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James Feghali, Risheng Xu, Wuyang Yang, Jason Liew, Rafael J. Tamargo, Elisabeth B. Marsh and Judy Huang

OBJECTIVE

The authors aimed to determine whether differences exist in presentation and natural history when comparing Asian patients with moyamoya disease (MMD) to those of other ethnicities in North America.

METHODS

A database of 137 patients with MMD presenting to their institution between 1994 and 2015 was reviewed. Baseline characteristics and outcome variables, including stroke and functional outcome, were compared between Asian and non-Asian patients. Unadjusted Kaplan-Meier survival analysis and adjusted Cox regression models were used to compare stroke-free survival and stroke hazard after diagnosis among hemispheres of both racial groups. The analysis was stratified by age group, and censoring was performed until last follow-up or at the time of surgery. Because the relative rate of stroke changed between Asian and non-Asian adults after 1.5 years of follow-up, a time-segmented analysis focusing on the period 1.5 years after diagnosis was performed.

RESULTS

The cohort comprised 23% (31/137) Asian and 77% (106/137) non-Asian patients with MMD with a bimodal age distribution. Non-Asian patients had a higher prevalence of increased BMI (p = 0.02) and smoking (p = 0.04). Among patients who presented with stroke (n = 90), hemorrhage was significantly more common among Asians (p = 0.02). The natural history analysis included 250 hemispheres: 67 pediatric and 183 adult hemispheres. The overall mean follow-up duration since diagnosis was 3.3 years. Among adults, Asian patients had a higher incidence of stroke (8.0 per 100 person-years vs 3.0 per 100 person-years) over a mean follow-up of 3.3 years, but results were not statistically significant (p = 0.45). In the period beginning 1.5 years after diagnosis, Asian adults had a significantly higher hazard of stroke over a mean follow-up of 7.7 years, while controlling for sex, hypertension, and stroke before diagnosis (hazard ratio 8.8, p = 0.02). Among pediatric patients, Asians also had a higher stroke incidence (10.0 per 100 person-years vs 3.5 per 100 person-years) over a mean follow-up of 3.2 years; however, results did not reach statistical significance (p = 0.40). Functional outcome was similar between both ethnic groups at last follow-up (p = 0.57).

CONCLUSIONS

This study suggests a comparatively more progressive course of MMD in Asians. Further studies are required to fully characterize the phenotypic distinctions between different races and underlying pathophysiological mechanisms.

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James Feghali, Risheng Xu, Wuyang Yang, Jason Anthony Liew, Jaishri Blakeley, Edward S. Ahn, Rafael J. Tamargo and Judy Huang

OBJECTIVE

Phenotypic differences between moyamoya disease (MMD) and moyamoya syndrome (MMS) remain unclear. The purpose of this study was to evaluate whether such differences exist when presentation, procedure-related, and outcome variables are compared quantitatively.

METHODS

The study cohort included 185 patients with moyamoya presenting to the Johns Hopkins Medical Institutions between 1994 and 2015. Baseline demographic, angiographic, and clinical characteristics were compared between patients with MMS and MMD, in addition to procedure-related complications and length of stay (LOS) after surgery. Stroke-free survival was compared between both disease variants after diagnosis. Kaplan-Meier analysis and Cox proportional hazards regression were used to compare stroke-free survival between surgically treated and conservatively managed hemispheres in both types of disease, while evaluating interaction between disease variant and management.

RESULTS

The cohort consisted of 137 patients with MMD (74%) with a bimodal age distribution and 48 patients with MMS (26%) who were mostly under 18 years of age (75%). Underlying diseases included sickle cell disease (48%), trisomy 21 (12%), neurofibromatosis (23%), and other disorders (17%). Patients with MMS were younger (p < 0.001) and less likely to be female (p = 0.034). Otherwise, baseline characteristics were statistically comparable. The rate of surgical complications was 33% in patients with MMD and 16% in patients with MMS (p = 0.097). Both groups of patients had a similar LOS after surgery (p = 0.823). Survival analysis (n = 330 hemispheres) showed similar stroke-free survival after diagnosis (p = 0.856) and lower stroke hazard in surgically managed patients in both MMD (hazard ratio [HR] 0.29, p = 0.028) and MMS (HR 0.62, p = 0.586). The disease variant (MMD vs MMS) did not affect the relationship between management approach (surgery vs conservative) and stroke hazard (p = 0.787).

CONCLUSIONS

MMD and MMS have largely comparable clinical and angiographic phenotypes with analogously favorable responses to surgical revascularization.

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Matthew T. Bender, Geoffrey P. Colby, Li-Mei Lin, Bowen Jiang, Erick M. Westbroek, Risheng Xu, Jessica K. Campos, Judy Huang, Rafael J. Tamargo and Alexander L. Coon

OBJECTIVE

Flow diversion requires neointimal stent overgrowth to deliver aneurysm occlusion. The existing literature on aneurysm occlusion is limited by heterogeneous follow-up, variable antiplatelet regimens, noninvasive imaging modalities, and nonstandard occlusion assessment. Using a large, single-center cohort with low attrition and standardized antiplatelet tapering, the authors evaluated outcomes after flow diversion of anterior circulation aneurysms to identify predictors of occlusion and aneurysm persistence.

METHODS

Data from a prospective, IRB-approved database was analyzed for all patients with anterior circulation aneurysms treated by flow diversion with the Pipeline embolization device (PED) at the authors’ institution. Follow-up consisted of catheter cerebral angiography at 6 and 12 months postembolization. Clopidogrel was discontinued at 6 months and aspirin was reduced to 81 mg daily at 12 months. Occlusion was graded as complete, trace filling, entry remnant, or aneurysm filling. Multivariate logistic regression was performed to identify predictors of aneurysm persistence.

RESULTS

Follow-up catheter angiography studies were available for 445 (91%) of 491 PED procedures performed for anterior circulation aneurysms between August 2011 and August 2016. Three hundred eighty-seven patients accounted for these 445 lesions with follow-up angiography. The population was 84% female; mean age was 56 years and mean aneurysm size was 6.6 mm. Aneurysms arose from the internal carotid artery (83%), anterior cerebral artery (13%), and middle cerebral artery (4%). Morphology was saccular in 90% of the lesions, and 18% of the aneurysms has been previously treated. Overall, complete occlusion was achieved in 82% of cases at a mean follow-up of 14 months. Complete occlusion was achieved in 72%, 78%, and 87% at 6, 12, and 24 months, respectively. At 12 months, adjunctive coiling predicted occlusion (OR 0.260, p = 0.036), while male sex (OR 2.923, p = 0.032), aneurysm size (OR 3.584, p = 0.011), and incorporation of a branch vessel (OR 2.206, p = 0.035) predicted persistence. Notable variables that did not predict aneurysm occlusion were prior treatments, vessel of origin, fusiform morphology, and number of devices used.

CONCLUSIONS

This is the largest single-institution study showing high rates of anterior circulation aneurysm occlusion after Pipeline embolization. Predictors of persistence after flow diversion included increasing aneurysm size and incorporated branch vessel, whereas adjunctive coiling predicted occlusion.

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Matthew T. Bender, Geoffrey P. Colby, Li-Mei Lin, Bowen Jiang, Erick M. Westbroek, Risheng Xu, Jessica K. Campos, Judy Huang, Rafael J. Tamargo and Alexander L. Coon

OBJECTIVE

Flow diversion requires neointimal stent overgrowth to deliver aneurysm occlusion. The existing literature on aneurysm occlusion is limited by heterogeneous follow-up, variable antiplatelet regimens, noninvasive imaging modalities, and nonstandard occlusion assessment. Using a large, single-center cohort with low attrition and standardized antiplatelet tapering, the authors evaluated outcomes after flow diversion of anterior circulation aneurysms to identify predictors of occlusion and aneurysm persistence.

METHODS

Data from a prospective, IRB-approved database was analyzed for all patients with anterior circulation aneurysms treated by flow diversion with the Pipeline embolization device (PED) at the authors’ institution. Follow-up consisted of catheter cerebral angiography at 6 and 12 months postembolization. Clopidogrel was discontinued at 6 months and aspirin was reduced to 81 mg daily at 12 months. Occlusion was graded as complete, trace filling, entry remnant, or aneurysm filling. Multivariate logistic regression was performed to identify predictors of aneurysm persistence.

RESULTS

Follow-up catheter angiography studies were available for 445 (91%) of 491 PED procedures performed for anterior circulation aneurysms between August 2011 and August 2016. Three hundred eighty-seven patients accounted for these 445 lesions with follow-up angiography. The population was 84% female; mean age was 56 years and mean aneurysm size was 6.6 mm. Aneurysms arose from the internal carotid artery (83%), anterior cerebral artery (13%), and middle cerebral artery (4%). Morphology was saccular in 90% of the lesions, and 18% of the aneurysms has been previously treated. Overall, complete occlusion was achieved in 82% of cases at a mean follow-up of 14 months. Complete occlusion was achieved in 72%, 78%, and 87% at 6, 12, and 24 months, respectively. At 12 months, adjunctive coiling predicted occlusion (OR 0.260, p = 0.036), while male sex (OR 2.923, p = 0.032), aneurysm size (OR 3.584, p = 0.011), and incorporation of a branch vessel (OR 2.206, p = 0.035) predicted persistence. Notable variables that did not predict aneurysm occlusion were prior treatments, vessel of origin, fusiform morphology, and number of devices used.

CONCLUSIONS

This is the largest single-institution study showing high rates of anterior circulation aneurysm occlusion after Pipeline embolization. Predictors of persistence after flow diversion included increasing aneurysm size and incorporated branch vessel, whereas adjunctive coiling predicted occlusion.

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Geoffrey P. Colby, Bowen Jiang, Matthew T. Bender, Narlin B. Beaty, Erick M. Westbroek, Risheng Xu, Li-Mei Lin, Jessica K. Campos, Rafael J. Tamargo, Judy Huang, Alan R. Cohen and Alexander L. Coon

Intracranial aneurysms in the pediatric population are rare entities. The authors recently treated a 9-month-old infant with a 19-mm recurrent, previously ruptured, and coil-embolized left middle cerebral artery (MCA) pseudoaneurysm, which was treated definitively with single-stage Pipeline-assisted coil embolization. The patient was 5 months old when she underwent resection of a left temporal Grade 1 desmoplastic infantile ganglioglioma at an outside institution, which was complicated by left MCA injury with a resultant 9-mm left M1 pseudoaneurysm. Within a month, the patient had two aneurysmal rupture events and underwent emergency craniectomy for decompression and evacuation of subdural hematoma. The pseudoaneurysm initially underwent coil embolization; however, follow-up MR angiography (MRA) revealed aneurysm recanalization with saccular enlargement to 19 mm. The patient underwent successful flow diversion–assisted coil embolization at 9 months of age. At 7 months after the procedure, follow-up MRA showed complete aneurysm occlusion without evidence of in-stent thrombosis or stenosis. Experience with flow diverters in the pediatric population is still in its early phases, with the youngest reported patient being 22 months old. In this paper the authors report the first case of such a technique in an infant, whom they believe to be the youngest patient to undergo cerebral flow diversion treatment.

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Wuyang Yang, Risheng Xu, Jose L. Porras, Clifford M. Takemoto, Syed Khalid, Tomas Garzon-Muvdi, Justin M. Caplan, Geoffrey P. Colby, Alexander L. Coon, Rafael J. Tamargo, Judy Huang and Edward S. Ahn

OBJECTIVE

Sickle cell disease (SCD) in combination with moyamoya syndrome (MMS) represents a rare complication of SCD, with potentially devastating neurological outcomes. The effectiveness of surgical revascularization in this patient population is currently unclear. The authors’ aim was to determine the effectiveness of surgical intervention in their series of SCD-MMS patients by comparing stroke recurrence in those undergoing revascularization and those undergoing conservative transfusion therapy.

METHODS

The authors performed a retrospective chart review of patients with MMS who were seen at the Johns Hopkins Medical Institution between 1990 and 2013. Pediatric patients (age < 18 years) with confirmed diagnoses of SCD and MMS were included. Intracranial stroke occurrence during the follow-up period was compared between surgically and conservatively managed patients.

RESULTS

A total of 15 pediatric SCD-MMS patients (28 affected hemispheres) were included in this study, and all were African American. Seven patients (12 hemispheres) were treated with indirect surgical revascularization. The average age at MMS diagnosis was 9.0 ± 4.0 years, and 9 patients (60.0%) were female. Fourteen patients (93.3%) had strokes before diagnosis of MMS, with an average age at first stroke of 6.6 ± 3.9 years. During an average follow-up period of 11.6 years, 4 patients in the conservative treatment group experienced strokes in 5 hemispheres, whereas no patient undergoing the revascularization procedure had any strokes at follow-up (p = 0.029). Three patients experienced immediate postoperative transient ischemic attacks, but all recovered without subsequent strokes.

CONCLUSIONS

Indirect revascularization is suggested as a safe and effective alternative to the best medical therapy alone in patients with SCD-MMS. High-risk patients managed on a regimen of chronic transfusion should be considered for indirect revascularization to maximize the effect of stroke prevention.