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Postoperative epidural hematoma covering the galeal flap in pediatric patients with moyamoya disease: clinical manifestation, risk factors, and outcomes

Clinical article

Hyunho Choi, Ji Yeoun Lee, Ji Hoon Phi, Seung-Ki Kim, Byung-Kyu Cho, and Kyu-Chang Wang

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 postoperative 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 international 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.

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High prevalence of systemic hypertension in pediatric patients with moyamoya disease years after surgical treatment

Joongyub Lee, Seung-Ki Kim, Hee Gyung Kang, Il-Soo Ha, Kyu-Chang Wang, Ji Yeoun Lee, and Ji Hoon Phi

OBJECTIVE

Although an association between moyamoya disease (MMD) and renovascular hypertension has been acknowledged, the literature on systemic hypertension without renal artery stenosis among patients with MMD is scarce. The authors aimed to evaluate the prevalence and risk factors of hypertension using data from MMD patients who visited an outpatient clinic of a pediatric neurosurgical department in 2016.

METHODS

The authors evaluated the blood pressure (BP) of pediatric MMD patients at their postsurgical appointment following the American Academy of Pediatrics clinical practice guideline on high BP, in which hypertension was defined as BP measurements higher than the value of age-, sex-, and height-specific 95th percentile of the general population from at least 3 separate visits. Growth of patients was determined using 2017 Korean National Growth Charts for children and adolescents. The cutoff value of the 95th percentile of BP was determined by referring to normative BP tables of Korean children and adolescents. A logistic regression model was used to assess the associations between patients’ clinical characteristics and prevalent hypertension.

RESULTS

In total, 131 surgically treated pediatric MMD patients were included, of whom 38.9% were male and the median age at diagnosis was 8.0 years (range 1.2–15.0 years). The definition of hypertension was met in 38 patients, with a prevalence of 29.0% (95% CI 21.2%–36.8%). A tendency was observed for a higher prevalence of hypertension in male patients (31.4%), in patients with posterior cerebral artery (PCA) involvement (47.8%), and in cases in which infarction was shown on initial MRI (37.3%). Age at diagnosis (adjusted OR [aOR] 0.82, 95% CI 0.70–0.97), PCA involvement (aOR 3.81, 95% CI 1.29–11.23), body mass index (aOR 1.30, 95% CI 1.13–1.51), and years of follow-up since surgery (aOR 0.80, 95% CI 0.68–0.94) were related to systemic hypertension.

CONCLUSIONS

A high prevalence of hypertension was demonstrated in pediatric MMD patients. Therefore, adequate attention should be paid to reduce BP and prevent subsequent events.

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Long-term outcome of large sylvian arachnoid cysts: the role of surgery has been exaggerated

Kyung Hyun Kim, Ji Yeoun Lee, Ji Hoon Phi, Seung-Ki Kim, Byung-Kyu Cho, and Kyu-Chang Wang

OBJECTIVE

The surgical indications for some arachnoid cysts (ACs) are controversial. While surgical procedures can be effective when an AC is a definite cause of hydrocephalus or papilledema, most ACs do not cause any symptoms or signs. Some surgeons perform several procedures to treat ACs because of their large size. The purpose of this study was to compare the long-term outcomes of Galassi type III ACs between surgery and nonsurgery groups.

METHODS

The medical records of 60 patients diagnosed with sylvian ACs (Galassi type III) who visited Seoul National University Children’s Hospital from July 1990 to March 2018 were analyzed. The authors compared the outcomes between those treated with surgery and those not treated with surgery.

RESULTS

Of the 60 patients, 27 patients had no symptoms, 19 patients had vague symptoms and signs associated with ACs, and the remaining 14 patients had definite AC-related symptoms and signs. Thirty-eight patients underwent surgery, and 22 patients underwent observation. Some operations were accompanied by complications. Among the 33 patients in the surgery group, excluding 5 with hydrocephalus or papilledema, 8 patients needed 18 additional operations. However, there were no patients in the nonsurgery group who needed surgical intervention during the follow-up period (mean 67.5 months), although the size of the AC increased in 2 patients. Changes in AC size were not correlated with symptom relief.

CONCLUSIONS

When patients with hydrocephalus or papilledema were excluded, there was no difference in the outcomes between the surgery and nonsurgery groups regardless of the size of the sylvian AC. Surgeons should be cautious when deciding whether to operate.

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Multifocal intraparenchymal hemorrhages after ventriculoperitoneal shunt surgery in infants

Clinical article

Jung Won Choi, Seung-Ki Kim, Kyu-Chang Wang, Ji Yeoun Lee, Jung-Eun Cheon, and Ji Hoon Phi

Object

Ventriculoperitoneal (VP) shunt surgery is the most common treatment for hydrocephalus. In certain situations, uncommon complications can occur after shunting procedures. The authors undertook this study to analyze the clinical characteristics of pediatric patients who developed multifocal intraparenchymal hemorrhages (MIPHs) as a complication of shunt surgery. The authors also analyzed the risk factors for MIPH in a large cohort of patients with hydrocephalus.

Methods

This study included all pediatric patients (age < 18 years) who underwent VP shunt surgery at the authors' institution between January 2001 and December 2012. During this period, 507 VP shunt operations were performed in 330 patients. Four of these patients were subsequently diagnosed as having MIPH. The authors analyzed the clinical characteristics of these patients in comparison with those of the entire group of shunt-treated patients.

Results

The incidence of MIPH was 1.2% (4 of 330 cases) for all pediatric patients who underwent VP shunt placement but 2.9% (4 of 140 cases) for infants less than 1 year old. When the analysis was limited to patients whose corrected age was less than 3 months, the incidence was 5.3% (4 of 76 cases). Of the 4 patients with MIPH, 2 were male and 2 were female. Their median age at surgery was 54 days (range 25–127 days), and in all 4 cases, the patients' corrected age was less than 1 month. Three patients were preterm infants, whereas one patient was full-term. None of these patients had a prior history of intracranial surgery (including CSF diversion procedures). All showed severe hydrocephalus during the preoperative period. Their clinical courses as patients with MIPH were comparatively favorable, despite the radiological findings.

Conclusions

MIPH is a rare but not negligible complication of VP shunt surgery. This complication might be a unique phenomenon in infants, especially young, preterm infants with severe hydrocephalus. Moreover, the absence of previous intracranial procedures might be one of the risk factors for this complication. The rapid alteration of brain conditions in the setting of immaturity might cause MIPH. To prevent this complication, the authors recommend that pressure settings of programmable valves should be gradually adapted to the target pressure.

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Congenital solitary infantile myofibromatosis involving the spinal cord

Case report

Eun Ji Kim, Kyu-Chang Wang, Ji Yeoun Lee, Ji Hoon Phi, Sung-Hye Park, Jung-Eun Cheon, Young Eun Jang, and Seung-Ki Kim

Infantile myofibromatosis, a rare mesenchymal disorder that develops in early childhood, is classified by the number of lesions that occur: solitary or multicentric. Involvement of the CNS is unusual in either type. Infantile myofibromatosis in the spine is exceptional, and most published cases represent a secondary invasion. Here, the authors report on an 8-month-old girl presenting with weakness below the ankle and an intraspinal mass extending from T-6 to the conus. The patient underwent only partial surgical removal of the lesion, and the pathology was confirmed as infantile myofibromatosis. After the operation, weakness in the lower extremities gradually improved; however, she could not walk at the time of the final follow-up. On follow-up MRI performed 19 months after the operation, the residual lesion remained unchanged with decreased enhancement.

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Long-term endocrine outcome of suprasellar arachnoid cysts

Ji Yeoun Lee, Young Ah Lee, Hae Woon Jung, Sangjoon Chong, Ji Hoon Phi, Seung-Ki Kim, Choong-Ho Shin, and Kyu-Chang Wang

OBJECTIVE

Due to their distinct location, suprasellar arachnoid cysts are known to cause a wide variety of problems, such as hydrocephalus, endocrine symptoms, and visual abnormalities. The long-term outcome of these cysts has not been elucidated. To find out the long-term outcome of suprasellar arachnoid cysts, a retrospective review of the patients was performed. The neurological and endocrine symptoms were thoroughly reviewed.

METHODS

Forty-five patients with suprasellar arachnoid cysts, with an average follow-up duration of 9.7 years, were enrolled in the study. A comprehensive review was performed of the results of follow-up regarding not only neurological symptoms but also endocrine status. The outcomes of 8 patients who did not undergo operations and were asymptomatic or had symptoms unrelated to the cyst were included in the series.

RESULTS

Surgery was most effective for the symptoms related to hydrocephalus (improvement in 32 of 32), but endocrine symptoms persisted after surgery (4 of 4) and required further medical management. More surprisingly, a fairly large number of patients (14 of 40; 1 was excluded because no pre- or postoperative endocrine evaluation was available) who had not shown endocrine symptoms at the time of the initial diagnosis and treatment later developed endocrine abnormalities such as precocious puberty and growth hormone deficiency. The patients with endocrine symptoms detected during the follow-up included those in both the operated (n = 12 of 32) and nonoperated (n = 2 of 8) groups who had been stable during follow-up since the initial diagnosis.

CONCLUSIONS

This study implies that patients with suprasellar arachnoid cysts can develop late endocrine problems during follow-up, even if other symptoms related to the cyst have been successfully treated. Hence, patients with these cysts need long-term follow-up for not only neurological symptoms but also endocrine abnormalities.

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Clinical outcomes of pediatric cerebral cavernous malformation: an analysis of 124 consecutive cases

Youngbo Shim, Ji Hoon Phi, Kyu-Chang Wang, Byung-Kyu Cho, Ji Yeoun Lee, Eun Jung Koh, Kyung Hyun Kim, Eun Jung Lee, Ki Joong Kim, and Seung-Ki Kim

OBJECTIVE

One-fourth of cerebral cavernous malformation (CCM) patients are children, but studies on these patients are scarce. This study aimed to identify the clinical presentation of pediatric CCM patients and to investigate clinical outcomes according to the treatment modalities applied on the basis of our institution’s treatment strategy.

METHODS

The authors performed a retrospective analysis of 124 pediatric CCM patients with a follow-up of more than 1 year from 2000 to 2019. They performed resection (n = 62) on lesions causing intractable seizure, rebleeding, or mass effect and observed the clinical courses of patients with lesions in deep or eloquent areas without persistent symptoms (n = 52). Radiosurgery (n = 10) was performed when the patient refused resection or strongly desired radiosurgery. The authors investigated the clinical characteristics, performance status (modified Rankin Scale [mRS] score), and rebleeding rate at the 1-year and last follow-up examinations and compared these among 3 groups classified on the basis of treatment applied. The authors evaluated seizure outcomes at the 1-year and last follow-up examinations for the surgery (n = 32) and observation (n = 17) groups. Finally, the authors drew cumulative incidence curves for the discontinuation of antiepileptic drugs (AEDs) for patients in the surgery (n = 30) and observation (n = 9) groups.

RESULTS

The 3 groups showed slight differences in initial symptoms, lesion locations, and rates of recent hemorrhage. The proportion of patients with improved mRS score at the 1-year follow-up was significantly greater in the surgery group than in the other groups (67% of the surgery group, 52% observation group, and 40% radiosurgery group; p = 0.078), as well as at the last follow-up (73% surgery group, 54% observation group, and 60% radiosurgery group; p = 0.097). The surgery group also had the lowest rebleeding rate during the follow-up period (2% surgery group, 11% observation group, and 20% radiosurgery group; p = 0.021). At the 1-year follow-up, the proportion of seizure-free patients without AEDs was significantly higher in the surgery group than the observation group (88% surgery group vs 53% observation group, p < 0.001), and similar results were obtained at the last follow-up (91% surgery group vs 56% observation group, p = 0.05). The 5-year AED-free rates for the surgery and observation groups were 94% and 50%, respectively, on the cumulative incidence curve (p = 0.049).

CONCLUSIONS

The clinical presentation of pediatric CCM patients was not significantly different from that of adult patients. Lesionectomy may be acceptable for pediatric CCM patients with indications of persistent seizures despite AED medications, rebleeding, and mass effects.

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Dosimetric parameters associated with the long-term oncological outcomes of Gamma Knife surgery for sellar and parasellar tumors in pediatric patients

Eun Jung Lee, Ji Yeoun Lee, Jin-Wook Kim, Ji Hoon Phi, Yong Hwy Kim, Seung-Ki Kim, Hyun-Tai Chung, Kyu-Chang Wang, and Dong Gyu Kim

OBJECTIVE

The authors aimed to investigate the dosimetric parameter and the minimally required dose associated with long-term control of sellar and parasellar tumors after Gamma Knife surgery (GKS) in children.

METHODS

A retrospective analysis was performed on pediatric patients younger than 19 years of age who were diagnosed with sellar and parasellar tumors and received GKS at the authors’ institution from 1998 to 2019. Cox proportional hazards regression analyses were used to investigate the dosimetric parameters associated with treatment outcome. The Kaplan-Meier method was used to analyze tumor control rates after GKS.

RESULTS

Overall, 37 patients with 40 sellar and parasellar tumors, including 22 craniopharyngiomas and 12 pituitary adenomas, had a mean follow-up of 85.8 months. The gross target volume was 0.05 cm3 to 15.28 cm3, and the mean marginal dose was 15.8 Gy (range 9.6–30.0 Gy). Ten patients experienced treatment failure at a mean of 28.0 ± 26.7 months. The actuarial 5- and 10-year tumor control rates were 79.0% and 69.8%, respectively. D98% was an independent predictive factor of tumor control (HR 0.846 [95% CI 0.749–0.956], p = 0.007), with a cutoff value of 11.5 Gy for the entire cohort and 10 Gy for the craniopharyngioma group. Visual deterioration occurred in 2 patients with the maximum point dose of 10.1 Gy and 10.6 Gy to the optic apparatus.

CONCLUSIONS

In pediatric patients, D98% was a reliable index of the minimum required dose for long-term control of sellar and parasellar tumors after GKS. The optimal D98% value for each tumor diagnosis needs to be elucidated in the future.

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Modification of surgical procedure for “probable” limited dorsal myeloschisis

Ji Yeoun Lee, Sangjoon Chong, Young Hun Choi, Ji Hoon Phi, Jung-Eun Cheon, Seung-Ki Kim, Sung Hye Park, In-One Kim, and Kyu-Chang Wang

OBJECTIVE

Since the entity limited dorsal myeloschisis (LDM) was proposed, numerous confusing clinical cases have been renamed according to the embryopathogenesis. However, clinical application of this label appears to require some clarification with regard to pathology. There have been cases in which all criteria for the diagnosis of LDM were met except for the presence of a neural component in the stalk, an entity the authors call “probable” LDM. The present study was performed to meticulously review these cases and suggest that a modified surgical strategy using limited laminectomy is sufficient to achieve the surgical goal of untethering.

METHODS

The authors retrospectively reviewed the imaging findings, operative notes, and pathology reports of spinal dysraphism patients with subcutaneous stalk lesions who had presented to their institution between 2010 and 2014.

RESULTS

Among 33 patients with LDM, 13 had the typical nonsaccular lesions with simple subcutaneous stalks connecting the skin opening to the spinal cord. Four cases had “true” LDM meeting all criteria for diagnosis, including pathological confirmation of CNS tissue by immunohistochemical staining with glial fibrillary acidic protein. There were also 9 cases in which all clinical, imaging, and surgical findings were compatible with LDM, but the “neural” component in the resected stalk was not confirmed. For all the cases, limited exposure of the stalk was done and satisfactory untethering was achieved.

CONCLUSIONS

One can speculate based on the initial error of embryogenesis that if the entire stalk were traced to the point of insertion on the cord, the neural component would be proven. However, this would require an extended level of laminectomy/laminotomy, which may be unnecessary, at least with regard to the completeness of untethering. Therefore, the authors propose that for some selected cases of LDM, a minimal extent of laminectomy may suffice for untethering, although it may be insufficient for diagnosing a true LDM.

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Impaired functional recovery of endothelial colony-forming cells from moyamoya disease in a chronic cerebral hypoperfusion rat model

Seung Ah Choi, Sangjoon Chong, Pil Ae Kwak, Youn Joo Moon, Anshika Jangra, Ji Hoon Phi, Ji Yeoun Lee, Sung-Hye Park, and Seung-Ki Kim

OBJECTIVE

Endothelial colony-forming cells (ECFCs) isolated from pediatric patients with moyamoya disease (MMD) have demonstrated decreased numbers and defective functioning in in vitro experiments. However, the function of ECFCs has not been evaluated using in vivo animal models. In this study, the authors compared normal and MMD ECFCs using a chronic cerebral hypoperfusion (CCH) rat model.

METHODS

A CCH rat model was made via ligation of the bilateral common carotid arteries (2-vessel occlusion [2-VO]). The rats were divided into three experimental groups: vehicle-treated (n = 8), normal ECFC-treated (n = 8), and MMD ECFC-treated (n = 8). ECFCs were injected into the cisterna magna. A laser Doppler flowmeter was used to evaluate cerebral blood flow, and a radial arm maze test was used to examine cognitive function. Neuropathological examinations of the hippocampus and agranular cortex were performed using hematoxylin and eosin and Luxol fast blue staining in addition to immunofluorescence with CD31, von Willebrand factor, NeuN, myelin basic protein, glial fibrillary acidic protein, and cleaved caspase-3 antibodies.

RESULTS

The normal ECFC-treated group exhibited improvement in the restoration of cerebral perfusion and in behavior compared with the vehicle-treated and MMD ECFC-treated groups at the 12-week follow-up after the 2-VO surgery. The normal ECFC-treated group showed a greater amount of neovasculogenesis and neurogenesis, with less apoptosis, than the other groups.

CONCLUSIONS

These results support the impaired functional recovery of MMD ECFCs compared with normal ECFCs in a CCH rat model. This in vivo study suggests the functional role of ECFCs in the pathogenesis of MMD.