J Neurosurg Pediatrics 12:344–350, 2013 ©AANS, 2013

An institutional series and literature review of pial arteriovenous fistulas in the pediatric population Clinical article Peter J. Madsen, M.D., M.B.E.,1 Shih-Shan Lang, M.D.,1 Jared M. Pisapia, M.D., M.T.R.,1 Phillip B. Storm, M.D.,1,3 Robert W. Hurst, M.D., 2 and Gregory G. Heuer, M.D., Ph.D.1,3 Departments of 1Neurosurgery and 2Radiology, Hospital of the University of Pennsylvania; and 3Division of Neurosurgery, Children’s Hospital of Philadelphia, Pennsylvania Object. Pial arteriovenous fistulas (PAVFs) are a rare form of cerebrovascular disease that tend to be overrepresented in the pediatric population. There have been limited studies of the clinical features and outcomes in this group of patients. Here, the authors attempt to better delineate this clinical entity with institutional cases and a review of the literature. Methods. A retrospective review of cases at our institution was performed to identify all pediatric patients treated for a PAVF between 2000 and 2012. Results. Five patients treated for a PAVF were identified. Patients had a mean age of 1.9 years at diagnosis, and the most common presenting symptoms were seizure and macrocephaly. Patients were treated primarily with embolization, and 3 patients required both N-butyl cyanoacrylate (NBCA) glue and coiling. Four of the patients had complete obliteration of the PAVF and had a pediatric overall performance category score of either 1 (n = 3) or 2 (n = 1) at follow-up. There was 1 death due to heart failure. Analysis of the literature review suggested that a younger age or presence of intracerebral hemorrhage (ICH) or congestive heart failure (CHF) at presentation likely predicts a worse prognosis. Older patients presented more often with ICH, whereas younger patients presented significantly more often in CHF. The majority of pediatric patients reported on in the literature were treated with endovascular embolization, most commonly with NBCA glue alone. Most patients (65.4%) in the literature had an excellent outcome without neurological deficit. Conclusions. Pial AVFs represent a serious yet rare form of cerebrovascular disease. Pediatric patients with ICH or CHF at presentation or those who are very young are likely to have a worse prognosis. Endovascular management of these patients has greatly changed the natural history of this disease, but the complication and mortality rates suggest the need for continued insights and advances in treatment. (http://thejns.org/doi/abs/10.3171/2013.6.PEDS13110)

Key Words      •      pial arteriovenous fistula      •      AVF      •      varix      •      surgery      •      embolization      •      pediatric      •      vascular disorders

P

(or nongalenic) arteriovenous fistulas are a rare form of cerebrovascular disease consisting of a high-flow connection between one or more pial arteries and the venous circulation.18,48,53 They are typically classified as a subtype of pial AVMs, yet are differentiated by their lack of an intervening nidus between the arterial feeder(s) and venous drainage.24 Pial AVFs have been found to account for 4.7% of pial AVMs;47 however, they tend to be overrepresented in the pediatric populaial

Abbreviations used in this paper: AVM = arteriovenous malformation; CHF = congestive heart failure; CN = cranial nerve; GDC = Guglielmi Detachable Coil; ICH = intracerebral hemorrhage; MCA = middle cerebral artery; NBCA = N-butyl cyanoacrylate; PAVF = pial arteriovenous fistula; PCA = posterior cerebral artery.

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tion at an increased incidence of 17.2% of pial AVMs.52 The clinical features of PAVFs, especially in children, have been described in limited detail in the literature due to the rarity of this entity. It has been suggested that there is an increased incidence of venous varices, a higher rate of seizures, and a lower rate of hemorrhage in children than in adults.53 The management strategies for PAVFs have undergone considerable evolution with the advancement and refinement of endovascular techniques. Despite advances in treatment, PAVFs remain a potentially life-threatening condition, necessitating further evaluation and investigation. In this study, we identify and delineate the clinical course of pediatric patients with PAVFs at our tertiary care children’s hospital. In addition, because of the rarity J Neurosurg: Pediatrics / Volume 12 / October 2013

Pial arteriovenous fistulas in the pediatric population of pediatric PAVFs, we performed a literature review of published cases.

Methods Study Design and Clinical Data

A retrospective review of cases at a single tertiary referral children’s hospital was performed to identify patients who demonstrated angiographic evidence of a PAVF between 2000 and 2012. Patients older than 18 years and those with an isolated AVM or vein of Galen malformation were excluded. Patient demographics, clinical presentation, radiographic images, angioarchitecture, treatment details, complications, and outcomes were extracted from inpatient hospital records and neurosurgical outpatient clinic charts. Only patients with angiographic features of a PAVF such as rapid venous filling, large arterial feeder(s), and direct filling of a venous varix were included. Neurological outcomes were assessed using the pediatric overall performance category.11,12

Literature Review

We performed a MEDLINE and a Cochrane database search of articles published in the English-language literature before December 2012 containing the terms “pial arteriovenous fistula” and “nongalenic arteriovenous fistula.” We supplemented our search using the “Related Citations” feature of PubMed and performing manual reviews of the bibliographies of selected articles. Only studies in which individual patient data could be clearly extracted were included in our review. Patients with AVMs, vein of Galen malformations, or with unclear angiographic characterization were excluded.

Results Summary of Cases

Between 2000 and 2012, 5 patients were identified as meeting our inclusion criteria for a PAVF (Tables 1 and 2). Individual patient cases are described.

Case 1. This 3-month-old boy, who was previously reported on in the literature,45 presented with evidence of right CN III palsy, emesis, and a cranial bruit. Magnetic resonance imaging and MR angiography and conventional cerebral angiography demonstrated a large (6.6 × 4.4 × 4.7–cm) dilation of the M2 branch of the right MCA, causing mass effect on the midbrain, pons, and CN III. There was direct communication of this dilation with enlarged venous drainage into the junction of the right transverse and sigmoid sinuses. Embolization of the fistula was performed using GDCs and NBCA glue, achieving minimal residual filling. The procedure was complicated by ischemic stroke of the right MCA territory, resulting in mild hemiparesis. At 1 year of follow-up, complete occlusion of the fistula was achieved. The patient’s hemiparesis improved; however, he ultimately required medial and lateral rectus muscle resection to correct persistent CN III dysfunction. Case 2. This 9-month-old boy with seizures, increas-

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ing head circumference, and delay of motor development was found to have angiographic evidence of a mixed AVM and PAVF with venous varix fed by the right angular artery that drained into the right sigmoid sinus. Embolization of both the AVM and PAVF was performed using NBCA glue and resulted in complete occlusion. The residual nidus of the AVM was resected. There were no complications from either procedure, and the patient remained in excellent condition and seizure free during 4 years of follow-up.

Case 3. This 6-month-old boy who presented with atonic seizures and macrocephaly was found on CT to have a thrombosed varix. Magnetic resonance angiography, MR venography, and cerebral angiography confirmed the presence of an occipital PAVF fed by the right MCA and draining into the straight and right transverse sinuses via the vein of Labbé (Fig. 1A–C). Embolization of the fistula was performed using detachable coils and NBCA glue, with postembolization angiography showing minimal flow through the PAVF. Radiographic follow-up over the next 3 months demonstrated complete obliteration of the fistula (Fig. 1D). After the procedure, the patient neglected stimuli presented in his left visual field, but this finding resolved over 3 months. At 3 years followup the patient was neurologically stable and seizure free. Case 4. This 1-week-old girl presented with CHF and associated pulmonary hypertension. Magnetic resonance imaging, MR angiography, MR venography, and cerebral angiography demonstrated a large PAVF adjacent to the midbrain comprising numerous dilated arterial feeders arising from the right posterior choroidal artery and right posterior inferior cerebellar artery with drainage to the deep cerebral veins. The malformation was associated with mild hydrocephalus. An attempt at embolization was performed using NBCA and detachable coils with incomplete obliteration and residual arterial feeding vessels. Postembolization ultrasonography of the head showed evidence of a possible thalamic infarct. The patient’s heart failure continued to worsen, and she died at 3 weeks of age of multisystem organ failure.

Case 5. This 8-year-old girl was found to have a left parietooccipital vascular anomaly on MRI during workup for multiple cutaneous hemangiomas present since birth. Genetic testing uncovered a RASA1 mutation passed along by her father who harbored the same mutation. RASA1-related disorders are characterized by face and appendicular capillary malformations as well as AVMs and/or AVFs in the skin, muscle, bone, spine, and brain.10 The patient was neurologically asymptomatic from the vascular lesion. On cerebral angiography, she was noted to have a multichannel PAVF that was fed by the left pericallosal and posterior cerebral arteries and drained via the straight sinus with an associated venous varix (Fig. 2A–C). Embolization was performed using multiple GDCs, with the achievement of immediate complete obliteration (Fig. 2D). The patient had no complications from the procedure and continued to be neurologically intact at 1 month of follow-up. 345

P. J. Madsen et al. TABLE 1: Patient characteristics* Case No.

Age at Dx, Sex

Presentation

1

3 mos, M

2

9 mos, M

3 4

6 mos, M 1 wk, F

5

8 yrs, F

CN III palsy, cranial bruit,  emesis seizure, macrocephaly,   developmental delay seizure, macrocephaly heart failure, pulmonary  HTN cutaneous hemangiomas

Location

Feeding Vessel

Draining Vessel

Varix

rt frontotemporal

M2 branch of MCA

rt transverse sinus

yes

rt temporoparietal

rt MCA

rt sigmoid sinus

yes

rt vein of Labbé deep cerebral  veins straight sinus

yes yes

rt occipital rt MCA interpeduncular fossa rt posterior choroidal   artery, rt PICA lt parietooccipital lt pericallosal artery, lt PCA

yes

*  Dx = diagnosis; HTN = hypertension; PICA = posterior inferior cerebellar artery.

Literature Review

Sixty-two papers were reviewed; 40 of which were considered suitable for the current study.1–9,13–17,20–23,26–28, 30–33,35–38,40–44,50–52,54–56 These studies included 27 case reports or series and 13 retrospective studies and yielded extractable data on 147 cases of intracranial PAVF in patients younger than 18 years old (Table 3). The mean age of patients in the literature was 5.02 years with a slight male predominance, and the most common presenting symptom was seizure, followed by CHF. The most common first-line treatment modality performed was embolization with NBCA glue, and the vast majority of patients had no complications and excellent neurological outcomes.

Discussion

Pial AVF is a rare form of cerebrovascular disease, with a reported incidence of 3%–7.3% in clinical series of AVMs in all age groups.40 This increases to a reportedly higher incidence of 17.2% of AVMs in the pediatric population.52 Limited distinction has been made between the clinical features of this disease in pediatric and adult patients. To better define the pathogenesis, clinical elements, therapeutic strategies, and outcomes of this disease in the pediatric population, we describe our experience with this clinical entity at our tertiary care children’s hospital

and interpret the data reported from our literature review of pediatric PAVFs. Clinical Presentation

Similar to vein of Galen aneurysmal malformations, the clinical presentation in pediatric patients with PAVFs tends to vary by age. Studies have suggested that neonates with a PAVF are more likely to present in CHF than older patients.18,40 This is further supported by the fact that 22 of the 28 patients in our literature review who presented with cardiac failure were in the neonatal period (< 28 days). The average age of patients presenting in CHF was 0.21 ± 0.52 years compared with 6.2 ± 5.4 years for those patients presenting without CHF (p < 0.0001, unpaired ttest). Our series also supported this association, as our patient who presented with CHF was only 1 week old (Table 1). The other 4 patients were all 3 months of age or older and did not have symptoms of heart failure. Historically, newborns with CHF due to a cranial arteriovenous shunt have a very poor prognosis that approached 100%, but advances in endovascular techniques in this population have improved outcomes significantly.13,40 Intracerebral hemorrhage at presentation is also suggested to be age dependent, in that it is typically seen as a presenting sign in older patients, especially those older than 15 years.53 In our literature review, the mean age of patients presenting with ICH was 6.4 ± 5.5 years versus a

TABLE 2: Treatment and patient outcomes* Case No.

Treatment Modality

Embolization Material

1

embol

NBCA, GDCs

2 3 4 5

embol, op‡ embol embol embol

NBCA NBCA, GDCs NBCA, GDCs GDCs

Complication

Fistula Occlusion

Outcome (POPC)†

Follow-Up (yrs)

MCA territory infarct, mild  hemiparesis none transient visual field neglect thalamic infarct none

100%

2

0.9

100% 100% incomplete 100%

1 1 6 1

4.2 2.8 NA 0.1

*  embol = embolization; NA = not applicable; POPC = pediatric overall performance category. †  Based on the system of Fiser11 and Fiser and colleagues:12 1 = good overall performance, 2 = mild overall disability, 6 = brain death. ‡  Surgery was performed only on the nidal portion of the patient’s associated AVM.

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Pial arteriovenous fistulas in the pediatric population

Fig. 1.  Case 3. Preembolization lateral (A) and anteroposterior (B) digital subtraction angiograms and MR angiogram (C) showing a right temporooccipital PAVF arising from an enlarged, distal MCA branch with deep (vein of Labbé) and superficial drainage and an associated venous varix. Postembolization MR angiogram (D) demonstrating obliteration of the PAVF.

mean of 4.8 ± 5.4 years for those patients presenting without ICH (p = 0.19, unpaired t-test), although this finding was not statistically significant. Treatment of PAVFs

The vast majority of pediatric patients with PAVF in the literature were treated with endovascular embolization (113 patients [83.7%]) rather than surgical intervention (23 patients [17.0%]) (Table 3). Of the 23 reports involving surgical interventions, 19 of these cases were reported prior to 2002, which represents a significant shift in management strategies with the advancement of the endovascular field. In terms of the type of embolic material used, NBCA glue alone was the most common (53 [46.9%] of 113) followed by coiling alone (26 [23.0%] of 113) and combined coiling and NBCA glue (21 [18.6%] of 113; Table 3). Of the 108 patients who underwent embolization as their initial treatment and had data reported on fistula obliteration, 74 (68.5%) had angiographic evidence of complete obliteration of their PAVF. Of the 34 patients who continued to have residual filling of the PAVF, 24 (70.6%) had initially received NBCA glue alone, 7 (20.6%) received coiling and NBCA glue, 2 (5.9%) received coiling alone, and 1 (2.9%) received balloon occlusion. In our series, all patients were treated with endovascular embolization, with one patient subsequently undergoing open resection of an associated AVM (Table 2). Three of the patients from our institutional series required combined embolization material

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Fig. 2.  Case 5. Preembolization digital subtraction angiograms of the lateral left internal carotid artery injection (A), lateral left vertebral artery injection (B), and superimposed, separate carotid and vertebral injections (C) showing a left parietooccipital PAVF arising from the left pericallosal and PCA with drainage into the straight sinus and an associated venous varix (circle). Embolization was performed through a microcatheter threaded from the vertebral artery through the PCA across the fistula and into the distal anterior cerebral artery. Postembolization angiogram demonstrating obliteration of the PAVF with no filling from either the internal carotid artery or vertebral artery on separate injections (circle, D).

(GDCs and NBCA glue) to achieve complete obliteration of the PAVF. Notably, there were very few patients (4 [3.5%] of 113) in the literature review whose PAVFs were embolized with Onyx, which contrasts with the increasing usage of this agent for treating other cerebrovascular malformations, especially in the adult population. At our institution, NBCA glue is preferred over Onyx, because Onyx utilization typically extends the embolization29 and requires more fluoroscopic time,49 which potentially increases the detrimental effects of ionizing radiation on children’s developing nervous systems. Furthermore, the potentially large doses of Onyx required for embolization of these fistulas increases the risk for the rare complication of DMSO (dimethyl sulfoxide)–related pulmonary toxicity39,46 associated with Onyx. This pulmonary toxicity may exacerbate the preexisting cardiovascular and pulmonary comorbidities often seen in this group of children. Complications and Outcomes

Procedure-related death was infrequent in the literature review (3.0%), representing 4 patients who died of ICH after embolization.30,40 The most common procedurerelated complication reported in the literature was the development of new intracranial hemorrhage occurring in 17 (12.6%) of 135 patients, followed by the development of new neurological deficit (10 [7.4%] of 135 patients; Table 3). Complication rates in series of patients with related malformations, such as vein of Galen aneurysmal malformations, have been reported at 17%–36%.19,25,34 Among cases in the literature in which outcome was 347

P. J. Madsen et al. TABLE 3: Composite data from a literature review of 147 pediatric patients presenting with PAVFs* Parameter patient demographics (n = 147)  age   mean   range   male/female ratio   male   female common presenting signs/symptoms (n = 147)  seizure  CHF   neurological deficit  headache  hemorrhage  macrocephaly   genetic syndrome   developmental delay presence of varix (n = 119)†  present  absent treatment modality (n = 135)‡   surgical clipping/resection  embolization   w/ glue   w/ coiling    w/ glue & coiling   balloon occlusion   Onyx   unknown material  SRS  observation complications (n = 135)§,¶  none  any   procedure-related death   any intracranial hemorrhage   ICH   IVH   SAH   SDH   new neurological deficit   coil/balloon migration   secondary DAVF   CSF diversion required   venous sinus occlusion   venous infarct  sepsis   heart failure

Value

5.02 yrs 0 days–17 yrs 1.5:1 88 (59.9) 59 (40.1) 36 (24.5) 28 (19.0) 27 (18.4) 24 (16.3) 22 (15.0) 21 (14.3) 19 (12.9) 12 (8.2) 110 (92.4) 9 (7.6) 23 (17.0) 113 (83.7) 53 (46.9) 26 (23.0) 21 (18.6) 11 (9.7) 4 (3.5) 2 (1.8) 1 (0.7) 7 (5.2) 102 (75.6) 34 (25.2) 4 (3.0) 17 (12.6) 8 (5.9) 4 (3.0) 3 (2.2) 2 (1.5) 10 (7.4) 6 (4.4) 4 (3.0) 3 (2.2) 3 (2.2) 1 (0.7) 1 (0.7) 1 (0.7) (continued)

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TABLE 3: Composite data from a literature review of 147 pediatric patients presenting with PAVFs* (continued) Parameter complications (n = 135)§,¶ (continued)  seizure   mental retardation   glued microcatheter   pedicle embolization outcome (n = 130)¶   excellent (no deficit)   good (minimal deficit)  poor  death average LOF (n = 49)¶

Value 1 (0.7) 1 (0.7) 1 (0.7) 1 (0.7) 85 (65.4) 21 (16.2) 13 (10.0) 11 (8.5) 17.4 mos

*  Unless otherwise noted, values represent the number of patients (%). DAVF = dural arteriovenous fistula; IVH = intraventricular hemorrhage; LOF = length of follow-up; SAH = subarachnoid hemorrhage; SDH = subdural hemorrhage; SRS = stereotactic radiosurgery. †  Includes only cases in which the presence or absence of varix was noted or could be determined from images provided. ‡  The sum of individual treatment numbers is greater than the total number of treated patients because some patients had multiple interventions. §  The sum of individual complications is greater than the total number of patients with complications because some patients had multiple complications. ¶  Includes only cases in which individual complications, outcomes, or length of follow-up was reported.

clearly reported, the majority of patients (85 [65.4%] of 130) achieved an excellent outcome, defined as the absence of any neurological deficit at follow-up. Twenty-one patients (16.2%) were noted to have a minimal neurological deficit at follow-up, considered a good outcome, and 13 (10.0%) had a poor outcome, representing a significant neurological deficit at follow-up (for example, persistent hemiparesis, mental retardation, and persistent visual field deficit). In the literature review, 11 patients died (8.5%); most deaths were due to either ICH (n = 5) or CHF (n = 4). The 1 death reported in our series was attributable to the patient’s CHF rather than any neurological compromise. Patients with a clearly reported outcome in the literature who presented with ICH had a higher mortality rate than those without ICH on presentation (4 [18.2%] of 22 vs 7 [6.5%] of 108, respectively; p = 0.09, Fisher exact test). In addition to ICH, age at diagnosis also seemed to be a potential indicator of increased mortality. In the reviewed literature the mean age at diagnosis of those patients who died was 2.3 ± 3.7 years compared with 5.6 ± 5.5 years for those who survived (p = 0.05, unpaired ttest). The observation of a worse prognosis in younger patients (especially those < 2 years) has also been described by Hetts et al., who attributed it to the high rate of severe, life-threatening CHF seen in these patients.18 In our literature review, 6 (26.1%) of 23 patients with a clear outcome reported, and who presented with CHF, died, which represents a significantly higher mortality rate compared J Neurosurg: Pediatrics / Volume 12 / October 2013

Pial arteriovenous fistulas in the pediatric population with the 5 (4.7%) of 107 who died but presented without CHF symptoms (p = 0.004, Fisher exact test). This finding would support the notion that CHF at presentation is predictive of a worse prognosis in pediatric patients with PAVFs. Our study is limited by the number of cases and its retrospective nature, which makes it difficult to form definitive conclusions about the pathogenesis, clinical course, and optimal treatment strategy for pediatric patients with PAVF. Our review of the literature is subject to reporting bias and potentially represents a more historical perspective rather than a current account of this disease and its treatment.

Conclusions

This study demonstrates both the serious nature of PAVF and its heterogeneous presentation. Aggregated data from the literature suggest that a younger age or presence of ICH or CHF at presentation may signify a worse prognosis. Furthermore, older patients seem to present with more frequent ICH, whereas younger patients presented significantly more often in CHF. The treatment of PAVFs has greatly changed with advanced endovascular techniques. As shown in our series and with a review of the literature, PAVFs are typically amenable to endovascular intervention; however, they may require more than one type of embolization material to achieve complete obliteration. As with many complex medical conditions, pediatric patients with PAVFs require the input of a team of physicians in varying disciplines—neurosurgery, interventional radiology, neurology, and pediatrics—to develop and implement an effective treatment plan. 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: Heuer, Madsen, Lang, Storm, Hurst. Acquisition of data: Madsen, Lang, Pisapia, Hurst. Analysis and interpretation of data: Heuer, Madsen, Lang, Pisapia, Hurst. Drafting the article: Heuer, Madsen, Lang, Storm, Hurst. 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: Heuer. Statistical analysis: Madsen, Lang. Study supervision: Heuer, Storm, Hurst. References   1.  Aguilar M, González A, López A, Gutiérrez I, Durand F, Mayol A: Endovascular treatment of a pial arteriovenous fistula with occipital remodeling secondary to giant torcular dilation. J Child Neurol 26:1015–1020, 2011   2.  Almeida GM, Shibata MK: Hemispheric arteriovenous fistulae with giant venous dilation. Childs Nerv Syst 6:216–219, 1990   3.  Antunes JL, DiGiacinto GV, Michelsen WJ: Giant hemispheric arteriovenous fistula in an infant. Surg Neurol 7:45–48, 1977   4.  Aoki N, Sakai T, Oikawa A: Intracranial arteriovenous fistula manifesting as progressive neurological deterioration in an infant: case report. Neurosurgery 28:619–623, 1991   5.  Barnwell SL, Ciricillo SF, Halbach VV, Edwards MS, Cogen PH: Intracerebral arteriovenous fistulas associated with intra-

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Manuscript submitted March 6, 2013. Accepted June 20, 2013. Please include this information when citing this paper: published online August 2, 2013; DOI: 10.3171/2013.6.PEDS13110. Address correspondence to: Gregory G. Heuer, M.D., Ph.D., Division of Neurosurgery, The Children’s Hospital of Philadelphia, 34th St. & Civic Center Blvd., Philadelphia, PA 19104. email: [email protected].

J Neurosurg: Pediatrics / Volume 12 / October 2013

An institutional series and literature review of pial arteriovenous fistulas in the pediatric population: clinical article.

Pial arteriovenous fistulas (PAVFs) are a rare form of cerebrovascular disease that tend to be overrepresented in the pediatric population. There have...
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