J Neurosurg Pediatrics 13:647–649, 2014 ©AANS, 2014
Development of a de novo arteriovenous malformation after bilateral revascularization surgery in a child with moyamoya disease Case report Miki Fujimura, M.D., Ph.D.,1,2 Naoto Kimura, M.D., Ph.D., 2 Masayuki Ezura, M.D., Ph.D., 2 Kuniyasu Niizuma, M.D., Ph.D.,1,2 Hiroshi Uenohara, M.D., Ph.D., 2 and Teiji Tominaga, M.D., Ph.D.1 Department of Neurosurgery, Tohoku University Graduate School of Medicine; and 2Department of Neurosurgery, National Hospital Organization Sendai Medical Center, Sendai, Japan
1
The development of a de novo arteriovenous malformation (AVM) in patients with moyamoya disease is extremely rare. A 14-year-old girl developed an AVM in the right occipital lobe during the 4-year postoperative period following successful bilateral revascularization surgeries. She suffered a transient ischemic attack with hemodynamic compromise of the bilateral hemispheres at the age of 10 years. Results of an initial examination by 1.5-T MRI and MR angiography satisfied the diagnostic criteria of moyamoya disease but failed to detect any vascular malformation. Bilateral direct and indirect revascularization surgeries in the anterior circulation relieved her symptoms, and she underwent MRI and MR angiography follow-up every year after surgery. Serial T2-weighted MRI revealed the gradual appearance of flow voids in the right occipital lobe during the follow-up period. Magnetic resonance angiography ultimately indicated the development of an AVM 4 years after these surgeries when catheter angiography confirmed the diagnosis of an AVM in the right occipital lobe. The AVM remained asymptomatic, and the patient remained free of cerebrovascular events during the time she was observed by the authors. Acquired AVM in moyamoya disease is extremely rare, with only 3 pediatric cases including the present case being reported in the literature. The development of a de novo AVM in a postoperative patient with moyamoya disease appears to be unique, and this case may provide insight into the dynamic pathology of AVMs. (http://thejns.org/doi/abs/10.3171/2014.3.PEDS13610)
Key Words • arteriovenous malformation • moyamoya disease • de novo development • vascular disorders
A
rteriovenous malformation (AVM) is a congenital cerebrovascular disease that is believed to appear at the early embryonic stage of 3 weeks; however, evidence suggesting its dynamic nature of rapid growth, recurrence after total removal, and de novo development, despite its “congenital” nature, is increasing.2,7 Moyamoya disease is a chronic occlusive cerebrovascular disease with unknown etiology characterized by bilateral steno-occlusive changes in the terminal portion of the internal carotid artery and an abnormal vascular network at the base of the brain.4 Although the rare association of moyamoya disease with an AVM has been documented in detail, the development of de novo AVMs in patients with moyamoya disease is extremely rare; it has been reported in only 2 pediatric cases.3,5 Here, we describe a 10-year-
Abbreviations used in this paper: AVM = arteriovenous malformation; PCA = posterior cerebral arery.
J Neurosurg: Pediatrics / Volume 13 / June 2014
old girl with ischemic-onset moyamoya disease who underwent successful bilateral revascularization surgeries and developed acquired AVM in the occipital lobe during the 4-year follow-up period.
Case Report
A 10-year-old girl had repeated weakness in her bilateral upper extremities, was diagnosed with moyamoya disease, and was subsequently transferred to our hospital. A neurological examination showed no abnormalities, and 1.5-T MR angiography revealed steno-occlusive changes at the terminal portion of the bilateral internal carotid arteries (Fig. 1A). No abnormality was found in the posterior circulation, including the right posterior ceThis article contains some figures that are displayed in color online but in black-and-white in the print edition.
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Fig. 1. A: Initial MR angiogram demonstrating steno-occlusive changes at the terminal portions of the bilateral internal carotid arteries (arrows). B–F: Temporal profile of T2-weighted MR imaging before surgery (B and C) and 1 year (D), 3 years (E), and 4 years (F) after bilateral direct/indirect revascularization surgeries. Preoperative MR images demonstrated several flow voids at the bilateral basal ganglia (asterisks in B), without any abnormality in the right occipital lobe (C). Flow voids were evident in the right occipital lobe 3 (arrow in E) and 4 (arrow in F) years after surgeries, while it was equivocal 1 year after the surgeries (D). G: Magnetic resonance angiogram obtained 4 years after the surgeries, demonstrating apparent visualization of the nidus in the right occipital lobe (arrow). H: Right anterior oblique view of the right vertebral angiogram revealing a right occipital lobe AVM (arrow).
rebral artery (PCA) territory on MR angiography (Fig. 1A). Axial T2-weighted MRI showed several flow voids at the bilateral basal ganglia (Fig. 1B asterisks), but none in the occipital lobe (Fig. 1C). Since SPECT revealed apparent hemodynamic compromise, the patient underwent bilateral revascularization surgeries with superficial temporal artery–middle cerebral artery anastomosis with indirect pial synangiosis as previously described.1 After the completion of superficial temporal artery–middle cerebral artery anastomosis, conventional encephalo-duromyo-synangiosis was performed at the territory of the middle cerebral artery (MCA). No additional bur holes or extended indirect bypass procedure was performed in the posterior circulation. The patient’s postoperative course was uneventful, and her transient ischemic attacks completely disappeared after the surgeries. She underwent routine follow-up MR imaging/angiography every year at an outpatient clinic. Four years postoperatively, T2-weighted imaging revealed an apparent flow void in the right occipital lobe (Fig. 1F), and MR angiography showed an AVM in the vascular territory of the right PCA. Flow voids at the bilateral basal ganglia were partially decreased by the effect of revascularization surgeries. Catheter angiography confirmed a Spetzler-Martin Grade II AVM in the right occipital lobe. A retrospective inspection of T2-weighted 648
images obtained 3 years postoperatively identified a flow void in the right occipital lobe (Fig. 1E arrow). In light of a previous report indicating the efficacy of radiosurgery for AVM associated with moyamoya disease,6 we proposed Gamma Knife radiosurgery for the de novo AVM in this patient. We introduced this patient and family to the outpatient consultation service for Gamma Knife radiosurgery, but the patient and her parents finally chose conservative observation. The patient remained asymptomatic after the surgeries; we have continued to observe the patient and have observed no cerebrovascular events for 2 years.
Discussion
We demonstrated the temporal profile of MRI findings for the development of AVM during a 4-year postoperative period after bilateral revascularization surgeries for moyamoya disease in a 14-year-old girl. The exact mechanism by which an acquired AVM developed in the vascular territory supplied by the PCA without steno-occlusive changes is unknown. In light of the absence of hemodynamic compromise in the occipital lobe, as shown by SPECT pre- and postoperatively, cerebral ischemia was not likely to be the major trigger for the development of the acquired AVM. Because we did not perform extended indirect pial synanJ Neurosurg: Pediatrics / Volume 13 / June 2014
De novo AVM in moyamoya disease giosis and/or an additional bur hole technique in the posterior circulation, the initiation of AVM development could not have been due to the iatrogenic arteriovenous fistula at the initial surgery for moyamoya disease. Alternatively, based on the absence of catheter angiography at the initial onset of moyamoya disease as well as on the classic observation that AVM is a congenital disease, we do not completely rule out the possibility that the patient initially had a micro-AVM or small arteriovenous fistula before bilateral revascularization, which was not evident on MRI. From the viewpoint of basic pathology, moyamoya disease and an AVM are known to have similar biological backgrounds of the increased expression of angiogenic factors such as vascular endothelial growth factor, as well as inflammatory molecules, including tumor necrosis factor–a, interleukin-6, and matrix metalloproteinases.4,7 The expression of these molecules in moyamoya disease could have caused the acquired AVM to develop in the present case. Alternatively, the development of the de novo AVM in the present case may provide an insight into elucidating the dynamic pathology of AVMs. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Fujimura. Acquisition of data: Fujimura, Kimura, Ezura, Niizuma. Analysis and interpretation of data: Fujimura. Drafting the article: Fujimura. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Fujimura. Administrative/technical/material support: Kimura, Niizuma. Study supervision: Tominaga. References 1. Fujimura M, Shimizu H, Inoue T, Mugikura S, Saito A, Tomi-
J Neurosurg: Pediatrics / Volume 13 / June 2014
naga T: Significance of focal cerebral hyperperfusion as a cause of transient neurologic deterioration after extracranialintracranial bypass for moyamoya disease: comparative study with non-moyamoya patients using N-isopropyl-p-[(123)I] iodoamphetamine single-photon emission computed tomography. Neurosurgery 68:957–965, 2011 2. Gonzalez LF, Bristol RE, Porter RW, Spetzler RF: De novo presentation of an arteriovenous malformation. Case report and review of the literature. J Neurosurg 102:726–729, 2005 3. O’Shaughnessy BA, DiPatri AJ Jr, Parkinson RJ, Batjer HH: Development of a de novo cerebral arteriovenous malformation in a child with sickle cell disease and moyamoya arteriopathy. Case report. J Neurosurg 102 (2 Suppl):238–243, 2005 4. Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis: Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52: 245–266, 2012 5. Schmit BP, Burrows PE, Kuban K, Goumnerova L, Scott RM: Acquired cerebral arteriovenous malformation in a child with moyamoya disease. Case report. J Neurosurg 84:677–680, 1996 6. Seol HJ, Kim DG, Oh CW, Han DH: Radiosurgical treatment of a cerebral arteriovenous malformation in a patient with moyamoya disease: case report. Neurosurgery 51:478–482, 2002 7. Sturiale CL, Puca A, Sebastiani P, Gatto I, Albanese A, Di Rocco C, et al: Single nucleotide polymorphisms associated with sporadic brain arteriovenous malformations: where do we stand? Brain 136:665–681, 2013
Manuscript submitted November 18, 2013. Accepted March 17, 2014. Please include this information when citing this paper: published online April 18, 2014; DOI: 10.3171/2014.3.PEDS13610. Address correspondence to: Miki Fujimura, M.D., Ph.D., Department of Neurosurgery, Tohoku University Graduate School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan. email: [email protected].
649
Development of a de novo arteriovenous malformation after bilateral revascularization surgery in a child with moyamoya disease Case report Miki Fujimura, M.D., Ph.D.,1,2 Naoto Kimura, M.D., Ph.D., 2 Masayuki Ezura, M.D., Ph.D., 2 Kuniyasu Niizuma, M.D., Ph.D.,1,2 Hiroshi Uenohara, M.D., Ph.D., 2 and Teiji Tominaga, M.D., Ph.D.1 Department of Neurosurgery, Tohoku University Graduate School of Medicine; and 2Department of Neurosurgery, National Hospital Organization Sendai Medical Center, Sendai, Japan
1
The development of a de novo arteriovenous malformation (AVM) in patients with moyamoya disease is extremely rare. A 14-year-old girl developed an AVM in the right occipital lobe during the 4-year postoperative period following successful bilateral revascularization surgeries. She suffered a transient ischemic attack with hemodynamic compromise of the bilateral hemispheres at the age of 10 years. Results of an initial examination by 1.5-T MRI and MR angiography satisfied the diagnostic criteria of moyamoya disease but failed to detect any vascular malformation. Bilateral direct and indirect revascularization surgeries in the anterior circulation relieved her symptoms, and she underwent MRI and MR angiography follow-up every year after surgery. Serial T2-weighted MRI revealed the gradual appearance of flow voids in the right occipital lobe during the follow-up period. Magnetic resonance angiography ultimately indicated the development of an AVM 4 years after these surgeries when catheter angiography confirmed the diagnosis of an AVM in the right occipital lobe. The AVM remained asymptomatic, and the patient remained free of cerebrovascular events during the time she was observed by the authors. Acquired AVM in moyamoya disease is extremely rare, with only 3 pediatric cases including the present case being reported in the literature. The development of a de novo AVM in a postoperative patient with moyamoya disease appears to be unique, and this case may provide insight into the dynamic pathology of AVMs. (http://thejns.org/doi/abs/10.3171/2014.3.PEDS13610)
Key Words • arteriovenous malformation • moyamoya disease • de novo development • vascular disorders
A
rteriovenous malformation (AVM) is a congenital cerebrovascular disease that is believed to appear at the early embryonic stage of 3 weeks; however, evidence suggesting its dynamic nature of rapid growth, recurrence after total removal, and de novo development, despite its “congenital” nature, is increasing.2,7 Moyamoya disease is a chronic occlusive cerebrovascular disease with unknown etiology characterized by bilateral steno-occlusive changes in the terminal portion of the internal carotid artery and an abnormal vascular network at the base of the brain.4 Although the rare association of moyamoya disease with an AVM has been documented in detail, the development of de novo AVMs in patients with moyamoya disease is extremely rare; it has been reported in only 2 pediatric cases.3,5 Here, we describe a 10-year-
Abbreviations used in this paper: AVM = arteriovenous malformation; PCA = posterior cerebral arery.
J Neurosurg: Pediatrics / Volume 13 / June 2014
old girl with ischemic-onset moyamoya disease who underwent successful bilateral revascularization surgeries and developed acquired AVM in the occipital lobe during the 4-year follow-up period.
Case Report
A 10-year-old girl had repeated weakness in her bilateral upper extremities, was diagnosed with moyamoya disease, and was subsequently transferred to our hospital. A neurological examination showed no abnormalities, and 1.5-T MR angiography revealed steno-occlusive changes at the terminal portion of the bilateral internal carotid arteries (Fig. 1A). No abnormality was found in the posterior circulation, including the right posterior ceThis article contains some figures that are displayed in color online but in black-and-white in the print edition.
647
M. Fujimura et al.
Fig. 1. A: Initial MR angiogram demonstrating steno-occlusive changes at the terminal portions of the bilateral internal carotid arteries (arrows). B–F: Temporal profile of T2-weighted MR imaging before surgery (B and C) and 1 year (D), 3 years (E), and 4 years (F) after bilateral direct/indirect revascularization surgeries. Preoperative MR images demonstrated several flow voids at the bilateral basal ganglia (asterisks in B), without any abnormality in the right occipital lobe (C). Flow voids were evident in the right occipital lobe 3 (arrow in E) and 4 (arrow in F) years after surgeries, while it was equivocal 1 year after the surgeries (D). G: Magnetic resonance angiogram obtained 4 years after the surgeries, demonstrating apparent visualization of the nidus in the right occipital lobe (arrow). H: Right anterior oblique view of the right vertebral angiogram revealing a right occipital lobe AVM (arrow).
rebral artery (PCA) territory on MR angiography (Fig. 1A). Axial T2-weighted MRI showed several flow voids at the bilateral basal ganglia (Fig. 1B asterisks), but none in the occipital lobe (Fig. 1C). Since SPECT revealed apparent hemodynamic compromise, the patient underwent bilateral revascularization surgeries with superficial temporal artery–middle cerebral artery anastomosis with indirect pial synangiosis as previously described.1 After the completion of superficial temporal artery–middle cerebral artery anastomosis, conventional encephalo-duromyo-synangiosis was performed at the territory of the middle cerebral artery (MCA). No additional bur holes or extended indirect bypass procedure was performed in the posterior circulation. The patient’s postoperative course was uneventful, and her transient ischemic attacks completely disappeared after the surgeries. She underwent routine follow-up MR imaging/angiography every year at an outpatient clinic. Four years postoperatively, T2-weighted imaging revealed an apparent flow void in the right occipital lobe (Fig. 1F), and MR angiography showed an AVM in the vascular territory of the right PCA. Flow voids at the bilateral basal ganglia were partially decreased by the effect of revascularization surgeries. Catheter angiography confirmed a Spetzler-Martin Grade II AVM in the right occipital lobe. A retrospective inspection of T2-weighted 648
images obtained 3 years postoperatively identified a flow void in the right occipital lobe (Fig. 1E arrow). In light of a previous report indicating the efficacy of radiosurgery for AVM associated with moyamoya disease,6 we proposed Gamma Knife radiosurgery for the de novo AVM in this patient. We introduced this patient and family to the outpatient consultation service for Gamma Knife radiosurgery, but the patient and her parents finally chose conservative observation. The patient remained asymptomatic after the surgeries; we have continued to observe the patient and have observed no cerebrovascular events for 2 years.
Discussion
We demonstrated the temporal profile of MRI findings for the development of AVM during a 4-year postoperative period after bilateral revascularization surgeries for moyamoya disease in a 14-year-old girl. The exact mechanism by which an acquired AVM developed in the vascular territory supplied by the PCA without steno-occlusive changes is unknown. In light of the absence of hemodynamic compromise in the occipital lobe, as shown by SPECT pre- and postoperatively, cerebral ischemia was not likely to be the major trigger for the development of the acquired AVM. Because we did not perform extended indirect pial synanJ Neurosurg: Pediatrics / Volume 13 / June 2014
De novo AVM in moyamoya disease giosis and/or an additional bur hole technique in the posterior circulation, the initiation of AVM development could not have been due to the iatrogenic arteriovenous fistula at the initial surgery for moyamoya disease. Alternatively, based on the absence of catheter angiography at the initial onset of moyamoya disease as well as on the classic observation that AVM is a congenital disease, we do not completely rule out the possibility that the patient initially had a micro-AVM or small arteriovenous fistula before bilateral revascularization, which was not evident on MRI. From the viewpoint of basic pathology, moyamoya disease and an AVM are known to have similar biological backgrounds of the increased expression of angiogenic factors such as vascular endothelial growth factor, as well as inflammatory molecules, including tumor necrosis factor–a, interleukin-6, and matrix metalloproteinases.4,7 The expression of these molecules in moyamoya disease could have caused the acquired AVM to develop in the present case. Alternatively, the development of the de novo AVM in the present case may provide an insight into elucidating the dynamic pathology of AVMs. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Fujimura. Acquisition of data: Fujimura, Kimura, Ezura, Niizuma. Analysis and interpretation of data: Fujimura. Drafting the article: Fujimura. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Fujimura. Administrative/technical/material support: Kimura, Niizuma. Study supervision: Tominaga. References 1. Fujimura M, Shimizu H, Inoue T, Mugikura S, Saito A, Tomi-
J Neurosurg: Pediatrics / Volume 13 / June 2014
naga T: Significance of focal cerebral hyperperfusion as a cause of transient neurologic deterioration after extracranialintracranial bypass for moyamoya disease: comparative study with non-moyamoya patients using N-isopropyl-p-[(123)I] iodoamphetamine single-photon emission computed tomography. Neurosurgery 68:957–965, 2011 2. Gonzalez LF, Bristol RE, Porter RW, Spetzler RF: De novo presentation of an arteriovenous malformation. Case report and review of the literature. J Neurosurg 102:726–729, 2005 3. O’Shaughnessy BA, DiPatri AJ Jr, Parkinson RJ, Batjer HH: Development of a de novo cerebral arteriovenous malformation in a child with sickle cell disease and moyamoya arteriopathy. Case report. J Neurosurg 102 (2 Suppl):238–243, 2005 4. Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis: Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52: 245–266, 2012 5. Schmit BP, Burrows PE, Kuban K, Goumnerova L, Scott RM: Acquired cerebral arteriovenous malformation in a child with moyamoya disease. Case report. J Neurosurg 84:677–680, 1996 6. Seol HJ, Kim DG, Oh CW, Han DH: Radiosurgical treatment of a cerebral arteriovenous malformation in a patient with moyamoya disease: case report. Neurosurgery 51:478–482, 2002 7. Sturiale CL, Puca A, Sebastiani P, Gatto I, Albanese A, Di Rocco C, et al: Single nucleotide polymorphisms associated with sporadic brain arteriovenous malformations: where do we stand? Brain 136:665–681, 2013
Manuscript submitted November 18, 2013. Accepted March 17, 2014. Please include this information when citing this paper: published online April 18, 2014; DOI: 10.3171/2014.3.PEDS13610. Address correspondence to: Miki Fujimura, M.D., Ph.D., Department of Neurosurgery, Tohoku University Graduate School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai 980-8574, Japan. email: [email protected].
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