Spinal juvenile (Type III) extradural-intradural arteriovenous malformations

Clinical article

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Object

Owing to their rarity, demographics, natural history, and treatment, results for spinal juvenile (Type III) extradural-intradural arteriovenous malformations (AVMs) are frequently only provided in case report format.

Methods

A pooled analysis was performed utilizing the PubMed database through April 2013. Individualized patient data were extracted to elucidate demographics, hemorrhage risk, and treatment result information.

Results

Twenty-nine studies describing 51 patients were included. The mean age at presentation was 15.0 ± 10.5 years with a slight male predilection (63%, 1.7:1 sex ratio). Presentation modality included progressive deficits in 35%, hemorrhage in 31%, acute deficits not attributed to hemorrhage in 22%, and asymptomatic/incidental in 12% of patients. The annual hemorrhage rate was 2.1%; statistically significant risk factors for hemorrhage included presentation age (HR 0.39 [95% CI 0.18–0.87]) and associated aneurysms (HR 8.74 [95% CI 1.76–43.31]). Seventy-seven percent of patients underwent treatment; after a mean follow-up of 2.6 ± 3.2 years, 73% were improved, 10% were the same, and 17% were worse neurologically. Of 25 cases with described angiographic results, 8 lesions were obliterated (32%). Of these 25 patients, 8 had AVMs with associated aneurysms, and the aneurysm was obliterated in all 8 patients. Over the course of 57.9 patient-years of follow-up, including 55.3 patient-years for partially treated AVMs, no hemorrhages were described, reflecting a trend toward protection from hemorrhage after treatment (p = 0.12, likelihood ratio test).

Conclusions

Spinal juvenile (Type III) extradural-intradural AVMs commonly present symptomatically. Associated arterial aneurysms increase their hemorrhage risk, and protection from hemorrhage may be achieved from partial obliteration of these lesions, particularly if targeted toward associated aneurysms.

Abbreviations used in this paper:AVF = arteriovenous fistula; AVM = arteriovenous malformation.

Abstract

Object

Owing to their rarity, demographics, natural history, and treatment, results for spinal juvenile (Type III) extradural-intradural arteriovenous malformations (AVMs) are frequently only provided in case report format.

Methods

A pooled analysis was performed utilizing the PubMed database through April 2013. Individualized patient data were extracted to elucidate demographics, hemorrhage risk, and treatment result information.

Results

Twenty-nine studies describing 51 patients were included. The mean age at presentation was 15.0 ± 10.5 years with a slight male predilection (63%, 1.7:1 sex ratio). Presentation modality included progressive deficits in 35%, hemorrhage in 31%, acute deficits not attributed to hemorrhage in 22%, and asymptomatic/incidental in 12% of patients. The annual hemorrhage rate was 2.1%; statistically significant risk factors for hemorrhage included presentation age (HR 0.39 [95% CI 0.18–0.87]) and associated aneurysms (HR 8.74 [95% CI 1.76–43.31]). Seventy-seven percent of patients underwent treatment; after a mean follow-up of 2.6 ± 3.2 years, 73% were improved, 10% were the same, and 17% were worse neurologically. Of 25 cases with described angiographic results, 8 lesions were obliterated (32%). Of these 25 patients, 8 had AVMs with associated aneurysms, and the aneurysm was obliterated in all 8 patients. Over the course of 57.9 patient-years of follow-up, including 55.3 patient-years for partially treated AVMs, no hemorrhages were described, reflecting a trend toward protection from hemorrhage after treatment (p = 0.12, likelihood ratio test).

Conclusions

Spinal juvenile (Type III) extradural-intradural AVMs commonly present symptomatically. Associated arterial aneurysms increase their hemorrhage risk, and protection from hemorrhage may be achieved from partial obliteration of these lesions, particularly if targeted toward associated aneurysms.

Spinal juvenile (Type III) extradural-intradural arteriovenous malformations (AVMs) are known for their formidable angioarchitecture and presumed poor natural history.18,27,30,41,44,45,48 These lesions are angioarchitecturally distinct from the more common intramedullary glomus (Type II) AVMs;16,18,49 their management remains in the format of case reports even to date.23,29,41 Supplied by pial, dural, and paraspinal arteries with expansive nidi spanning the extradural and intradural space, these large AVMs may have a greater proclivity toward causing symptomatic mass effect or venous hypertension.27,44,49 Although their ability to cause hemorrhage is known,4,8,28 it is yet to be quantified. Considering their large size, the impact of partial treatment of these lesions on natural history is particularly important to address. Does targeted therapy, such as targeted obliteration of associated aneurysms, improve their natural history? In this report, we attempt to address these questions by compiling demographic information, hemorrhage risk data, and treatment results for these lesions.

Methods

Study Selection

The PubMed database was queried with the terms “arteriovenous malformation,” “avm,” “juvenile,” “metameric,” “cobb syndrome,” “spinal,” “cervical,” “thoracic,” and “lumbar” through April 1, 2013 (Table 1). No publication date or publication status restrictions were imposed. We incorporated all English-language studies that provided individualized data. To enhance the comprehensiveness of the review, references within studies were perused and incorporated if they met our inclusion criteria. Review articles and studies without individualized patient information, those not involving human subjects, or those evaluating only different spinal AVM subtypes were excluded. Patients described as having “juvenile” and/or “metameric” lesions that had only intramedullary glomus AVMs or arteriovenous fistulas (AVFs) were excluded.

TABLE 1:

Summary of incorporated studies*

Authors & YearNo. of PtsMean Age (yrs)M/FPresentationLevelTxObliterationCondition at Follow-Up After Tx
Alomari et al., 2011482:21 progressive ND, 1 acute ND, 1 asymptomatic3 thoracic, 1 lumbar2 combo0/11 worse
Baraitser & Shieff, 19901131:0hemorrhagethoracic
Biondi et al., 19923,45173:25 hemorrhages2 cervical, 3 thoracic5 embo1/55 improved
Cullen et al., 2006232:01 acute ND, 1 asymptomatic1 thoracic, 1 lumbar
Clark et al., 2008180:1hemorrhagelumbar
Dilmé-Carreras et al., 20101121:0asymptomaticthoracic
Eldridge et al., 19891121:0hemorrhagelumbarsurgerysame
Ferch et al., 20011211:0progressive NDthoraciccombo0/1worse
Johnson & Petrie, 20091241:0acute NDthoracicembo0/1worse
Kalani et al., 20122111:11 acute ND, 1 progressive ND1 cervical, 1 thoracic1 combo, 1 surgery2/22 improved
Kähärä et al., 19971161:0progressive NDthoracicembo0/1same
Kalhorn et al., 20101170:1acute NDthoraciccombo0/1improved
Kaplan et al., 1976111:0hemorrhagelumbarsurgery0/1improved
Kerber et al., 19781470:1acute NDthoraciccombo1/1improved
Konan et al., 19992181:12 hemorrhages1 cervical, 1 thoracic2 embo0/22 improved
Linfante et al., 2012190:1progressive NDthoracicembo1/1improved
Martin et al., 19951151:0progressive NDthoracicsurgery1/1improved
Matsumaru et al., 199910168:27 progressive NDs, 2 hemorrhages, 1 asymptomatic2 cervical, 6 thoracic, 2 lumbar6 embo1/11 same, 1 worse
Matullo et al., 20071111:0hemorrhagethoracicemboimproved
Menkü et al., 20051211:0progressive NDcervicalcombo1/1improved
Ommaya et al., 19692111:11 hemorrhage, 1 progressive ND1 thoracic, 1 lumbar1 embo0/11 improved
Pascual-Castroviejo et al., 2002171:0hemorrhagethoracic
Rudy & Woodside, 19832100:21 acute ND, 1 progressive ND2 thoracic1 combo, 1 surgery2 improved
Schirmer et al., 20121151:0asymptomaticlumbarcombo0/1worse
Shim et al., 19961190:1acute NDthoracic
Soeda et al., 20031newborn0:1acute NDthoracicembo0/1improved
Spetzler et al., 19891320:1progressive NDcervicalcombo1/1improved
Touho et al., 19911430:1acute NDthoraciccombo1/1improved
Wang et al., 20052182:02 acute NDs2 thoracic

combo = combined surgery and endovascular treatment; embo = embolization; ND = neurological deficit; Pts = patients; Tx = treatment.

Age at initial clinical presentation.

Data Extraction

From all studies, we extracted individualized demographic, symptomatic, and AVM angioarchitectural data including patient age, sex, presenting neurological deficits, hemorrhage on presentation, AVM location, and associated arterial aneurysms. For each patient with at least 1 month of untreated follow-up, the time in years from original clinical presentation until treatment or last clinical follow-up was noted. Hemorrhages over this time period were noted. For treatment results, we extracted information detailing the surgical or endovascular approach, obliteration rates, and neurological condition at follow-up.

Statistical Analysis

Statistical analysis was performed using R version 2.11. Pooled rates were calculated for demographic information, annual hemorrhage rates, and results of intervention. Comparisons between pooled rates for treatment subgroups were performed using the Fisher exact test for categorical variables and with a 2-tailed t-test for mean follow-up periods. For our analysis of hemorrhage risk prior to treatment, AVM presence was assumed since birth. The Cox proportional hazards regression model was calculated using the survival package in R. Hemorrhage was used as the censoring event, and multiple events per subject were taken into account. To explain the variability in the primary outcome, we defined 4 a priori variables: age, sex, presence of an aneurysm, and location.

Results

After an initial screening of 358 studies, 125 full-text articles were assessed for eligibility, and 29 reports with 51 patients met inclusion criteria (Table 1).1–4,8,10,12–14,20–25,29,32–37,39,41–43,45,48,50 For these 51 patients, the mean age at presentation was 15.0 ± 10.5 years (± SD), and there was a slight male sex predilection (63% male, 1.7:1 male/female ratio) (Table 2). Presentation modalities included progressive neurological deficits in 35% of cases, acute hemorrhage in 31%, an acute neurological deficit without hemorrhage in 22% of cases, and incidental discovery in the remaining 12%. Arteriovenous malformations were most commonly thoracic (63%); 20% were cervical and 18% were lumbar. Across 23 cases where angioarchitecture described associated arterial aneurysms, 48% of AVMs had at least one associated aneurysm.

TABLE 2:

Pooled background, demographic, and AVM angioarchitectural data

ParameterValue
no. of patients51
no. of reports29
mean age at presentation in yrs (± SD)15.0 ± 10.5
% male63%
male/female ratio1.7:1
presentation
 incidental6/51 (12%)
 acute neurological deficit11/51 (22%)
 progressive deficit18/51 (35%)
 hemorrhage presentation16/51 (31%)
level
 cervical10/51 (20%)
 thoracic32/51 (63%)
 lumbar/conus9/51 (18%)
associated aneurysm11/23 (48%)

Hemorrhage Risk

Assuming AVM presence since birth, a total of 825.7 patient-years until treatment or last clinical follow-up were tallied for the 51 patients analyzed. Over this period, 17 hemorrhages occurred, corresponding to an annual rate of 2.1%. Hazard ratios for hemorrhage risk factors after univariate and multivariate Cox proportional hazards regression are summarized in Table 3. After univariate analysis, lumbar/conus location (HR 3.66 [95% CI 1.19–11.22], p = 0.02) and associated aneurysms (HR 8.09 [95% CI 1.73–37.82], p = 0.008) were significant risk factors for hemorrhage while increasing age at presentation was associated with a lower risk of hemorrhage (HR 0.82 [95% CI 0.74–0.91], p = 0.0002). After multivariate analysis, associated aneurysms remained a significant risk factor for hemorrhage (HR 8.74 [95% CI 1.76–43.31], p = 0.02; Fig. 1) while increasing age at presentation remained associated with a lower risk of hemorrhage (HR 0.39 [95% CI 0.18–0.87], p = 0.02).

TABLE 3:

Hazard ratios for hemorrhage risk factors after univariate and multivariate Cox proportional hazards regression

Risk FactorUnivariate HR (95% CI)p ValueMultivariate HR (95% CI)p Value
presentation age0.82 (0.74–0.91)0.00020.39 (0.18–0.87)0.02
female sex1.07 (0.40–2.85)0.901.26 (0.19–8.36)0.81
lumbar/conus3.66 (1.19–11.22)0.021.60 (0.17–14.7)0.62
associated aneurysm8.09 (1.73–37.82)0.0088.74 (1.76–43.31)0.02
Fig. 1.
Fig. 1.

Kaplan-Meier curve of hemorrhage-free survival for AVMs with versus those without associated arterial aneurysms.

Treatment Results

Treatment information was provided for 45 patients. Ten patients did not undergo surgery or embolization (22%). Twenty underwent embolization (44%), 11 underwent embolization followed by resection (24%), and 4 underwent resection alone (9%). Treatment results for those undergoing surgery with or without embolization and those undergoing embolization alone are provided in Table 4. Angiographic obliteration after treatment was described in 25 cases overall; in 8, complete obliteration was achieved (32%). Rates of obliteration did not significantly differ between treatment modalities, although angiographic results at follow-up were rarely addressed. Of note, of 8 cases with associated aneurysms with described angiographic results, the aneurysm was obliterated endovascularly in all cases. The overall mean follow-up was 2.6 ± 3.2 years, corresponding to a total of 57.9 patient-years, including 55.3 patient-years of follow-up for partially treated lesions. Over this time period, no cases of hemorrhage were described, reflecting a trend toward protection from hemorrhage after treatment (p = 0.12, likelihood ratio test). Neurological condition at follow-up was described for 30 patients—22 were improved (73%), 3 were the same (10%), and 5 were worse (17%). This did not significantly differ between treatment modalities.

TABLE 4:

Treatment results

ParameterSurgery*Embolizationp ValueTotal
no. of patients15/35 (43%)20/35 (57%)0.3435
mean follow-up in yrs (± SD)2.2 ± 3.62.9 ± 3.00.592.6 ± 3.2
obliteration4/11 (36%)4/14 (29%)1.08/25 (32%)
condition at follow-up
 improved10/13 (77%)12/17 (71%)1.022/30 (73%)
 same1/13 (8%)2/17 (12%)1.03/30 (10%)
 worse2/13 (15%)3/17 (18%)1.05/30 (17%)

Surgery with or without embolization.

Embolization only.

Discussion

Although a modern perception of spinal “juvenile metameric” AVMs is that of a formidable extradural-intradural lesion,27,44,49 the terms “juvenile” and/or “metameric” historically encompass a broader subset of spinal vascular malformations. Juvenile spinal vascular arteriovenous shunts have also referred to intramedullary AVMs in some reports.11,31 Some of the earliest descriptions of spinal AVMs likely referred to diffuse intramedullary spinal AVMs as the juvenile or “Type III” lesion in contrast to more compact lesions referred to as “Type II.”10 Most now consider both compact and diffuse intramedullary AVMs as Type II lesions or as, in the Spetzler classification, in the group of intramedullary AVMs.27,44 These lesions group well together angioarchitecturally in contrast to formidable extradural-intradural lesions that are better considered as a separate Type III subgroup (Fig. 2). The Type III distinction should not be based on a patient possessing a spinal metameric/Cobb syndrome, as any spinal arteriovenous shunt7,31,38,51 or cavernous malformation9,19 may serve as the spinal component, not necessarily an extradural-intradural AVM. We thus do not use the term “juvenile metameric AVM” to refer to these lesions but rather “juvenile extradural-intradural” to more specifically describe these lesions.

Fig. 2.
Fig. 2.

Representative spinal extradural-intradural AVM. This right T-8 segmental artery injection demonstrates supply to an extradural-intradural AVM. The arrowhead denotes the extradural component, and the arrow denotes the intradural component. Adapted from Linfante et al: J Neurosurg Spine 16:408–413, 2012, with permission.

Most classification schemes consider 4 spinal dural/intradural arteriovenous shunts: dural AVFs (Type I), glomus AVMs (Type II), juvenile extradural-intradural AVMs (Type III), and pial AVFs (Type IV).6,16–18,49 A comparative analysis of these spinal arteriovenous shunts is provided in Table 5. Our study confirms that patients with extradural-intradural AVMs present at the youngest age. We also now demonstrate a slight male sex predilection for these lesions, somewhat akin to Type I and Type IV lesions,17,40,47 but an interesting contrast to glomus AVMs where no sex predilection is seen.16 Angioarchitecturally, Type III AVMs seem to have the greatest prevalence of associated aneurysms. Aside from Type I lesions that essentially do not present a significant risk of hemorrhage,40,47 annual hemorrhage rates for the other spinal arteriovenous shunt subtypes are generally similar.16,17 The similarity of hemorrhage rates among spinal AVMs draws analogy to the modern cerebral AVM maxim that AVM size does not impact hemorrhage rate.15,52

TABLE 5:

Comparison of spinal dural/intradural arteriovenous shunts

ParameterDural AVFGlomus AVM*Extradural-Intradural AVMPial AVF
subclassificationA) single feeder; B) multiple feederscompact; diffuseA) small fistula, low flow; B) inter- mediate; C) large, high flow
mean presentation age in yrs64291532; Type A: 47; Type C: 19
male/female ratio3.5:11:11.7:11.3:1; Type A: 2.1:1; Type C: 1:1
arterial aneurysmsvery rare29%48%10%
annual hemorrhage ratevery rare4%2.1%2.5%
surgical obliteration rate95–98%§78%36%88%
endovascular obliteration rate46%§33%29%74%
worse at follow-up after treatment4%12%17%8%

From a 293-patient pooled analysis (Gross and Du16).

From a 213-patient pooled analysis (Gross and Du17).

From a 154-patient single-center series (Saladino et al.).

From a meta-analysis (Steinmetz et al.).

Our method of assuming AVM presence since birth is a contrast to the other analyses that used lesion follow-up after presentation.15–17,26,46,52 Although our assumption of AVM presence since birth may ostensibly deflate the observed hemorrhage rate, a recent analysis of cerebral AVMs has provided some validation for this approach.26 In this report, it allowed us to additionally evaluate risk factors for hemorrhage, revealing arterial aneurysms and younger age to be associated with a higher hemorrhage risk, similar to glomus AVMs.16 Given that aneurysms are likely acquired, dynamic components of the AVM, our assumption of their static presence since birth is conservative; the fact that they nonetheless remain a significant risk factor for hemorrhage further emphasizes the importance of identifying them and their significant impact on hemorrhage risk.

Not surprisingly, obliteration rates are lowest for extradural-intradural lesions. In fact, our observed obliteration rates are likely an overestimate as we included case reports that may inflate this rate as a result of publication bias of only successful cases. Furthermore, likely in part due to the natural history of partially treated AVMs, worsening at follow-up was seen most commonly among extradural-intradural lesions. The impact of partial treatment of AVMs on outcome thus becomes a particularly important issue to address when considering these lesions. Recent data have suggested a potential benefit on hemorrhage risk for glomus AVMs,16 and this study shows a trend toward protection from hemorrhage after treatment of extradural-intradural AVMs as well (p = 0.12). Given that aneurysms are a known risk factor for hemorrhage and 8 of 8 described aneurysms were obliterated in our reviewed cases, one may postulate that the observed protection from hemorrhage after partial treatment may be in part from securing arterial aneurysms. Thus, although strong treatment recommendations cannot be derived from this report, it does provide preliminary evidence supporting partial treatment aimed at least at securing associated arterial aneurysms to mitigate hemorrhage risk.

Limitations of This Study

Our study encompasses a small, heterogeneous cohort of spinal juvenile (Type III) extradural-intradural AVMs. As a result of extradural-intradural AVM rarity, our pooled results primarily comprise case reports, introducing publication bias of successful or intriguing cases. As mentioned earlier, this likely inflates the already low obliteration rates for endovascular and surgical management; however, treatment goals were frequently not specified in our reviewed studies, limiting our analysis of procedural “success” rates. Unfortunately, as a result of a lack of detailed information, a relatively large series of 15 patients with reportedly “metameric” AVMs was excluded.5

This study largely focuses on the risk of hemorrhage from these lesions, which is only one of several sources of neurological morbidity from these AVMs. Mass effect from growing lesions (or residual lesions after partial treatment) or symptoms from venous hypertension requires better attention in a comprehensive analysis of the natural history of these lesions prior to and after treatment. Although we illustrate similar hemorrhage rates for these lesions that draw analogy to glomus AVMs,16 these larger, more formidable lesions may pose a greater risk of symptomatic deterioration as a result of mass effect or venous hypertension. Such deterioration may be as debilitating as a hemorrhagic event and thus requires better attention in future studies and over a longer period of follow-up. A specific question to address is the feasibility and durability of partial treatment aimed at alleviating venous hypertension.

Importantly, our study could not accumulate ample long-term angiographic or clinical follow-up in patients. This is particularly crucial in the context of the high proportion of partially treated lesions and the young age of patients with these AVMs. Only 3 patients in our analysis had more than 5 years of follow-up,3,20,39 and of them, the condition in one deteriorated neurologically without hemorrhage 9 years after treatment.20 Thus, the true impact of treatment on outcome remains to be addressed, and must be considered in the context of not only protection from hemorrhage, but also from durability of alleviated venous hypertension and mass effect.

Conclusions

Spinal juvenile (Type III) extradural-intradural AVMs affect young patients with a slight male sex predilection. Approximately one-third present with progressive neurological deterioration, another one-third with hemorrhage, approximately one-fifth with acute deficits not attributable to hemorrhage, and the remaining one-eighth with incidental lesions. Interestingly, nearly half have associated arterial aneurysms. Assuming AVM presence since birth, the annual hemorrhage rate for these lesions was 2.1% with age at presentation (HR 0.39 [95% CI 0.18–0.87]) and associated aneurysms (HR 8.74 [95% CI 1.76–43.31]) serving as significant risk factors for hemorrhage (p = 0.02 for each after multivariate analysis). Complete obliteration after treatment was infrequent, although arterial aneurysms were secured in 8 of 8 cases described. After treatment, 17% of patients were neurologically worse after a mean follow-up of 2.6 years. Interestingly, no cases of hemorrhage were described over 57.9 patient-years of follow-up after treatment, perhaps in part due to the beneficial effect of securing associated arterial aneurysms. Although strong recommendations in favor of treatment cannot be made based on our data, the data may support partial treatment aimed at least at securing associated arterial aneurysms, a pertinent finding given their prevalent association with this spinal AVM subtype.

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: both authors. Acquisition of data: Gross. Analysis and interpretation of data: both authors. Drafting the article: Gross. Critically revising the article: both authors. Reviewed submitted version of manuscript: both authors. Approved the final version of the manuscript on behalf of both authors: Du. Statistical analysis: both authors. Administrative/technical/material support: Du. Study supervision: Du.

References

  • 1

    Alomari AIChaudry GRodesch GBurrows PEMulliken JBSmith ER: Complex spinal-paraspinal fast-flow lesions in CLOVES syndrome: analysis of clinical and imaging findings in 6 patients. AJNR Am J Neuroradiol 32:181218172011

  • 2

    Baraitser PShieff C: Cutaneomeningo-spinal angiomatosis: the syndrome of Cobb. A case report. Neuropediatrics 21:1601611990

  • 3

    Biondi AMerland JJHodes JEAymard AReizine D: Aneurysms of spinal arteries associated with intramedullary arteriovenous malformations. II. Results of AVM endovascular treatment and hemodynamic considerations. AJNR Am J Neuroradiol 13:9239311992

  • 4

    Biondi AMerland JJHodes JEPruvo JPReizine D: Aneurysms of spinal arteries associated with intramedullary arteriovenous malformations. I. Angiographic and clinical aspects. AJNR Am J Neuroradiol 13:9139221992

  • 5

    Biondi AMerland JJReizine DAymard AHodes JELecoz P: Embolization with particles in thoracic intramedullary arteriovenous malformations: long-term angiographic and clinical results. Radiology 177:6516581990

  • 6

    Black P: Spinal vascular malformations: an historical perspective. Neurosurg Focus 21:6E112006

  • 7

    Bun YYMing CKMing CHLing CYMing CC: Endovascular treatment of a neonate with dural arteriovenous fistula and other features suggestive of cerebrofacial arteriovenous metameric syndromes. Childs Nerv Syst 25:3833872009

  • 8

    Clark MTBrooks ELChong WPappas CFahey M: Cobb syndrome: a case report and systematic review of the literature. Pediatr Neurol 39:4234252008

  • 9

    Clinton TSCooke LMGraham BS: Cobb syndrome associated with a verrucous (angiokeratomalike) vascular malformation. Cutis 71:2832872003

  • 10

    Cullen SAlvarez HRodesch GLasjaunias P: Spinal arteriovenous shunts presenting before 2 years of age: analysis of 13 cases. Childs Nerv Syst 22:110311102006

  • 11

    Di Chiro GWener L: Angiography of the spinal cord. A review of contemporary techniques and applications. J Neurosurg 39:1291973

  • 12

    Dilmé-Carreras EIglesias-Sancho MMárquez-Balbás GSola-Ortigosa JUmbert-Millet P: Cobb syndrome: case report and review of the literature. Dermatology 221:1101122010

  • 13

    Eldridge PRHolland IMPunt JA: Spinal arteriovenous malformations in children. Br J Neurosurg 3:3933971989

  • 14

    Ferch RDMorgan MKSears WR: Spinal arteriovenous malformations: a review with case illustrations. J Clin Neurosci 8:2993042001

  • 15

    Gross BADu R: Natural history of cerebral arteriovenous malformations: a meta-analysis. Clinical article. J Neurosurg 118:4374432013

  • 16

    Gross BADu R: Spinal glomus (type II) arteriovenous malformations: a pooled analysis of hemorrhage risk and results of intervention. Neurosurgery 72:25322013

  • 17

    Gross BADu R: Spinal pial (type IV) arteriovenous fistulae: a systematic pooled analysis of demographics, hemorrhage risk, and treatment results. Neurosurgery 73:1411512013

  • 18

    Heros RCDebrun GMOjemann RGLasjaunias PLNaessens PJ: Direct spinal arteriovenous fistula: a new type of spinal AVM. Case report. J Neurosurg 64:1341391986

  • 19

    Jessen RTThompson SSmith EB: Cobb syndrome. Arch Dermatol 113:158715901977

  • 20

    Johnson WDPetrie MM: Variety of spinal vascular pathology seen in adult Cobb syndrome. Report of 2 cases. J Neurosurg Spine 10:4304352009

  • 21

    Kähärä VJSeppänen SKKuurne TLaasonen EM: Diagnosis and embolizing of spinal arteriovenous malformations. Ann Med 29:3773821997

  • 22

    Kalani MYAhmed ASMartirosyan NLCronk KMoon KAlbuquerque FC: Surgical and endovascular treatment of pediatric spinal arteriovenous malformations. World Neurosurg 78:3483542012

  • 23

    Kalhorn SPFrempong-Boadu AKMikolaenko IBecske THarter DH: Metameric thoracic lesion: report of a rare case and a guide to management. Case report. J Neurosurg Spine 12:4975022010

  • 24

    Kaplan PHollenberg RDFraser FC: A spinal arteriovenous malformation with hereditary cutaneous hemangiomas. Am J Dis Child 130:132913311976

  • 25

    Kerber CWCromwell LDSheptak PE: Intraarterial cyanoacrylate: an adjunct in the treatment of spinal/paraspinal arteriovenous malformations. AJR Am J Roentgenol 130:991031978

  • 26

    Kim HMcCulloch CEJohnston SCLawton MTSidney SYoung WL: Comparison of 2 approaches for determining the natural history risk of brain arteriovenous malformation rupture. Am J Epidemiol 171:131713222010

  • 27

    Kim LJSpetzler RF: Classification and surgical management of spinal arteriovenous lesions: arteriovenous fistulae and arteriovenous malformations. Neurosurgery 59:5 Suppl 3S3-195S3-2012006

  • 28

    Konan AVRaymond JRoy D: Transarterial embolization of aneurysms associated with spinal cord arteriovenous malformations. Report of four cases. J Neurosurg 90:1 Suppl1481541999

  • 29

    Linfante ITari Capone FDabus GGonzalez-Arias SLau PESamaniego EA: Spinal arteriovenous malformation associated with spinal metameric syndrome: a treatable cause of long-term paraplegia? Case report. J Neurosurg Spine 16:4084132012

  • 30

    Malis LI: Microsurgery for spinal cord arteriovenous malformations. Clin Neurosurg 26:5435551979

  • 31

    Maramattom BVCohen-Gadol AAWijdicks EFKallmes D: Segmental cutaneous hemangioma and spinal arteriovenous malformation (Cobb syndrome). Case report and historical perspective. J Neurosurg Spine 3:2492522005

  • 32

    Martin NAKhanna RKBatzdorf U: Posterolateral cervical or thoracic approach with spinal cord rotation for vascular malformations or tumors of the ventrolateral spinal cord. J Neurosurg 83:2542611995

  • 33

    Matsumaru YPongpech SLaothamas JAlvarez HRodesch GLasjaunias P: Multifocal and metameric spinal cord arteriovenous malformations. Review of 19 cases. Interv Neuroradiol 5:27341999

  • 34

    Matullo KSSamdani ABetz R: Low-back pain and unrecognized Cobb syndrome in a child resulting in paraplegia. Orthopedics 30:2372382007

  • 35

    Menkü AAkdemir HDurak ACOktem IS: Successful surgical excision of juvenile-type spinal arteriovenous malformation in two stages following partial embolization. Minim Invasive Neurosurg 48:57622005

  • 36

    Ommaya AKDi Chiro GDoppman J: Ligation of arterial supply in the treatment of spinal cord arteriovenous malformations. J Neurosurg 30:6796921969

  • 37

    Pascual-Castroviejo IFrutos RViaño JPascual-Pascual SIGonzalez P: Cobb syndrome: case report. J Child Neurol 17:8478492002

  • 38

    Piske RSampaio MCampos CNunes JA JrLima SS: Trifocal monomyelomeric spinal cord arteriovenous fistulae in a seven-year-old boy. Interv Neuroradiol 7:1211262001

  • 39

    Rudy DCWoodside JR: Familial juvenile type III spinal cord arteriovenous malformation: urodynamic findings. J Urol 130:9469471983

  • 40

    Saladino AAtkinson JLDRabinstein AAPiepgras DGMarsh WRKrauss WE: Surgical treatment of spinal dural arteriovenous fistulae: a consecutive series of 154 patients. Neurosurgery 67:135013582010

  • 41

    Schirmer CMHwang SWRiesenburger RIChoi ISDavid CA: Obliteration of a metameric spinal arteriovenous malformation (Cobb syndrome) using combined endovascular embolization and surgical excision. Case report. J Neurosurg Pediatr 10:44492012

  • 42

    Shim JHLee DWCho BK: A case of Cobb syndrome associated with lymphangioma circumscriptum. Dermatology 193:45471996

  • 43

    Soeda ASakai NIihara KNagata I: Cobb syndrome in an infant: treatment with endovascular embolization and corticosteroid therapy: case report. Neurosurgery 52:7117152003

  • 44

    Spetzler RFDetwiler PWRiina HAPorter RW: Modified classification of spinal cord vascular lesions. J Neurosurg 96:2 Suppl1451562002

  • 45

    Spetzler RFZabramski JMFlom RA: Management of juvenile spinal AVM's by embolization and operative excision. Case report. J Neurosurg 70:6286321989

  • 46

    Stapf CMast HSciacca RRChoi JHKhaw AVConnolly ES: Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology 66:135013552006

  • 47

    Steinmetz MPChow MMKrishnaney AAAndrews-Hinders DBenzel ECMasaryk TJ: Outcome after the treatment of spinal dural arteriovenous fistulae: a contemporary single-institution series and meta-analysis. Neurosurgery 55:77882004

  • 48

    Touho HKarasawa JShishido HYamada KShibamoto K: Successful excision of a juvenile-type spinal arteriovenous malformation following intraoperative embolization. Case report. J Neurosurg 75:6476511991

  • 49

    Veznedaroglu ENelson PKJabbour PMRosenwasser RH: Endovascular treatment of spinal cord arteriovenous malformations. Neurosurgery 59:5 Suppl 3S3-202S3-2092006

  • 50

    Wang GBXu LZhao BCai SFShi HLi HH: Medical imaging findings in Cobb syndrome: two case reports. Chin Med J (Engl) 118:105010532005

  • 51

    Wetter DADavis MDHand JL: Acute paralysis in a 17-year-old man with subtle cutaneous vascular malformations: an unusual case of Cobb syndrome. J Eur Acad Dermatol Venereol 22:5255262008

  • 52

    Yamada STakagi YNozaki KKikuta KHashimoto N: Risk factors for subsequent hemorrhage in patients with cerebral arteriovenous malformations. J Neurosurg 107:9659722007

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Article Information

Address correspondence to: Rose Du, M.D., Ph.D., Department of Neurological Surgery, Brigham and Women's Hospital and Harvard Medical School, 75 Francis St., Boston, MA 02115. email: rdu@partners.org.

Please include this information when citing this paper: published online February 14, 2014; DOI: 10.3171/2014.1.SPINE13498.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Kaplan-Meier curve of hemorrhage-free survival for AVMs with versus those without associated arterial aneurysms.

  • View in gallery

    Representative spinal extradural-intradural AVM. This right T-8 segmental artery injection demonstrates supply to an extradural-intradural AVM. The arrowhead denotes the extradural component, and the arrow denotes the intradural component. Adapted from Linfante et al: J Neurosurg Spine 16:408–413, 2012, with permission.

References

1

Alomari AIChaudry GRodesch GBurrows PEMulliken JBSmith ER: Complex spinal-paraspinal fast-flow lesions in CLOVES syndrome: analysis of clinical and imaging findings in 6 patients. AJNR Am J Neuroradiol 32:181218172011

2

Baraitser PShieff C: Cutaneomeningo-spinal angiomatosis: the syndrome of Cobb. A case report. Neuropediatrics 21:1601611990

3

Biondi AMerland JJHodes JEAymard AReizine D: Aneurysms of spinal arteries associated with intramedullary arteriovenous malformations. II. Results of AVM endovascular treatment and hemodynamic considerations. AJNR Am J Neuroradiol 13:9239311992

4

Biondi AMerland JJHodes JEPruvo JPReizine D: Aneurysms of spinal arteries associated with intramedullary arteriovenous malformations. I. Angiographic and clinical aspects. AJNR Am J Neuroradiol 13:9139221992

5

Biondi AMerland JJReizine DAymard AHodes JELecoz P: Embolization with particles in thoracic intramedullary arteriovenous malformations: long-term angiographic and clinical results. Radiology 177:6516581990

6

Black P: Spinal vascular malformations: an historical perspective. Neurosurg Focus 21:6E112006

7

Bun YYMing CKMing CHLing CYMing CC: Endovascular treatment of a neonate with dural arteriovenous fistula and other features suggestive of cerebrofacial arteriovenous metameric syndromes. Childs Nerv Syst 25:3833872009

8

Clark MTBrooks ELChong WPappas CFahey M: Cobb syndrome: a case report and systematic review of the literature. Pediatr Neurol 39:4234252008

9

Clinton TSCooke LMGraham BS: Cobb syndrome associated with a verrucous (angiokeratomalike) vascular malformation. Cutis 71:2832872003

10

Cullen SAlvarez HRodesch GLasjaunias P: Spinal arteriovenous shunts presenting before 2 years of age: analysis of 13 cases. Childs Nerv Syst 22:110311102006

11

Di Chiro GWener L: Angiography of the spinal cord. A review of contemporary techniques and applications. J Neurosurg 39:1291973

12

Dilmé-Carreras EIglesias-Sancho MMárquez-Balbás GSola-Ortigosa JUmbert-Millet P: Cobb syndrome: case report and review of the literature. Dermatology 221:1101122010

13

Eldridge PRHolland IMPunt JA: Spinal arteriovenous malformations in children. Br J Neurosurg 3:3933971989

14

Ferch RDMorgan MKSears WR: Spinal arteriovenous malformations: a review with case illustrations. J Clin Neurosci 8:2993042001

15

Gross BADu R: Natural history of cerebral arteriovenous malformations: a meta-analysis. Clinical article. J Neurosurg 118:4374432013

16

Gross BADu R: Spinal glomus (type II) arteriovenous malformations: a pooled analysis of hemorrhage risk and results of intervention. Neurosurgery 72:25322013

17

Gross BADu R: Spinal pial (type IV) arteriovenous fistulae: a systematic pooled analysis of demographics, hemorrhage risk, and treatment results. Neurosurgery 73:1411512013

18

Heros RCDebrun GMOjemann RGLasjaunias PLNaessens PJ: Direct spinal arteriovenous fistula: a new type of spinal AVM. Case report. J Neurosurg 64:1341391986

19

Jessen RTThompson SSmith EB: Cobb syndrome. Arch Dermatol 113:158715901977

20

Johnson WDPetrie MM: Variety of spinal vascular pathology seen in adult Cobb syndrome. Report of 2 cases. J Neurosurg Spine 10:4304352009

21

Kähärä VJSeppänen SKKuurne TLaasonen EM: Diagnosis and embolizing of spinal arteriovenous malformations. Ann Med 29:3773821997

22

Kalani MYAhmed ASMartirosyan NLCronk KMoon KAlbuquerque FC: Surgical and endovascular treatment of pediatric spinal arteriovenous malformations. World Neurosurg 78:3483542012

23

Kalhorn SPFrempong-Boadu AKMikolaenko IBecske THarter DH: Metameric thoracic lesion: report of a rare case and a guide to management. Case report. J Neurosurg Spine 12:4975022010

24

Kaplan PHollenberg RDFraser FC: A spinal arteriovenous malformation with hereditary cutaneous hemangiomas. Am J Dis Child 130:132913311976

25

Kerber CWCromwell LDSheptak PE: Intraarterial cyanoacrylate: an adjunct in the treatment of spinal/paraspinal arteriovenous malformations. AJR Am J Roentgenol 130:991031978

26

Kim HMcCulloch CEJohnston SCLawton MTSidney SYoung WL: Comparison of 2 approaches for determining the natural history risk of brain arteriovenous malformation rupture. Am J Epidemiol 171:131713222010

27

Kim LJSpetzler RF: Classification and surgical management of spinal arteriovenous lesions: arteriovenous fistulae and arteriovenous malformations. Neurosurgery 59:5 Suppl 3S3-195S3-2012006

28

Konan AVRaymond JRoy D: Transarterial embolization of aneurysms associated with spinal cord arteriovenous malformations. Report of four cases. J Neurosurg 90:1 Suppl1481541999

29

Linfante ITari Capone FDabus GGonzalez-Arias SLau PESamaniego EA: Spinal arteriovenous malformation associated with spinal metameric syndrome: a treatable cause of long-term paraplegia? Case report. J Neurosurg Spine 16:4084132012

30

Malis LI: Microsurgery for spinal cord arteriovenous malformations. Clin Neurosurg 26:5435551979

31

Maramattom BVCohen-Gadol AAWijdicks EFKallmes D: Segmental cutaneous hemangioma and spinal arteriovenous malformation (Cobb syndrome). Case report and historical perspective. J Neurosurg Spine 3:2492522005

32

Martin NAKhanna RKBatzdorf U: Posterolateral cervical or thoracic approach with spinal cord rotation for vascular malformations or tumors of the ventrolateral spinal cord. J Neurosurg 83:2542611995

33

Matsumaru YPongpech SLaothamas JAlvarez HRodesch GLasjaunias P: Multifocal and metameric spinal cord arteriovenous malformations. Review of 19 cases. Interv Neuroradiol 5:27341999

34

Matullo KSSamdani ABetz R: Low-back pain and unrecognized Cobb syndrome in a child resulting in paraplegia. Orthopedics 30:2372382007

35

Menkü AAkdemir HDurak ACOktem IS: Successful surgical excision of juvenile-type spinal arteriovenous malformation in two stages following partial embolization. Minim Invasive Neurosurg 48:57622005

36

Ommaya AKDi Chiro GDoppman J: Ligation of arterial supply in the treatment of spinal cord arteriovenous malformations. J Neurosurg 30:6796921969

37

Pascual-Castroviejo IFrutos RViaño JPascual-Pascual SIGonzalez P: Cobb syndrome: case report. J Child Neurol 17:8478492002

38

Piske RSampaio MCampos CNunes JA JrLima SS: Trifocal monomyelomeric spinal cord arteriovenous fistulae in a seven-year-old boy. Interv Neuroradiol 7:1211262001

39

Rudy DCWoodside JR: Familial juvenile type III spinal cord arteriovenous malformation: urodynamic findings. J Urol 130:9469471983

40

Saladino AAtkinson JLDRabinstein AAPiepgras DGMarsh WRKrauss WE: Surgical treatment of spinal dural arteriovenous fistulae: a consecutive series of 154 patients. Neurosurgery 67:135013582010

41

Schirmer CMHwang SWRiesenburger RIChoi ISDavid CA: Obliteration of a metameric spinal arteriovenous malformation (Cobb syndrome) using combined endovascular embolization and surgical excision. Case report. J Neurosurg Pediatr 10:44492012

42

Shim JHLee DWCho BK: A case of Cobb syndrome associated with lymphangioma circumscriptum. Dermatology 193:45471996

43

Soeda ASakai NIihara KNagata I: Cobb syndrome in an infant: treatment with endovascular embolization and corticosteroid therapy: case report. Neurosurgery 52:7117152003

44

Spetzler RFDetwiler PWRiina HAPorter RW: Modified classification of spinal cord vascular lesions. J Neurosurg 96:2 Suppl1451562002

45

Spetzler RFZabramski JMFlom RA: Management of juvenile spinal AVM's by embolization and operative excision. Case report. J Neurosurg 70:6286321989

46

Stapf CMast HSciacca RRChoi JHKhaw AVConnolly ES: Predictors of hemorrhage in patients with untreated brain arteriovenous malformation. Neurology 66:135013552006

47

Steinmetz MPChow MMKrishnaney AAAndrews-Hinders DBenzel ECMasaryk TJ: Outcome after the treatment of spinal dural arteriovenous fistulae: a contemporary single-institution series and meta-analysis. Neurosurgery 55:77882004

48

Touho HKarasawa JShishido HYamada KShibamoto K: Successful excision of a juvenile-type spinal arteriovenous malformation following intraoperative embolization. Case report. J Neurosurg 75:6476511991

49

Veznedaroglu ENelson PKJabbour PMRosenwasser RH: Endovascular treatment of spinal cord arteriovenous malformations. Neurosurgery 59:5 Suppl 3S3-202S3-2092006

50

Wang GBXu LZhao BCai SFShi HLi HH: Medical imaging findings in Cobb syndrome: two case reports. Chin Med J (Engl) 118:105010532005

51

Wetter DADavis MDHand JL: Acute paralysis in a 17-year-old man with subtle cutaneous vascular malformations: an unusual case of Cobb syndrome. J Eur Acad Dermatol Venereol 22:5255262008

52

Yamada STakagi YNozaki KKikuta KHashimoto N: Risk factors for subsequent hemorrhage in patients with cerebral arteriovenous malformations. J Neurosurg 107:9659722007

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