?fulltext=complications&sortspec=date&submit=Submit&andorexactfulltext=phrasehttp://stroke.ahajournals.org/content/37/10/2535.full#ref-1http://stroke.ahajournals.org/content/37/10/2535.full#ref-2http://stroke.ahajournals.org/content/37/10/2535.full#ref-6http://stroke.ahajournals.org/content/37/10/2535.full#ref-8http://stroke.ahajournals.org/content/37/10/2535.full#T1http://stroke.ahajournals.org/search?fulltext=catheter-based+angiography&sortspec=date&submit=Submit&andorexactfulltext=phrasehttp://stroke.ahajournals.org/search?fulltext=children&sortspec=date&submit=Submit&andorexactfulltext=phrasehttp://stroke.ahajournals.org/search?fulltext=complications&sortspec=date&submit=Submit&andorexactfulltext=phrasehttp://stroke.ahajournals.org/content/37/10/2535.full#ref-1http://stroke.ahajournals.org/content/37/10/2535.full#ref-2http://stroke.ahajournals.org/content/37/10/2535.full#ref-6http://stroke.ahajournals.org/content/37/10/2535.full#ref-8http://stroke.ahajournals.org/content/37/10/2535.full#T1


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TABLE 1. Patient Age Distribution

Age Group (in Years) No. of Patients

$ vascular lesion. The normal angiograms (n@ *! included patients undergoing a ADA test as

part of their presurgical wor up (n@2 ! as well as follow-up angiograms after successfultreatment of a vascular lesion.

ormal *Arterial stenosis occlusion $Dural cortical venous thrombosisCerebral aneurysm $2ascular malformation )2ascular tumor #ascular trauma 7'ther 7

Angiographi Proto ol

Arterial access was obtained in every patient via femoral puncture. A micropuncture set was usedin most cases, with the e1ception of some teenagers of adult siBe. onographic assistance wasre5uired for a few small children with no or barely palpable pulses. #= systems (arterial sheathsand diagnostic catheters! were used in almost all cases, whereas = systems were occasionally
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used in teenagers of adult siBe. Continuous flushing of the sheath with hepariniBed saline wasmaintained throughout the procedure (2* mE h, #*** heparin < E of normal saline solution!. A

bolus dose of heparin ($** < g, to a ma1imum of "***

compression. &n the vast ma0ority of cases, contrast agent in0ections were performed by hand.The ma1imum dose of contrast agent used in children under $7 years of age was " mE g. =orchildren >$7 years of age, the adult ma1imum dose of $8 mE was applied (though neverreached in this series!. &odi1anol ( isipa5ue 2"*, Amersham Fealth!, an iso-osmolar (")*m'smol g water!, nonionic, water-soluble, iodinated (2"* mg & mE! radiographic contrastagent, was used in most cases. A standard nonionic contrast agent (&ohe1ol, 'mnipa5ue 2**,Amersham Fealth! was used only in children >$7 years of age.

All angiography was performed in dedicated biplane neuroangiography suites. 6ost childrenwere investigated under general anesthesia. G1ceptions were represented by a few older children($7 years of age or above!, who were investigated under conscious sedation and local anesthesia,

and by children undergoing a ADA test, in whom either local anesthesia only (n@2#! or spinalanesthesia (n@$! was performed. 'utpatients were observed for a - to 7-hour period in theneuroangiography recovery area. Discharge evaluation in outpatients always included puncturesite status and femoral and distal pulses, whereas inpatients were chec ed during evening rounds.&n small children or in children unable to cooperate, the lower e1tremity used for arterial accesswas secured to a cushioned board to prevent, as much as possible, hip fle1ion.

Data A 'uisition

The " outcomes of interest in this study were the rates of complication of cerebral D A occurringduring the intraprocedural and immediate postprocedural periods. This information was ac5uired

prospectively and recorded into an &4;-approved pediatric neuroangiography database. &naddition, in consideration of the potential ris of delayed lower-e1tremity complications in the pediatric population, the parents or guardians of children H$$ years old were personallycontacted by phone (2 months to # years after the procedure! to in5uire about signs andsymptoms of such complications (eg, leg pain, wal ing difficulties, limping, or leg lengthdiscrepancy!. These interviews were the ob0ect of a separate approval from the &4;.

The information was stored and analyBed by commercially available database and statisticalsoftware (=ile6a er Iro 8, =ile6a er, anta Clara, Calif/ tata ), tata Corp EI, Collegetation, Te1!.

Results

ntrapro e"ural #o pli ations

All of the angiograms were technically successful. o intraprocedural complication was noted/in particular, there was no occurrence of iatrogenic vessel in0ury (arterial dissection! and notransient or permanent neurological deficit secondary to a thromboembolic event. There was no


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instance of contrast agent allergy and no evidence of contrast nephroto1icity. The rate ofintraprocedural complications was therefore *.*3 () 3 C&, *.*3 to $.#3!.

Postpro e"ural #o pli ations

'ne immediate postprocedural complication occurring 2 hours after the angiographic procedurewas observed (*.#3/ ) 3 C&, *.*$3 to ".")3!. A comatose 7-year-old girl transferred forinvestigation of a large temporal hemorrhage was diagnosed with a type & dural arteriovenousfistula of the right transverse sinus, with e1tensive cortical venous drainage. ubtotalemboliBation of the lesion was performed uneventfully, with e1cellent recovery and return to

baseline neurological e1amination (including cognitive slowing present before the acute event! atdischarge. A follow-up angiogram was obtained 7 months later because of recurrent periorbitalvenous engorgement and acute headache. The angiography was performed uneventfully andshowed new arteriovenous shunts in a nontreated segment of the transverse sinus, with drainagethrough a large posterior fossa vari1. The patient awo e from anesthesia without deficit but withslight nausea. Appro1imately 2 hours after angiography, she reported worsening of the nausea

and had an episode of vomiting, after which she complained of a sudden, severe headache and became comatose. Gmergent CT showed a posterior fossa hemorrhage at the site of the vari1.he was immediately brought to the operating room but died of uncontrollable hemorrhage.

*inor Postpro e"ural E+ents

Although no groin hematomas were observed, " minor events are worth mentioning here. &n $child investigated under general anesthesia and who was slightly hypothermic at the end of the

procedure, hemostasis of the femoral puncture site necessitated $ hour of continuous groincompression. 'ne 7-month-old baby had a minor lea from the femoral puncture site ?$ hourafter the end of the procedure, necessitating an additional "*-minute period of groin

compression. &n both cases, the follow-up was simple, without groin hematoma or othercomplications.

Dela,e" Lo-er E/tre it, #o pli ations in ! aller #hil"ren (Age 11 an"Younger)

The parents of #8 of the 8$ patients aged $$ and younger could be contacted by phone (77."3!.The median follow-up time was " months (range, to months!. o evidence of lower-e1tremity complication was reported (including leg pain, difficulty wal ing, limping, and leglength discrepancy!.

Pre%iou" Se#$ion &e3$ Se#$ion

Discussion

Despite the significant advances recently made in the field of noninvasive neurovascularimaging, cerebral D A remains the most accurate techni5ue for the diagnosis of vasculardisorders of the central nervous system .$ Although the number of diagnostic angiograms

performed for evaluation of carotid atheromatous disease has sharply decreased, this decline has
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been in part compensated by an increase in angiographic studies aimed at clarifying anomalies or suspicious findings revealed by 64A and CTA. &n our practice, this applies to the pediatric

population as well, with a steady increase in the number of re5uested studies documented duringthe past few years. The growing attention given to cerebrovascular disorders in children, a

population in which this type of diseases was, until recently, either ignored or considered with

undue fatalistic attitude, is certainly playing a role in this trend. This is clearly the case, in particular for the field of pediatric stro e. )%$" Fowever, if recent studies have established thesafety of diagnostic cerebral angiography in the adult population, 7,8 no recent study hasspecifically investigated the complication rates observed in children. &n adult patients, risfactors nown to significantly influence the rate of neurological complication during cerebralangiography have been identified, notably advanced age and the pree1istence of symptomaticatheromatous disease. &n $))#, Feiserman et al $2 reported a significant rate of permanent deficit(*. 3! but noted that all of the complications occurred in patients presenting with a history ofstro e, transient ischemic accident, or carotid bruit. Dion and coauthors $# similarly observed that,in their series, all permanent ischemia was the worsening of a pree1isting phenomenon. Thesefindings are consistent with the study of Cloft and colleagues, 7 who documented a *.*83 ris of

complication in patients investigated for aneurysms or vascular malformations. 6ost of the risfactors nown to have an influence on the rate of neurological complication during cerebralangiography, such as long procedures (>7* minutes!, use of a large volume of contrast agent,increased serum creatinine levels, symptomatic atheromatous disease, and studies necessitatingthe use of 2 or more catheters, are not usually, if at all, encountered in the pediatric population.Iediatric cerebral angiography is typically characteriBed by short procedures performed in

patients without atheromatous changes, with a low volume of contrast agent, and rarelynecessitating >$ catheter. &n small children, for e1ample, #-vessel cerebral angiography isroutinely performed with $ to "* mE of contrast agent and " to 2 minutes of total fluoroscopytime. The ris of a transient or permanent neurological deficit from an intraprocedural adverseevent, resulting from either a thromboembolic phenomenon or a traumatic mechanism, such asan arterial dissection, remains nonetheless the main factor contributing to the reluctance ofreferring physicians to consider catheter angiography in children. &n a study focusing solely oniatrogenic emboliBation during pediatric cerebral angiography published " years ago byIettersson and colleagues, thromboembolic events occurred in $# of $ $ children (*.)3/ ) 3C&, *. 3 to $. 3!, or *.#3 of the studied vessels ($# of 282$!. The authors emphasiBed themilder aspect of periangiographic thromboembolic events in the pediatric population whencompared with similar events occurring in adult patientsJ only $ child had transient neurologicalsymptoms (*.*73!, whereas there was no incidence of permanent deficit. They also noted thatthe relative incidence of inadvertent emboliBation was slightly higher, yet not significantly so, for the less-e1perienced angiographies and during longer procedures. 'ur report shows that theserates may nowadays be even lower, because no transient or permanent neurologic deficit wasobserved in our patients, and no thromboembolic event or arterial dissection was documentedradiologically or clinically in our series.

The reduction in the ris of intraprocedural complication during the last " decades is certainlymultifactorial. A ma0or role has to be attributed to improvements in the 5uality of angiographicdevices, including the development of smaller and softer catheters, the introduction ofhydrophilic biomaterials, and micropuncture access systems. The routine use of biplaneangiographic e5uipment, by offering " simultaneous pro0ections for each contrast agent in0ection,
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provides a double gain in study duration and contrast load. The introduction of nonionic and,more recently, iso-osmolar contrast agents may help decrease the ris of nephrologiccomplications. &ntraprocedural anticoagulation, both systemic and through flushing of the arterialsheath and catheters, represents a ma0or factor in the prevention of thromboemboliccomplication. ystemic anticoagulation is routinely used, with the e1ception of patients

investigated for an acute hemorrhage. A very low incidence of arterial thrombosis at the accesssite can be achieved in the pediatric population with systemic hepariniBation. $ &t should be notedthat although hepariniBed saline (at a concentration of #*** < E of normal saline solution! isused liberally to flush the sheath and catheters throughout the procedure, this heparin flush alonedoes not provide ade5uate anticoagulation in the pediatric population. $7 e routinely use aninitial bolus of $** < g, with a ma1imal dose of "*** < for diagnostic angiography,administered intravenously immediately after arterial access has been gained.

'ne ma0or complication potentially related to cerebral angiography was documented in ourseries. A 8-year-old girl died of a ruptured posterior fossa vari1 2 hours after completion of anuneventful cerebral angiogram. This patient had initially presented a few months earlier in a

comatose state resulting from a similar hemorrhagic episode. The second, fatal bleeding occurredshortly after the patient complained of nausea and vomited several times. e thin it possiblethat the rupture of the varicose vein may have been coincidental or precipitated by the straininginduced by the vomiting. &t is indeed unli ely that intra-arterial contrast agent administration (inthis case, gentle in0ections performed by hand! might have provo ed the rupture of a remotevenous structure 2 hours after completion of the study. Although it happened in the immediate

postprocedural period, this complication therefore may be technically unrelated to the angiogramitself.

An interesting and, to some e1tent, une1pected finding in our series was the absence of groincomplications. o hematomas were documented in our patients, despite the difficulty

represented by immobiliBing the leg of small children for a - to 7-hour period. &t is possible thatmanual hemostasis is more efficient in children owing to the superficial position of the femoralartery. &n our practice, femoral hemostasis in children is performed only by senior fellows orattending physicians, a factor that may play a role as well. 'ne child re5uired prolonged groincompression before hemostasis was achieved, without subse5uent hematoma, despite the absenceof a documented coagulation anomaly. This child, however, was slightly hypothermic at the endof the procedure, a condition nown to alter the coagulation pathways. $8 Another child had a mildfemoral lea shortly after the procedure that re5uired additional groin compression, againwithout hematoma. =ollow-up interviews of the parents of #8 of the 78 children aged $* oryounger did not document signs or symptoms of delayed limb complication, such as pain,limping, or leg length discrepancy. &t should be noted, however, that iliac or femoral arteryocclusion may remain asymptomatic in children, than s to their capacity at establishing acollateral blood supply.

Although the present study was mainly aimed at evaluating the rate of periproceduralcomplications, the potential long-term ris related to radiation e1posure needs to be mentioned.Children are particularly sensitive to radiation e1posure, a factor that obviously plays a rolewhen posing the indication for any radiological investigation based on ioniBing radiation. $ ,$) Therelative radiation e1posure from conventional angiography compared with CTA is still unclear. A
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recent study comparing radiation doses from multislice CT coronary angiography andconventional diagnostic angiography has shown the dose to be significantly higher for CTA ."* The same was found for CT urography versus conventional urography ,"$ whereas a similar studyinvestigating pulmonary angiography showed a slightly lower dose for CT. "" The fluoroscopytimes re5uired for pediatric D A are typically low, a factor that may tilt the balance in favor of

D A in children, although dedicated investigations in this field are re5uired.

&n $)8#, Kyepes "2 ended the preface to the first te1tboo dedicated to pediatric angiography byremar ing that LM high-5uality angiograms, performed by interested and competent radiologistson sound clinical indications are the best means to educateM about the usefulness ofangiography in children.N This must remain true today, as cerebral angiography continues to bethe Lgold standardN in neurovascular imaging, playing a decisive role when clinical 5uestions arenot resolved by noninvasive techni5ues such as CTA and 64A.

&n summary, our report shows that diagnostic cerebral angiography can be performed in childrenwith e1tremely low periprocedural complication rates. Iotential complications of pediatric

cerebral angiography that were not long ago regarded as significant,"#

eg, spasm induced by largecatheters, bleeding at puncture sites, and emboli from catheter tips, have nowadays been reducedto very low levels (none of these complications occurred in our study!. &t is obviously animportant ethical responsibility for referring physicians and angiographers to carefully determinethe appropriateness of an invasive procedure in a child/ it is, however, e5ually important not todeny pediatric patients the potentially crucial assistance of an invasive techni5ue based onunwarranted assumptions of danger.

References!. Chappell ET, Moure FC, Good MC. Comparison of computed tomographic

angiography with digital subtraction angiography in the diagnosis of cerebral

aneurysms: a meta-analysis. eurosurgery. !""#$ %!: &!'()$discussion"().. *be T, +irohata M, Tana a , chiyama , /o0ima /, Fu0imoto /, orbash *M,

+ayabuchi . Clinical bene1ts of rotational #2 angiography in endo3asculartreatment of ruptured cerebral aneurysm. *4 5 *m 4 euroradiol. !""!$ !#:&6&(&66.

6. +irai T, /orogi , 7uginohara /, 8no /, ishi T, emura 7, amura M,amashita . Clinical usefulness of unsubtracted #2 digital angiographycompared with rotational digital angiography in the pretreatment e3aluationof intracranial aneurysms. *4 5 *m 4 euroradiol. !""#$ !': )"&9()"9'.

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8. 7ugahara T, /orogi , a ashima /, +amata e 7, +onda 7, Ta ahashi M.Comparison of !2 and #2 digital subtraction angiography in e3aluation ofintracranial aneurysms. *4 5 *m 4 euroradiol. !""!$ !#: )%'%()%%!.
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