Pediatric cerebral arteriovenous malformation

Pediatric cerebral arteriovenous malformation

Although brain arteriovenous malformations (bAVMs) account for a very small proportion of cerebral pathologies in the pediatric population, they are the cause of roughly 50% of spontaneous intracranial hemorrhages. Pediatric bAVMs tend to rupture more frequently and seem to have higher recurrence rates than bAVMs in adults 1) 2) 3) 4) 5) 6) 7).

Natural History

The natural history of untreated cerebral AVMs in children is worse than in adults, in relation to a longer life expectation, a higher annual risk of AVM bleeding (3.2% vs. 2.2%) and a higher incidence of posterior fossa and basal ganglia AVMs, most of which present with massive haemorrhages 8).

Treatment

The management of pediatric bAVMs is particularly challenging. In general, the treatment options are conservative treatment, microsurgeryendovascular therapy (EVT), gamma knife radiosurgery (GKRS), proton-beam stereotactic radiosurgery (PSRS), or a combination of the above.


In 2019 Meling et al., performed a systematic review, according to the PRISMA guidelines, with the result that none of the options seem to offer a clear advantage over the others when used alone. Microsurgery provides the highest obliteration rate, but has higher incidence of neurological complications. EVT may play a role when used as adjuvant therapy, but as a stand-alone therapy, the efficacy is low and the long-term side effects of radiation from the multiple sessions required in deep-seated pediatric bAVMs are still unknown. GKRS has a low risk of complication, but the obliteration rates still leave much to be desired. Finally, PSRS offers promising results with a more accurate radiation that avoids the surrounding tissue, but data is limited due to its recent introduction. Overall, a multi-modal approach, or even an active surveillance, might be the most suitable when facing deep-seated bAVM, considering the difficulty of their management and the high risk of complications in the pediatric population 9).


In 2016 El-Ghanem et al., published a Review of the Existing Literature:

Microsurgical resection remains the gold standard for the treatment of all accessible pediatric AVMs. Embolization and radiosurgery should be considered as an adjunctive therapy. Embolization provides a useful adjunct therapy to microsurgery by preventing significant blood loss and to radiosurgery by decreasing the volume of the AVM. Radiosurgery has been described to provide an alternative treatment approach in certain circumstances either as a primary or adjuvant therapy 10).

Outcome

Intracranial haemorrhage is the presenting clinical manifestation in 75-80% of paediatric patients and is associated with a high morbidity and mortality 11).

Case series

A prospectively maintained database of children between January 1997 and October 2012 for bAVMs was retrospectively queried to identify all consecutive ruptured bAVMs treated by surgery, embolization, and radiosurgery. The impact of baseline clinical and bAVM characteristics on clinical outcome, rebleeding rate, annual bleeding rate, and bAVM obliteration was studied using univariate and multivariate Cox regression analysis.

One hundred six children with ruptured bAVMs were followed up for a total of 480.5 patient-years (mean, 4.5 years). Thirteen rebleeding events occurred, corresponding to an annual bleeding rate of 2.71±1.32%, significantly higher in the first year (3.88±1.39%) than thereafter (2.22±1.38%; P<0.001) and in the case of associated aneurysms (relative risk, 2.68; P=0.004) or any deep venous drainage (relative risk, 2.97; P=0.002), in univariate and multivariate analysis. Partial embolization was associated with a higher annual bleeding rate, whereas initial surgery for intracerebral hemorrhage evacuation was associated with a lower risk of rebleeding.

Associated aneurysms and any deep venous drainage are independent risk factors for rebleeding in pediatric ruptured bAVMs. Immediate surgery or total embolization might be advantageous for children harboring such characteristics, whereas radiosurgery might be targeted at patients without such characteristics 12).

References

1) , 8) , 11)

Di Rocco C, Tamburrini G, Rollo M. Cerebral arteriovenous malformations in children. Acta Neurochir (Wien). 2000;142(2):145-56; discussion 156-8. PubMed PMID: 10795888.
2)

Millar C, Bissonnette B, Humphreys RP. Cerebral arteriovenous malformations in children. Can J Anaesth. 1994;41:321–331.
3)

Kiris T, et al. Surgical results in pediatric Spetzler-Martin grades I–III intracranial arteriovenous malformations. Childs Nerv Syst. 2005;21:69–74. discussion 75–76.
4)

Hoh BL, et al. Multimodality treatment of nongalenic arteriovenous malformations in pediatric patients. Neurosurgery. 2000;47:346–357. discussion 357–358.
5)

Kondziolka D, et al. Arteriovenous malformations of the brain in children: a forty year experience. Can J Neurol Sci. 1992;19:40–45.
6)

11. Wilkins RH. Natural history of intracranial vascular malformations: a review. Neurosurgery. 1985;16:421–430.
7)

Jankowitz BT, et al. Treatment of pediatric intracranial vascular malformations using Onyx-18. J Neurosurg Pediatr. 2008;2:171–176.
9)

Meling TR, Patet G. What is the best therapeutic approach to a pediatric patient with a deep-seated brain AVM? Neurosurg Rev. 2019 Apr 13. doi: 10.1007/s10143-019-01101-8. [Epub ahead of print] Review. PubMed PMID: 30980204.
10)

El-Ghanem M, Kass-Hout T, Kass-Hout O, Alderazi YJ, Amuluru K, Al-Mufti F, Prestigiacomo CJ, Gandhi CD. Arteriovenous Malformations in the Pediatric Population: Review of the Existing Literature. Interv Neurol. 2016 Sep;5(3-4):218-225. Epub 2016 Sep 1. Review. PubMed PMID: 27781052; PubMed Central PMCID: PMC5075815.
12)

Blauwblomme T, Bourgeois M, Meyer P, Puget S, Di Rocco F, Boddaert N, Zerah M, Brunelle F, Rose CS, Naggara O. Long-term outcome of 106 consecutive pediatric ruptured brain arteriovenous malformations after combined treatment. Stroke. 2014 Jun;45(6):1664-71. doi: 10.1161/STROKEAHA.113.004292. Epub 2014 May 1. PubMed PMID: 24788975.

Cerebral arteriovenous malformation epidemiology

Cerebral arteriovenous malformation epidemiology

There has been increased detection of incidental Cerebral arteriovenous malformations (CAVM)s as result of the frequent use of advanced imaging techniques 1).

Common estimates of the prevalence rate vary widely, and their accuracy is questionable and are unfounded.

The prevalence of cerebral arteriovenous malformation (CAVM) in first-degree relatives (FDRs) of patients with a CAVM was increased but did not meet a prespecified criterion for a shared familial risk factor. In combination with the low absolute risk of a CAVM in FDRs, the results do not support screening of FDRs for CAVMs 2).

Since the most severe complication of an AVM is hemorrhagic stroke, most epidemiologic studies have concentrated on the hemorrhage risk and its risk factors 3).

Because of the rarity of the disease and the existence of asymptomatic patients, establishing a true prevalence rate is not feasible. Owing to variation in the detection rate of asymptomatic AVMs, the most reliable estimate for the occurrence of the disease is the detection rate for symptomatic lesions: 0.94 per 100,000 person-years (95% confidence interval, 0.57-1.30/100,000 person-years). This figure is derived from a single population-based study, but it is supported by a reanalysis of other data sources. The prevalence of detected, active (at risk) AVM disease is unknown, but it can be inferred from incidence data to be lower than 10.3 per 100,000 population. 4).

AVMs account for between 1 and 2% of all strokes, 3% of strokes in young adults, 9% of subarachnoid haemorrhages and, of all primary intracerebral haemorrhages, they are responsible for 4% overall, but for as much as one-third in young adults. AVMs are far less common causes of first presentations with unprovoked seizures (1%), and of people presenting with headaches in the absence of neurological signs (0.3%). At the time of detection, at least 15% of people affected by AVMs are asymptomatic, about one-fifth present with seizures and for approximately two-thirds of them the dominant mode of presentation is with intracranial haemorrhage. The limited high quality data available on prognosis suggest that long-term crude annual case fatality is 1-1.5%, the crude annual risk of first occurrence of haemorrhage from an unruptured AVM is approximately 2%, but the risk of recurrent haemorrhage may be as high as 18% in the first year, with uncertainty about the risk thereafter. For untreated AVMs, the annual risk of developing de novo seizures is 1%. There is a pressing need for large, prospective studies of the frequency and clinical course of AVMs in well-defined, stable populations, taking account of their prognostic heterogeneity 5).

According to reports, 0.1% of the population harbors an AVM 6) 7).

Both sexes are affected equally. AVMs are the leading cause of nontraumatic intracerebral hemorrhage in people less than 35 years old 8).

Most lesions reach attention in patients in their 40’s and 75% of the hemorrhagic presentations occur before the age of 50 years 9)

According to autopsy studies, only 12% of AVMs become symptomatic during life 10).


They are the most frequently encountered structural cause of spontaneous intracerebral hemorrhage in childhood, excluding hemorrhages of prematurity.

AVMs are seen more frequently on MRI with advancing age in children and young adults 11).

References

1) Ajiboye N, Chalouhi N, Starke RM, Zanaty M, Bell R. Cerebral arteriovenous malformations: evaluation and management. ScientificWorldJournal. 2014;2014:649036. doi: 10.1155/2014/649036. Epub 2014 Oct 15. Review. PubMed PMID: 25386610; PubMed Central PMCID: PMC4216697. 2) van Beijnum J, van der Worp HB, Algra A, Vandertop WP, van den Berg R, Brouwer PA, van der Sprenkel JW, Kappelle LJ, Rinkel GJ, Klijn CJ. Prevalence of brain arteriovenous malformations in first-degree relatives of patients with a brain arteriovenous malformation. Stroke. 2014 Nov;45(11):3231-5. doi: 10.1161/STROKEAHA.114.005442. Epub 2014 Sep 18. PubMed PMID: 25236872. 3) Laakso A, Hernesniemi J. Arteriovenous malformations: epidemiology and clinical presentation. Neurosurg Clin N Am. 2012 Jan;23(1):1-6. doi: 10.1016/j.nec.2011.09.012. Review. PubMed PMID: 22107853. 4) Berman MF, Sciacca RR, Pile-Spellman J, Stapf C, Connolly ES Jr, Mohr JP, Young WL. The epidemiology of brain arteriovenous malformations. Neurosurgery. 2000 Aug;47(2):389-96; discussion 397. Review. PubMed PMID: 10942012. 5) Al-Shahi R, Warlow C. A systematic review of the frequency and prognosis of arteriovenous malformations of the brain in adults. Brain. 2001 Oct;124(Pt 10):1900-26. Review. PubMed PMID: 11571210. 6) , 9) Brown R. D., Jr., Wiebers D. O., Torner J. C., O’Fallon W. M. Frequency of intracranial hemorrhage as a presenting symptom and subtype analysis: a population-based study of intracranial vascular malformations in Olmsted County, Minnesota. Journal of Neurosurgery. 1996;85(1):29–32. doi: 10.3171/jns.1996.85.1.0029. 7) The Arteriovenous Malformation Study Group Arteriovenous malformations of the brain in adults. The New England Journal of Medicine. 1999;340(23):1812–1818. doi: 10.1056/NEJM199906103402307. 8) Ruíz-Sandoval J. L., Cantú C., Barinagarrementeria F. Intracerebral hemorrhage in young people: analysis of risk factors, location, causes, and prognosis. Stroke. 1999;30(3):537–541. doi: 10.1161/01.STR.30.3.537. 10) McCormick W. E. Classification, pathology and natural history of angiomas of the central nervous system. Weekly Update: Neurology and Neurosurgery. 1978;14:2–7. 11) O’Lynnger TM, Al-Holou WN, Gemmete JJ, Pandey AS, Thompson BG, Garton HJ, Maher CO. The effect of age on arteriovenous malformations in children and young adults undergoing magnetic resonance imaging. Childs Nerv Syst. 2011 Aug;27(8):1273-9. doi: 10.1007/s00381-011-1434-9. Epub 2011 Mar 26. PubMed PMID: 21442267.

Internal maxillary artery to middle cerebral artery bypass

Internal maxillary artery to middle cerebral artery bypass

The cervical carotid system has been used as a source of donor vessels for radial artery or saphenous vein grafts in cerebral bypassInternal maxillary artery to middle cerebral artery bypass has been described as an alternative, with reduction of graft length potentially correlating with improved potency.

The internal maxillary artery to middle cerebral artery “middle” flow bypass allows for shorter graft length with both the proximal and distal anastomoses within the same microsurgical field. These unique variable flow grafts represent an ideal opportunity for use of the cephalic vein of the forearm, which is more easily harvested than the wider saphenous vein graft and which has good match size to the M1/M2 segments of the middle cerebral artery. The vessel wall is supple, which facilitates handling during anastomosis. There is lower morbidity potential than utilization of the radial artery. Going forward, the cephalic vein will be the preferred choice for external carotid-internal carotid transplanted conduit bypass for Nossek et al. 1).

The internal maxillary artery (IMA) has been proposed as a donor to decrease invasiveness, but its length is insufficient for direct intra intracranial bypass surgery. Feng et al., reported interposition of a superficial temporal artery (STA) graft for high-flow IMA to middle cerebral artery (MCA) bypass using a middle fossa approach.

Twelve specimens were studied. A 7.5-cm STA graft was obtained starting 1.5 cm below the zygomatic arch. The calibers of STA were measured. After a pterional craniotomy, the IMA was isolated inside the infratemporal fossa through a craniectomy within the lateral triangle (lateral to the posterolateral triangle) in the middle fossa and transposed for proximal end-to-end anastomosis to the STA. The Sylvian fissure was split exposing the insular segment of the MCA, and an STA-M2 end-to-side anastomosis was completed. Finally, the length of graft vessel was measured.

Average diameters of the proximal and distal STA ends were 2.3 ± 0.2 and 2.0 ± 0.1 mm, respectively. At the anastomosis site, the diameter of the IMA was 2.4 ± 0.6 mm, and the MCA diameter was 2.3 ± 0.3 mm. The length of STA graft required was 56.0 ± 5.9 mm.

The STA can be used as an interposition graft for high-flow IMA-MCA bypass if the STA is obtained 1.5 cm below the zygomatic arch and the IMA is harvested through the proposed approach. This procedure may provide an efficient and less invasive alternative for high-flow EC-IC bypass 2).


The maxillary artery runs parallel to the frontal branch of the superficial temporal artery and is located on average 24.8 ± 3.8 mm inferior to the midpoint of the zygomatic arch. The pterygoid segment of the MaxA is most appropriate for bypass with a maximal diameter of 2.5 ± 0.4 mm. The pterygoid segment can be divided into a main trunk and terminal part based on anatomic features and use in the bypass procedure. The main trunk of the pterygoid segment can be reached extracranially, either by following the deep temporal arteries downward toward their origin from the MaxA or by following the sphenoid groove downward to the terminal part of the pterygoid segment, which can be followed proximally to expose the entire MaxA. In comparison, the prebifurcation diameter of the superficial temporal artery is 1.9 ± 0.5 mm. The average lengths of the mandibular and pterygoid MaxA segments are 6.3 ± 2.4 and 6.7 ± 3.3 mm, respectively.

The MaxA can be exposed without zygomatic osteotomies or resection of the middle fossa floor. Anatomic landmarks for exposing the MaxA include the anterior and posterior deep temporal arteries and the pterygomaxillary fissure 3).


Long Wang published all internal maxillary artery (IMA) bypasses performed between January 2010 and July 2018 in a single-center, single-surgeon practice.

In total, 12 patients (9 males, 3 females) with Complex middle cerebral artery aneurysms (CMCAAs) managed by high-flow IMA bypass were identified.

The mean size of CMCAAs was 23.7 mm (range 10–37 mm), and the patients had a mean age of 31.7 years (range 14–56 years). The aneurysms were proximally occluded in 8 cases, completely trapped in 3 cases, and completely resected in 1 case. The radial artery was used as the graft vessel in all cases. At discharge, the graft patency rate was 83.3% (n = 10), and all aneurysms were completely eliminated (83.3%, n = 10) or greatly diminished (16.7%, n = 2) from the circulation. Postoperative ischemia was detected in 2 patients as a result of graft occlusion, and 1 patient presenting with subarachnoid hemorrhage achieved improved modified Rankin Scale scores compared to the preoperative status but retained some neurological deficits. Therefore, neurological assessment at discharge showed that 9 of the 12 patients experienced unremarkable outcomes. The mean interval time from bypass to angiographic and clinical follow-up was 28.7 months (range 2–74 months) and 53.1 months (range 19–82 months), respectively. Although 2 grafts remained occluded, all aneurysms were isolated from the circulation, and no patient had an unfavorable outcome.

The satisfactory result in the present study demonstrated that IMA bypass is a promising method for the treatment of CMCAAs and should be maintained in the neurosurgical armamentarium. However, cases with intraoperative radical resection or inappropriate bypass recipient selection such as aneurysmal wall should be meticulously chosen with respect to the subtype of MCA aneurysm 4).


Wang L, Qian H, Shi X. The Reiteration of “Less Invasive” Way and Graft Selections for Internal Maxillary Bypass. World Neurosurg. 2018 Sep 8. pii: S1878-8750(18)32037-0. doi: 10.1016/j.wneu.2018.08.228. [Epub ahead of print] PubMed PMID: 30205227.

Videos

Internal Maxillary Artery to M2 Middle Cerebral Artery Bypass With Modified Superficial Temporal Artery Graft: 3-Dimensional Operative Video 5).


A video demonstrates a 37-year-old female who presented with a 1-month history of severe headache. Her complex middle cerebral artery (MCA) aneurysm was treated by IMaxA bypass with radial artery graft. Preoperative neuroimaging revealed a giant, fusiform, thrombosed aneurysm that extensively involved the sphenoidal (M1) and insular (M2) segments of the MCA. After a multidisciplinary discussion, the reversal high-flow IMaxA bypass was performed, followed by proximal MCA occlusion. We approached the aneurysm using a frontotemporal craniotomy with zygomatic osteotomy to expose the pterygoid segment of IMaxA (IM2), which is defined as the “SHI” IMaxA bypass method. Simultaneously, the radial artery graft was harvested and prepared before being anastomosed in an end-to-end fashion to the IM2 using No. 9-0 polypropylene. The free end of the RAG was then brought to the sylvian fissure and anastomosed to the M2 in an end-to-side manner. The proximal part of M1 after the bypass takeoff was then occluded with a permanent aneurysm clip (Aesculap Instruments Corp., Tuttlingen, Germany). Complete elimination of the aneurysm with a patent graft artery was observed postoperatively, and the patient was discharged with intact neurologic function (modified Rankin Scale score 0) 6).

References

1)

Nossek E, Costantino PD, Chalif DJ, Ortiz RA, Dehdashti AR, Langer DJ. Forearm Cephalic Vein Graft for Short, “Middle”-Flow, Internal Maxillary Artery to Middle Cerebral Artery Bypass. Neurosurgery. 2015 Sep 23. [Epub ahead of print] PubMed PMID: 26418874.
2)

Feng X, Meybodi AT, Rincon-Torroella J, El-Sayed IH, Lawton MT, Benet A. Surgical Technique for High-Flow Internal Maxillary Artery to Middle Cerebral Artery Bypass Using a Superficial Temporal Artery Interposition Graft. Oper Neurosurg (Hagerstown). 2017 Apr 1;13(2):246-257. doi: 10.1093/ons/opw006. PubMed PMID: 28927217.
3)

Yağmurlu K, Kalani MYS, Martirosyan NL, Safavi-Abbasi S, Belykh E, Laarakker AS, Nakaji P, Zabramski JM, Preul MC, Spetzler RF. Maxillary Artery to Middle Cerebral Artery Bypass: A Novel Technique for Exposure of the Maxillary Artery. World Neurosurg. 2017 Apr;100:540-550. doi: 10.1016/j.wneu.2016.12.130. Epub 2017 Jan 9. PubMed PMID: 28089839.
5)

Benet A, Meybodi AT, Feng X, Lawton MT. Internal Maxillary Artery to M2 Middle Cerebral Artery Bypass With Modified Superficial Temporal Artery Graft: 3-Dimensional Operative Video. Oper Neurosurg (Hagerstown). 2017 Apr 1;13(2):280. doi: 10.1093/ons/opw010. PubMed PMID: 28927219.
6)

Wang L, Qian H, Shi X. The “SHI” Internal Maxillary Bypass for 1 Giant Fusiform MCA bifurcation 2 Aneurysm: 2-Dimensional Operative Video. World Neurosurg. 2018 Oct 19. pii: S1878-8750(18)32360-X. doi: 10.1016/j.wneu.2018.10.063. [Epub ahead of print] PubMed PMID: 30347305.
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