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Object. Postoperative epidural hematoma (EDH), a blood collection between the inserted galeal flap and the
overlying skull flap (epigaleal flap hematoma), is a frustrating complication of the surgical treatment of moyamoya
disease (MMD) in pediatric patients. The symptoms of postoperative EDH are often similar to those of postopera-
tive cerebral ischemia, and may cause confusion during clinical decision making. The authors designed this study to
evaluate the incidence, clinical presentation, risk factors, and treatment outcomes of postoperative EDH in pediatric
patients with MMD.
Methods. A retrospective review of 148 pediatric patients with 250 craniotomies who underwent indirect bypass
revascularization surgery between January 2002 and December 2006 was performed. This group consisted of 60 male
and 88 female patients, and the mean age at surgery was 7.5 years (range 1–18 years).
Results. Of the 250 craniotomies, postoperative EDH was detected in 32 cases. In 12 cases of EDH, surgical
treatment was necessary (4.8% of 250 craniotomies). During the same period, 743 non-MMD craniotomy operations
were performed. In 6 of these 743 operations, patients developed postoperative EDH that required surgical treatment,
significantly less than the percentage of EDH requiring postoperative treatment in patients with MMD (0.8%, p <
0.001). The average interval between craniotomy surgery and the detection of EDH was 1.8 days (range 0–5 days) in
patients with MMD and 0.5 days (range 0–2 days; p = 0.018) in the non-MMD craniotomy group.
Postoperative EDH was observed in significantly fewer cases (17 of 191) when a subcutaneous drain (SCD) was
inserted over the bone flap than in cases in which an SCD was not inserted (14 of 55; p = 0.001). The mean interna-
tional normalized ratio of prothrombin time in the immediate postoperative blood test was 1.27 ± 0.17 in the EDH
group and 1.20 ± 0.11 in the non-EDH group (values are expressed as the mean ± SD; p = 0.008). Central galeal flap
tenting suture and immediate postoperative platelet count were not related to the incidence of postoperative EDH
following pediatric MMD surgery.
Conclusions. Postoperative EDH is more likely to be found following craniotomy in patients with MMD than
in those without MMD, and may occur in a delayed fashion. Insertion of an SCD and immediate correction of an
abnormal value for international normalized ratio of prothrombin time can decrease the incidence of postoperative
EDH following surgery for pediatric MMD.
(http://thejns.org/doi/abs/10.3171/2013.4.PEDS12505)
T
he clinical features of pediatric MMD are mainly nial hemorrhage.8,17 Moyamoya disease accounts for 14%
ischemic symptoms, such as transient ischemic at- of all strokes in pediatric patients.18 The natural history
tack and cerebral infarction, whereas half of adult of MMD is not well understood; however, patients with
patients with MMD present with symptoms of intracra- conservative management demonstrate poorer intellectual
development and proficiency in daily living activities than
the patients who undergo surgical treatment.9,11,16 There-
Abbreviations used in this paper: EDAS = encephaloduroarterio fore, surgical treatment is generally recommended for pe-
synangiosis; EDH = epidural hematoma; EGS = encephalogaleo-
synangiosis; MMD = moyamoya disease; OA = occipital artery; diatric patients with MMD.
PT INR = international normalized ratio of prothrombin time; SCD Postoperative EDH, a blood collection between the
= subcutaneous drain; STA = superficial temporal artery; STAp = inserted galeal flap and the overlying skull flap (called the
parietal branch of the STA. “epigaleal flap hematoma” in this study), is a frustrating
complication of surgical treatment of MMD in pediatric and amount of postoperative EDH, and the interval be-
patients, sometimes causing disability, mental disturbance, tween the revascularization surgery and detection of EDH
and death. Many neurosurgeons are concerned about were collected. To evaluate risk factors of postoperative
EDH and use various methods to prevent its occurrence. EDH, we reviewed the presence of presumed risk factors
However, the incidence and risk factors of postoperative including age, sex, insertion of an SCD over the bone flap,
EDH are still unclear, and the effectiveness of preventive central galeal flap tenting suture, immediate postoperative
methods previously used by neurosurgeons has not been PT INR, platelet level, type of surgery, and number of sur-
investigated in pediatric MMD revascularization surgery. gery sites. Postoperative coagulation status was examined
Collateral vascular channels formed through the skull and by collecting peripheral blood within half an hour after
dura mater in MMD can be sources of slow blood accu- surgery.
mulation in the operative field. In addition, the indication Between January 2002 and December 2006, there
for surgical treatment for EDH in patients with MMD has were 148 patients: 49 patients who underwent revascu-
not yet been established because it is not unusual for these larization craniotomy once; 96 patients who underwent
patients to show postoperative transient ischemic attack the surgery twice; and 3 patients who experienced the
or infarction, and these events may combine with and ob- surgery 3 times. Two hundred fifty revascularization cra-
scure the occurrence of EDH. We designed a retrospec- niotomies were performed in all. The surgical treatment
tive analysis to evaluate the incidence, clinical presenta- is usually performed in 2–3 stages to obtain proper re-
tion, risk factors, and treatment outcomes of postoperative vascularization. This group consisted of 60 male (40.5%)
EDH in pediatric patients with MMD. and 88 female (59.5%) patients with a mean age at surgery
Our experimental questions were as follows. 1) Is of 7.5 years (range 1–18 years). A brain CT scan without
postoperative EDH more common in MMD surgery than enhancement was performed immediately after revas-
in non-MMD craniotomy operations? 2) Do EDHs result- cularization surgery as a routine postoperative checkup
ing from MMD surgery manifest more slowly than post- and when abnormal symptoms such as altered mentality,
operative EDHs resulting from non-MMD craniotomy significant headache and vomiting, or focal neurological
operations? 3) What are the risk factors of postoperative deficits were presented. The patients with an EDH larger
EDH in MMD? than 5 cm3 seen on the CT scan were included in the EDH
group.
To compare the incidence and time of diagnosis of
Methods EDH in patients with MMD after revascularization sur-
A retrospective review of medical records at Seoul gery with the same factors for non-MMD craniotomy sur-
National University Children’s Hospital in Seoul, Korea, geries, we also reviewed the information of patients who
was conducted for patients with MMD who were younger underwent craniotomy surgery unrelated to MMD during
than 18 years of age and who underwent indirect bypass the same period. The risk and clinical manifestation of
revascularization surgery including bifrontal EGS, STA EDH may vary according to the site of operation. There-
EDAS, and OA EDAS. fore, we excluded sites of bifrontal EGS and OA EDAS
An STA EDAS was performed for the collateral for- and focused on the “homogeneous” condition of STA
mation in the middle cerebral artery territory. The STA, EDAS.
most commonly the STAp, was dissected along with a Patients with MMD often exhibit cerebral infarction
strip of galea through a sigmoid skin incision. The dura or ischemic symptoms such as transient focal neurological
was opened without injury of the major meningeal artery deficit during the early postoperative period. For the man-
along the course of the STAp. Wide opening of arachnoid agement of postoperative EDH in patients with MMD, the
was performed to promote the ingrowth of the neovascu- effects of an EDH versus possible postoperative cerebral
lature. The STAp with the strip of galea overlying on the ischemia should be balanced in deciding on the treatment
exposed cortex was sutured to the edges of the dura mater. plan, especially when the hematoma is not large. For this
Bifrontal EGS was performed for the collateral for- reason, we reviewed the treatment outcome of patients
mation in the anterior cerebral artery territory. A trans- with postoperative EDH at the STA EDAS site only, where
verse S-shaped skin incision was made anterior to the both EDH and ischemia may similarly manifest as focal
coronal suture. The galea was freed from periosteum and neurological deficits. Surgical evacuation of EDH was de-
incised to make bilateral flaps that had bases on the lateral cided based on the symptoms, signs, and volume of the
side. After creation of a 4 × 8–cm rectangular craniotomy hematoma.
crossing the superior sagittal sinus, the dura was opened The incidences of EDH in MMD surgery and in
on both sides as for the galeal flaps, and wide opening of non-MMD types of craniotomy and the frequency of risk
arachnoid was performed. The galeal flap was sutured to factors in EDH and non-EDH groups were compared us-
the dural margins. ing the Pearson chi-square test, Student t-test, and Mann-
An EDAS was performed using the OA for the col- Whitney U-test. Multivariate analysis using logistic re-
lateral formation in the posterior cerebral artery territory. gression was performed for the risk factors related to the
The OA was dissected along with a strip of galea through EDH: age, sex, insertion of an SCD, central galeal flap
a sigmoid skin incision. The arachnoid was opened. The tenting suture, PT INR, platelet level, type of surgery, and
OA with the strip of galea was sutured to the edges of the number of surgery sites. A 2-tailed p value < 0.05 was
dura mater. considered statistically significant. All statistical analyses
All records were reviewed, and data regarding patient were performed using the SPSS software package (version
age, sex, name of the operation, occurrence, presentation, 12.0; SPSS, Inc.).
Op Site No. of Ops No. of Postop EDH Cases (%) Diagnosis No. of Cases (%)
STA EDAS 246 26 (10.6) benign brain tumor 312 (41.9)
bifrontal EGS 120 5 (4.2) malignant brain tumor 151 (20.3)
OA EDAS 24 1 (4.2) epilepsy 84 (11.3)
craniofacial anomaly 67 (9.0)
wound revision 25 (3.4)
reviewed. Of the 26 cases, 10 underwent surgical treat-
skull defect 22 (3.0)
ment due to EDH volume and remarkable symptoms, such
as altered mentality or focal neurological deficit, and 16 intracerebral hematoma 16 (2.2)
were managed conservatively. In 25 cases, patients were arteriovenous malformation 13 (1.8)
discharged from the hospital without additional neurologi- CSF disorder 12 (1.6)
cal deterioration. However, 1 patient who was treated with benign cyst 10 (1.3)
conservative management had fine motor dysfunction of miscellaneous 31 (4.2)
the hand.
total 743 (100)
Discussion
provide an alternative route for cerebral perfusion. We
The incidence of MMD is relatively low; however, it frequently found that these collateral vessels bled during
is a common cause of pediatric cerebral infarction. The the surgical procedure. We assumed that these epidural
early diagnosis and appropriate treatment of MMD is cru- fine vessels also exist on the periphery of the craniotomy
cial in preventing cerebral infarction.13 site. We also hypothesized that slow blood leakage from
The optimal treatment for MMD is not yet clearly es- injured fine collateral vessels in the cranial vault causes
tablished. The effectiveness of various medical treatments the hematoma. The difference in intervals between the
has not been proven in MMD, but surgical treatment has surgery and detection of postoperative EDH in MMD and
been an excellent option providing a favorable outcome.3 non-MMD craniotomies (1.8 days vs 0.5 day, respectively)
We previously reported a comparison between STA EDAS supports our hypothesis.
and STA EDAS with bifrontal EGS. An STA EDAS with Early recognition and diagnosis of postoperative EDH
bifrontal EGS could reperfuse regions of the brain requir- are essential in preventing devastating results because of
ing blood flow from the middle cerebral and anterior cere- frequent rapid progression during the first several hours.
bral arteries. Thus, this surgical approach may be a more In our study, frequent postoperative symptoms of an EDH
effective modality for the treatment of MMD.12,14,15 were altered mentality and nausea with vomiting. Howev-
Postoperative EDH is a common complication of re- er, these are nonspecific postoperative symptoms. Weak-
vascularization surgery for MMD. Palmer et al.19 reported ness, dysarthria, and tingling are common symptoms in
an overall incidence rate of 1.1% for postoperative hema- both postoperative EDH and postoperative cerebral isch-
tomas requiring surgical evacuation after craniotomies in emia. Thus, similarity of symptoms may cause confusion
general, and EDH accounted for 33% of these hematomas. in clinical decision making. Because of the difficulty in
Other prior studies have reported the incidence of postop- differentiating the symptoms of EDH from those of ce-
erative EDHs as 0.9%–1.3%.5,22 In our study, the incidence rebral ischemia, brain imaging is a crucial tool to verify
of postoperative EDH requiring surgical treatment was the occurrence of an EDH. Sometimes, however, when the
4.8% of craniotomies in patients with MMD and 0.8% hematoma is small or medium sized it is not clear whether
of craniotomies unrelated to MMD. Although postopera- the symptoms are caused by EDH, even after imaging
tive ischemia causing focal neurological deficits may have studies.
led to more frequent neuroimaging studies with increased Guangming et al.7 evaluated the efficacy of the epi-
incidence of postoperative EDH, the higher incidence of dural drain in preventing EDH following supratentorial
postoperative EDH in MMD surgery may be due to pa- craniotomy in epileptic patients. These authors concluded
tient and disease characteristics rather than to technical
reasons. Patients with MMD have characteristic collateral TABLE 6: Sites of 6 EDHs in non-MMD cases*
vessels at the cranial vault and the base of the brain that
Case No. Disease Site of EDH
TABLE 4: Incidence of EDH after MMD revascularization surgery
(by craniotomy) 1 pilocytic astrocytoma bifrontal
2 medulloblastoma rt parietal
No. of Postop EDH 3 medulloblastoma posterior fossa
Op No. of Ops Cases (%) p Value 4 medulloblastoma posterior fossa
STA EDAS alone 106 14 (13.2) 0.615 5 PNET lt parietal
STA EDAS + bifrontal EGS 118 13 (11.0)* 6 glioblastoma lt parietal
* Bifrontal EGS site in 4 cases, STA EDAS site in 9 cases. * PNET = primitive neuroectodermal tumor.
3. Choi JU, Kim DS, Kim EY, Lee KC: Natural history of moy- 15. Kim SK, Wang KC, Oh CW, Kim IO, Lee DS, Song IC, et al:
amoya disease: comparison of activity of daily living in surgery Evaluation of cerebral hemodynamics with perfusion MRI in
and non surgery groups. Clin Neurol Neurosurg 99 (Suppl 2): childhood moyamoya disease. Pediatr Neurosurg 38:68–75,
S11–S18, 1997 2003
4. Duthie G, Reaper J, Tyagi A, Crimmins D, Chumas P: Extradu- 16. Kurokawa T, Tomita S, Ueda K, Narazaki O, Hanai T, Hasuo K,
ral haematomas in children: a 10-year review. Br J Neurosurg et al: Prognosis of occlusive disease of the circle of Willis (moy-
23:596–600, 2009 amoya disease) in children. Pediatr Neurol 1:274–277, 1985
5. Fukamachi A, Koizumi H, Nagaseki Y, Nukui H: Postoperative 17. Matsushima Y, Aoyagi M, Niimi Y, Masaoka H, Ohno K: Symp-
extradural hematomas: computed tomographic survey of 1105 toms and their pattern of progression in childhood moyamoya
intracranial operations. Neurosurgery 19:589–593, 1986 disease. Brain Dev 12:784–789, 1990
6. Gerlach R, Raabe A, Scharrer I, Meixensberger J, Seifert V: 18. Nagaraja D, Verma A, Taly AB, Kumar MV, Jayakumar PN:
Post-operative hematoma after surgery for intracranial menin- Cerebrovascular disease in children. Acta Neurol Scand 90:
giomas: causes, avoidable risk factors and clinical outcome. 251–255, 1994
Neurol Res 26:61–66, 2004 19. Palmer JD, Sparrow OC, Iannotti F: Postoperative hematoma: a
7. Guangming Z, Huancong Z, Wenjing Z, Guoqiang C, Xiaosong 5-year survey and identification of avoidable risk factors. Neu-
W: Should epidural drain be recommended after supratentori rosurgery 35:1061–1065, 1994
al craniotomy for epileptic patients? Surg Neurol 72:138–141, 20. Swayne OB, Horner BM, Dorward NL: The hitch stitch: an ob-
2009 solete neurosurgical technique? Br J Neurosurg 16:541–544,
8. Han DH, Nam DH, Oh CW: Moyamoya disease in adults: 2002
characteristics of clinical presentation and outcome after en- 21. Tallon JM, Ackroyd-Stolarz S, Karim SA, Clarke DB: The ep
cephalo-duro-arterio-synangiosis. Clin Neurol Neurosurg 99 idemiology of surgically treated acute subdural and epidural
(Suppl 2):S151–S155, 1997 hematomas in patients with head injuries: a population-based
9. Imaizumi T, Hayashi K, Saito K, Osawa M, Fukuyama Y: Long- study. Can J Surg 51:339–345, 2008
term outcomes of pediatric moyamoya disease monitored to 22. Troupp H: Extradural hematoma during craniotomy. Report of
adulthood. Pediatr Neurol 18:321–325, 1998 five cases. J Neurosurg 40:783–785, 1974
10. Jamous MA, Abdel Aziz H, Al Kaisy F, Eloqayli H, Azab M, 23. Winston KR: Dural tenting sutures in pediatric neurosurgery.
Al-Jarrah M: Conservative management of acute epidural he- Pediatr Neurosurg 28:230–235, 1998
matoma in a pediatric age group. Pediatr Neurosurg 45:181– 24. Winston KR: Efficacy of dural tenting sutures. J Neurosurg
184, 2009 91:180–184, 1999
11. Karasawa J, Kikuchi H, Kuriyama Y, Sawada T, Nishimura T, 25. Zhao J, Liu Z, Liu Y, Liu J, Fang W, Rao Y, et al: [Effect of epi-
Kozuka T, et al: [Cerebral hemodynamics in “moyamoya” dis- dural drainage and dural tenting suture on epidural hematoma
ease. I. Dynamic brain scintigraphy before and after bypass sur- in 145 cases of craniotomy.] Zhong Nan Da Xue Xue Bao Yi
gery (author’s transl).] Neurol Med Chir (Tokyo) 21:923–930, Xue Ban 35:273–276, 2010 (Chinese)
1981 (Jpn)
12. Kim CY, Wang KC, Kim SK, Chung YN, Kim HS, Cho BK:
Encephaloduroarteriosynangiosis with bifrontal encephalogal
eo(periosteal)synangiosis in the pediatric moyamoya disease:
the surgical technique and its outcomes. Childs Nerv Syst
19:316–324, 2003 Manuscript submitted October 13, 2012.
13. Kim SK, Cho BK, Phi JH, Lee JY, Chae JH, Kim KJ, et al: Pe- Accepted April 29, 2013.
diatric moyamoya disease: an analysis of 410 consecutive cases. Please include this information when citing this paper: published
Ann Neurol 68:92–101, 2010 online June 7, 2013; DOI: 10.3171/2013.4.PEDS12505.
14. Kim SK, Wang KC, Kim IO, Lee DS, Cho BK: Combined en- Address correspondence to: Kyu-Chang Wang, M.D., Ph.D.,
cephaloduroarteriosynangiosis and bifrontal encephalo galeo Division of Pediatric Neurosurgery, Seoul National University Chil-
(periosteal)synangiosis in pediatric moyamoya disease. Neuro- dren’s Hospital, 101 Daehakro, Jongno-gu, Seoul 110-769, Republic
surgery 50:88–96, 2002 of Korea. email: kcwang@snu.ac.kr.