Correlation between angioarchitectural characteristics of brain arteriovenous malformations and clinical presentation of 183 patients

Batista, Ulysses Caus; Pereira, Benedito Jamilson Araujo; Joaquim, Andrei Fernandes; Tedeschi, Helder; Piske, Ronie Leo

doi:10.1590/0004-282X-ANP-2020-0291

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Article • Arq. Neuro-Psiquiatr. 80 (1) • Jan 2022 • https://doi.org/10.1590/0004-282X-ANP-2020-0291 copy

Correlation between angioarchitectural characteristics of brain arteriovenous malformations and clinical presentation of 183 patients

Impacto das características angioarquiteturais das malformações arteriovenosas cerebrais na apresentaçáo clínica: análise de 183 pacientes

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Background:

The correlation between angioarchitecture and clinical presentation of brain arteriovenous malformation (bAVM) remains a subject of debate.

Objective:

The main purpose of the present study was to assess the correlation between angioarchitectural characteristics of bAVM and clinical presentation.

Methods:

A retrospective review of all consecutive patients presenting a bAVM who underwent a cerebral angiography at Beneficencia Portuguesa Hospital in São Paulo between January 2006 and October 2016 was carried out. Patients were divided in five groups: group 1 - hemorrhage; group 2 - seizure; group 3 - headache; group 4 - progressive neurological deficits (PND); group 5 - incidental).

Results:

A total of 183 patients were included, with group 1 comprising 56 cases, group 2 49 cases, group 3 41 cases, group 4 28 cases, and group 5 9 cases. Regarding hemorrhage presentation, a statistical correlation was observed with female gender (P < 0.02), Spetzler-Martin 3B (P < .0015), and lesions with low flow (P < 0.04). A positive association was found between group 2 and age less than 36 years (P < 0.001), male sex (P < 0.018), presence of superficial lesions not classified as SM 3B (P < 0.002), presence of venous ectasia (p <0.03), and arterial steal phenomenon (P < 0.03). Group 4 was associated with older age (P < 0.01).

Conclusions:

Angioarchitectural characteristics can be correlated with some clinical presentations as well as with some clinical data, making it possible to create predictive models to differentiate clinical presentations.

Keywords:
Central Nervous System Vascular Malformations; Intracranial Arteriovenous Malformations; Seizures; Stroke

Characteristics studied	Description
Clinical presentation	Five groups were created: 1) intracranial hemorrhage, 2) epileptic seizures, 3) persistent headache, 4) progressive neurological deficits, 5) incidental finding on image exam.
Topography	Lesions related to cerebral cortex were classified as superficial AVMs; in the basal ganglia (exclusive nutrition by perforating branches) as deep lesions. Those located in the cerebellum or in the brainstem were classified as posterior fossa AVMs55. Lv X, Wu Z, Jiang C, Yang X, Li Y, Sun Y, et al. Angioarchitectural characteristics of brain arteriovenous malformations with and without hemorrhage. World Neurosurg. 2011 Jul-Ago;76(1-2):95-9. https://doi.org/10.1016/j.wneu.2011.01.044 https://doi.org/10.1016/j.wneu.2011.01.0... .
Grade 3 Spetzeler-Martin scale modified	Grade 3 Spetzeler-Martin Scale was divided into two groups: grade 3A and 3B. AVMs that received two points for medium size, one point for eloquent location, and zero for superficial venous drainage were classified as 3A. Those that were small (1 point), located in eloquent areas (1 point), and a deep venous drainage (1 point) were classified as 3B (Figure 1).
Intralesional flow	Classified as high or low flow. High flow referred to cases where contrast opacification occurred only in the malformation without filling other normal branches of this territory. In low-flow lesions, other arteries of the same vascular territory were also opacified.
Intranidal aneurysms	Aneurysmal formation located inside the nidus and confirmed in more than one angiographic projection (Figure 2-A).
Venous aneurysms	Aneurysmatic dilatations in a vein draining the lesion, confirmed by different angiographic projections (Figure 2-B).
Venous ectasia	Marked increase in the diameter and tortuosities of the vessel that drains the AVM (Figure 2-B)88. Hirai S, Mine S, Yamakami I, Ono J, Yamaura A. Angioarchitecture related to hemorrhage in cerebral arteriovenous malformations. Neurol Med Chir (Tokyo). 1998;38 Suppl 38:165-70. https://doi.org/10.2176/nmc.38.suppl_165 https://doi.org/10.2176/nmc.38.suppl_165... .
Venous congestion	Redirecting draining flow to other veins hindering normal brain-tissue drainage (Figure 2-C).
Arterial steal	Insufficient filling of the normal branches at the same territory where the AVM are located.
Dural vascularization	Participation of dural vessels supplying the AVM (Figure 2-D).
Deep venous drainage	Direct drainage to the deep venous system (Figure 3)99. Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg. 1986 Oct;65(4):476-83. https://doi.org/10.3171/jns.1986.65.4.0476 https://doi.org/10.3171/jns.1986.65.4.04... .

Demographic characteristics	General	%	Hemorrhage	%	Seizure	%	Headache	%	PND	%	Incidental	%
Mean age	37		37,5		32		34,5		45,2		45,4
Maximum age	84		75		55		69		71		84
Minimum age	18		18		18		18		22		19
Standat deviation	14		12		10,3		13,5		16,2		22,5
Male	93	50.8	22	39.2	31	63.2	18	43.9	17	60.7	5	55.5
Female	90	49.2	34	60.7	18	36.8	23	56.1	11	39.3	4	44.5
Superficial lesion	124	67.7	25	44.6	46	93.9	32	75.6	17	60.7	4	44.4
Deep lesion	36	18.6	19	33.9	3	6.1	6	14.6	6	21.4	2	22.2
Posterior fossa lesion	23	12.5	12	21.4	0	0	3	7.3	5	17.8	3	33.3
Total	183		56		49		41		28		9

Angioarchitectural characteristics	General	%	Hemorrhage	%	Seizure	%	Headache	%	PND	%	Incidental	%
SM 1	47	25.6	16	28.5	11	22.4	10	24.4	7	25	3	33.3
SM 2	61	33.3	13	23.2	17	34.6	21	42.8	10	35.7	2	22.2
mSM 3A	30	16.3	7	12.5	11	22.4	8	19.5	4	14.3	1	11.1
mSM 3B	30	16.3	17	30.3	2	4	3	7.3	6	21.4	2	22.2
SM 4	13	7.1	3	5.3	8	16.3	0	0	1	3.6	1	11.1
SM 5	2	1	0	0	1	2	0	0	1	3.6	0	0
High flow	65	35.5	13	23.2	20	40.8	19	46.3	11	39.2	2	22.2
Intranidal aneurysms	41	22.4	16	28.5	10	40.8	6	14.6	5	17.8	4	44.4
Venous aneurysms	30	16.3	5	8.9	8	16.3	10	24.4	5	17.8	2	22.2
Venous ectasias	26	14.2	5	8.9	12	24.5	2	4.9	7	25	0	0
Venous congestions	39	21.3	9	16	9	18.3	10	24.4	9	32.1	2	22.2
Arterial steal phenomenon	6	3.2	0	0	4	8.1	1	2.4	0	0	1	11.1
Dural vascularization	13	7.1	4	7.1	5	10.2	3	7.3	0	0	1	11.1
Deep venous drainage	64	34.9	25	44.6	13	26.5	9	22	13	46.4	4	44.4
Total	183		56		49		41		28		9

Angioarchitectural characteristics	Hemorrhage			Seizure			Headache			PND
Angioarchitectural characteristics	P	OR	CI	P	OR	CI	P	OR	CI	P	OR	CI
Superficial x deep location	0.0003	0.22	0.10 - 0.49	0.002	6.48	1.88 - 22.34	0.361	1.73	0.66 - 4.56	0.0007	7.72	2.42 - 24.62
Superficial x PF location	0.0028	0.23	0.09 - 0.585	0	0	0	0.29	2.31	0.64 - 8.32	0.012	5.56	1.59 - 19.37
Deep x PF location	0.82	1.02	0.35 - 2.92	0	0	0	0.995	1.33	0.29 - 5.95	0.8845	0.72	0.19 - 2.70
Grade 3B mSM scale	0.0015	3.82	1.70 - 8.57	-	-	-	-	-	-	-	-	-
Low flow	0.032	2.29	1.12 - 4.68	0.46	1.36	0.69 - 2.67	0.144	1.8	0.88 - 3.65	0.811	1.21	0.52 - 2.76
Intranidal aneurysms	0.25	1.63	0.78 - 3.37	0.848	0.85	0.381 - 1.90	0.25	0.52	0.20 - 1.35	0.7	0.71	0.25 - 2.02
Venous aneurysms	0.11	0.4	0.14 - 1.10	0.83	0.99	0.41 - 2.40	0.18	1.96	0.83 - 4.62	0.96	1.13	0.39 - 3.25
Venous ectasias	0.31	0.52	0.18 - 1.47	0.03	2.77	1.18 - 6.53	0.1	0.26	0.05 - 1.17	0.109	2.53	0.94 - 6.80
Venous congestions	0.34	0.61	0.27 - 1.40	0.7	0.78	0.34 - 1.78	0.74	1.25	0.55 - 2.85	0.204	1.97	0.81 - 4.79
Arterial "steal"	0	0	0	0.02	5.86	1.03 - 33.11	0.87	0.68	0.07 - 6.03	0	0	0
Dural vascularization	0.76	1.00	0.29 - 3.42	0.21	2.38	0.77 - 7.29	0.77	1.04	0.27 - 3.97	0	0	0
Deep venous drainage	0.087	1.79	0.94 - 3.44	0.191	0.58	0.28 - 1.19	0.08	0.45	0.20 - 1.03	0.25	1.75	0.77 - 3.95

Multivariate analysis	Hemorrhage		Seizure
Multivariate analysis	P	OR (CI 95%)	P	OR (CI 95%)
Mean age			0.001	0.95 (0.92 - 0.98)
Male	0.021	0.45 (0.23 a 0.89)	0.018	2.46 (1.17 a 5.19)
S-M 3B	0.001	3.95 (1.69 a 9.2)	0.002	0.08 (0.01 a 0.4)
High flow studied	0.047	0.47 (0.22 a 0.99)
Intranidal aneurysm
Venous aneurysm
Venous ectasia			0.037	2.84 (1.07 a 7.56)
Venous congestion
Arterial steal phenomenon			0.039	2.3 (1.04 a 5.1)
Dural vascularization
Deep venous drainage

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[1] Correspondence:
Ulysses Caus Batista; Email: ulysses@neurocirurgiacapixaba.com.