Cerebral arteriovenous malformations associated with aneurysms – a report of 10 cases and literature review

Cerebral arteriovenous malformation (AVM) associated with an aneurysm first appeared in the literature in 1925.1 Walsh and King in 1942 reported the first case of a patient with an AVM and an aneurysm.2,3 More and more AVMs associated with aneurysms were found as the neuroradiological technology developed.2–16 To confirm the clinical characteristics of this combination of lesions, we analysed 10 patients harbouring AVMs and aneurysms operated in our hospital between October 1992 and May 1998, as well as reported cases in the literature.

Case reports

Cerebral arteriovenous malformations associated with aneurysms Ð a report of 10 cases and literature review

CLINICAL MATERIAL AND ANALYSIS OF REPORTED CASES

Yuguang Liu, Shugan Zhu, Liqun Jiao, Hongwei Wang, Xingang Li, Gang Li

The ages and sex of our patients and past reports are shown in Table 1. Of the 10 patients, there were four cases of subarachnoid haemorrhage (SAH), three cases of intraparenchymal haemorrhage, and one case of intraventricular haemorrhage. The remaining two cases were investigated because of headache, convulsion and progressive ischaemia. All patients underwent surgical procedures, and both lesions were managed in a single operation. No death occurred. At present, all patients are returned to their previous occupations. The locations and operations of AVMs and aneurysms of the 10 patients are presented in Table 2. No cases of multiple aneurysms were found in our series. The aneurysm multipicity of this combination of intracranial vascular lesions in the past reports is seen in Table 3. This combination of vascular lesions was divided into four types, depending on the site of the aneurysms and the blood supply to the AVMs:1,7–9 Type I, aneurysms located on a major feeding artery itself; Type II, aneurysms located on the proximal portion of the feeding system, but removed by one or more branching points, such as the ipsilateral internal carotid artery, the anterior communicating artery feeding the AVM; Type III, aneurysms located on the distal portion of the feeding system; Type IV, aneurysms located on arteries haemodynamically unrelated to the AVM. The constituent ratio (CR) of Types I–IV in our study and in the previous literature are shown in Table 4.

Department of Neurosurgery, Affiliated Hospital of Shandong Medical University, Jinan, P. R. China

Summary We analysed 10 cases of arteriovenous malformations (AVMs) associated with aneurysms and reviewed the literature in order to confirm the clinical characteristics of AVMs associated with aneurysms. The mean incidence of aneurysms in our AVM population was 9.1% and the average age was 38 years. The ratio of male to female was 1.3 to 1. The aneurysms (40–96%) were often located on a feeding artery and seldom (23%) at an arterial bifurcation. The mortality rate was 0–26% in surgically managed patients and 38–60% in conservatively treated patients. The combination of intracranial vascular lesions is not rare. Most patients presented with symptoms referable to their AVMs. Treating both lesions in a single operation is the best option. The prognoses for most patients was good. © 2000 Harcourt Publishers Ltd Journal of Clinical Neuroscience (2000) 7(3), 254–256 © 2000 Harcourt Publishers Ltd DOI: 10.1054/ jocn.1999.0206, available online at http://www.idealibrary.com on

Received 30 November 1998 Accepted 10 March 1999 Correspondence to: Dr Yuguang Liu, Department of Neurosurgery, Affiliated Hospital of Shandong Medical University, Jinan, P. R. China.

Table 1 Age and sex in our series and past reports

Age (mean) Sex male female

Suzuki (1979)7

Hayashi (1981)13

Batjer (1986)8

Brown (1998)9

Liu (1998)

Total

21–52 (38)

1–74 (42.5)

11–55

17–67 (38)

16–52 (34)

1–74 (38)

4 5

44 28

13 9

5 11

8 2

74 55

Table 2 Location and operation of AVM and aneurysm Case

Location

Operation

No.

AVM

Aneurysm

AVM

Aneurysm

Outcome

1 2 3 4 5 6 7 8 9 10

Rt anterio temporal Lt frontal Rt medial frontal Rt frontal Lt frontal Lt frontal Rt occipital Rt frontal Lt collosal Rt parietotemporal

rt ATA lt ACoA rt CMA rt ACoA lt ACoA lt ACoA rt PCA rt PCoA lt ACA rt PCoA

extirpation extirpation extirpation extirpation extirpation extirpation extirpation extirpation Partial removal embolisation

resection clipping resection wrapping clipping clipping resection clipping ligation embolisation

recovery recovery recovery improvement recovery recovery improvement recovery improvement recovery

rt=right; lt=left; ATA=anterior temporal artery; ACoA=anterior communicating artery; CMA = callosomaginal artery; PCA = posterior cerebral artery; PcoA = posterior commnicating artery; ACA = anterior cerebral artery

254

AVMs associated with aneurysms 255 Table 3 Summary of aneurysm multipicity Suzuki (1979)7

Hayashi (1981)13

Batjer (1986)8

Brown (1990)9

Liu (1998)

Total

9 0

53 21

11 11

8 8

10 0

91 40

single multiple

Table 4 CR of types I–IV Suzuki (1979)7

Type

No.

CR(%)

4

44.4

I II I&II III I&III II&III IV

3 2

Hayashi (1981)13

33.3 22.2

No.

CR(%)

41

36.6

45

40.2

26

23.2

Batjer (1986)8 No.

CR(%)

Brown (1990)9

Liu (1998)

No.

CR(%)

No.

CR(%)

10 7

38.5 26.9

2 6

20 60

22 14

50 32

8

30.8

1

10

8

18

1

3.8

1

10

Total

%

16 54 22 23 45 3 38

8 26.9 10.9 11.4 22.4 1.5 18.9

CR = constituent ratio

Table 5 Summary of incidence of AVM associated with aneurysm Author, year

Paterson et al. 19564 Anderson et al. 19599 Cronqvist et al. 19665 Perret et al. 19666 Suzuki et al. 19797 Batjer et al. 19868 Silber et al. 19871 Brown et al. 19909 Fengling et al. 199110 Total

Total series

AVM No.

Aneurysm %

110 9(autopsy) 150 490 140 157 31 91 162 1331

3 5 13 37 9 22 3 16 18 121

2.7 55.6 8.7 7.6 6.4 14.0 10.0 17.6 11.1 9.1

DISCUSSION Incidence Previously published series have suggested that between 2.7% and 17.6% of patients with AVM have associated with aneurysms (Table 5).1,4,5,8–11 Anderson and Blackwood reported an autopsy series with a high incidence of AVM with aneurysms, namely, five of nine cases (55.6%).11 Yasargil thought that the actual incidence of this combination might be higher than that reported in the literature because many small aneurysms could not be found on cerebral angiography.12 The incidences in Table 5 show an increasing incidence with time of publication of these papers. We have reviewed 1331 cases of AVMs, among which 121 patients harboured cerebral aneurysms. The average incidence is 9.1%. Aneurysms associated with an AVM account for 0.1–2% of intracranial aneurysms.1 Hayashi et al. analysed 72 previous cases of AVM associated with aneurysm in 1981.13 The patients included 44 males and 28 females. Their ages ranged from 1 to 74 years, with an average of 42.5 years. In our study there were eight males and two females, whose ages ranged from 16 to 52 years, with an average of 34 years.13 We combined 129 previous cases and our patients in Table 1. Their average age was 38 years, with a male to female ratio of 1.3 to 1. The average age of patients with AVM associated with aneurysm was lower than that of patients with aneurysm alone, and higher than that of patients with AVM alone. We found no cases of multiple aneurysms in our study, nor did Suzuki and Onuma,7 but both Batjer et al. and Brown et al.

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reported that the incidence of multiple aneurysms of this combination of vascular lesions was as high as 50%.8,9 Twenty-one patients (28%) had multiple aneurysms among 74 cases reviewed by Hayashi et al.13 In Table 3 it can be seen that multiple aneurysms accounted for 30% of the total cases. From these results, we may conclude that the incidence of multiple aneurysms associated with an AVM is higher than that for aneurysm alone whose average incidence is 20%.

Mechanism At present, three hypotheses have been advanced to explain the mechanism of this association.4,11,18 The three hypotheses are as follows: 1. Aneurysms are caused by haemodynamic stresses resulting from the presence of an AVM; 2. Both lesions are congenital disorders of vascular developments; and, 3. The association is purely coincidental. The first theory was proposed firstly by Paterson and McKissock in 19564 and has become the most popular. The reasons for supporting this theory include: aneurysms often are located on the feeding artery or feeding system to the AVM, accounting for 40–96% of cases, whereas only 10–23.2% (Table 4) of aneurysms are located on arteries haemodynamically unrelated to the AVM;4–9,13–16 some conditions, such as moyamoya disease, causing haemodynamic abnormality, are often secondary to aneurysms;1 Somach and Shenkin reported two of six patients who had undergone carotid artery ligation and who had developed aneurysms on the contralateral internal carotid artery 3 to 10 years postoperatively;15 some aneurysms disappeared or decreased in size after excision of the AVM fed by the parent artery;13,15 some (23–55.6%) aneurysms are located at atypical sites, namely not at an arterial bifurcation9. The second theory was developed to explain the cases whose aneurysms had no involvement in AVM blood supply. Anderson and Blackwood thought that both lesions were simply part of a constellation of multiple vascular anomalies in the same patient in 1959.11 Deruty et al. reported three cases of deepseated AVMs associated with middle cerebral artery aneurysms;4 these AVMs were not high flow and the aneurysms were also unrelated haemodynamically. Boyd-Wilson thought that the association of

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256 Liu et al. / Sullivan et al.

these lesions was probably coincidental.17 The incidence of AVM associated with aneurysm in autopsies is markedly higher than that of aneurysm alone in the general population;1,11 this result suggests that the association is not a coincidence. It is shown that type IV accounts for 18.9% in Table 4, and it supports the theory that both lesions are congenital disorders of vascular development. Management and prognosis The mortality rate is high in conservatively managed patients. Fifteen of 26 cases which were treated conservatively were reported by Perret and Nishioka; nine died (60%).6 Gamache et al. reviewed 42 medically managed patients from the literature in 1981; 38% died, 7% had significant neurological difficulties, and only 14% did well.18 Suzuki and Onuma reported eight patients who were treated by radical surgery. No deaths occurred in their cases and they thought that surgery should be directed to treatment of the source of haemorrhage.7 Batjer et al. reported nineteen patients who underwent surgical procedures; operation was directed toward the aneurysm alone in eight cases, toward the AVM in three cases, and to both lesions in eight patients; five (26%) died, two of whom died as a result of massive intraoperative haemorrhage from aneurysm rupture after excision of the AVM. The remaining three patients (69%) had good outcomes, with a return to their premorbid occupations. They thought that the abrupt resection of an AVM could cause massive haemorrhage or disastrous SAH from aneurysms an feeding arteries.8,9 Exceptions to this general rule are cases of large intraparenchymal clots from AVM, or patients with unrelated remote aneurysms. Obliterating the aneurysms and then microsurgically resecting the AVMs is the safest approach to symptomatic lesions of this type. Elective obliteration of aneurysms associated with an AVM in asymptomatic patients was recommended by Batjer et al. even if subsequent resection of the AVM was not contemplated.8 Our operative principle is the same as that of Batjer et al. Treating both lesions in a single operation is the best option. In our ten cases, all were managed in a single operation, and with good outcome. Hayashi et al. observed that two unoperated aneurysms disappeared after excision of the AVM;13 they thought that aneurysms situated on arteries feeding an AVM may possibly be cured merely by excision of the AVM,13 but spontaneous disappearance of aneurysms is rare. REFERENCES 1. Jianning Zhang. The clinical characteristics and treatment of arteriovenous malformation associated with aneurysm. Foreign Medicine, Neurology and Neurosurgery 1992; 19: 228–230. 2. Walsh FB, King AB. Ocular signs of intracranial saccular aneurysms: experimental work on collarteral circulation through the ophthalmic artery. Arch Ophthalnol 1942; 27: 1–33. 3. Yuguang Liu Cerebral arteriovenous malformation. In: Yuguang Liu (ed.) Congential craniocerebal Diseases. Jinan: Jinan Press 1993; 211–212. 4. Paterson JH, Mckissock W. A clinical survey of intracranial angiomas with special reference to their mode of progression and surgical treatment: a report of 11 cases. Brain 1956; 79: 233–266. 5. Cronqvist S, Troupp H. Intracranial arteriovenous malformation and arterial aneurysm in the same patient. Acta Neurol Scand. 1966; 42: 307–316. 6. Perret G. Nishioka H. Report on the Cooperative Study of Intracranial Aneurysms and Subarachnoid Hemorrhage. Section VI. Arteriovenous malformations. An analysis of 545 cases of craniocerebral arteriovenous malformations and fistulae reported to the cooperative study. J Neurosurgery. 1966; 25: 467–490. 7. Suzuki J, Onuma T. Intracranial aneurysms associated with arteriovenous malformations. J Neurosurgery. 1979; 50: 742–746. 8. Batjer H. Suss R, Samson D. Intracranial arteriovenous malformations associated with aneurysms. Neurosurgery. 1986; 18: 29–25. 9. Boyed-wilson JS: The association of cerebral angiomas with intracranial aneurysms. J Neurol Neurosurg. Psychiatry. 1959; 22: 218–223.

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10. Feng Ling. Cerebral arteriovemsus malformation. In: Fengling, ed. Interventional Neuroradiology. Beijing: People’s Health Press, 1991; 105–106. 11. Anderson RM, Blackwood W: The association of atreriovenous agioma and saccular aneurysms of the arteries of the brain. J Pathol Bacteriol. 1959; 77: 101–110. 12. Yasargil MG. Microneurosurgery. Vol II, New York: Thieme-Stratton, 1984; 395. 13. Hayashi S, Arimoto T, Itakuma T et al. The association of intracranial aneurysms and arteriovenous malformation of the brain. J Neurosurgery. 1981; 55: 971–975. 14. Somach FM, Shenkin HA: Angiographic end-results of carotid ligation in the treatment of carotid aneurysm: J Neurosurgery. 1966; 24: 966–974. 15. Shenkin HA, Jenkins F, Kim K. Arteriovenous anomaly of the brain associated with cerebral aneurysm. Case report. J Neurosurgery. 1971; 34: 225–228. 16. Takara E. Inoue N. Kohno H. Disappearance of the co-existing aneurysms and arteriovenous malformation after wrapping of aneurysms. No. Shinkei Geka. 1980; 8: 587–591. 17. Brown R, Wiebers D, Forbes G. Unruptured intracranial aneurysms and arteriovenous malformations: frequency of intracranial hemorrhage and relationship of lesions. J Neurosurgery. 1990; 73: 859–863. 18. Gamache FW, Drake CG, Peerless SJ et al. Intracranial arteriovenous malformation associated with intracranial aneurysm: a review. Presented at the 50th Annual Meeting of the American Association of Neurological Surgeons. Boston, Massachusetts, 1981, April. 8.

Parkinsonism after correction of hyponatremia with radiological central pontine myelinolysis and changes in the basal ganglia A.A. Sullivan MBBS, R.D. Chervin MD, R.L. Albin, MD Department of Neurology, University of Michigan Medical Center, Ann Arbor, Michigan, USA

Summary Parkinsonism has been rarely described following central pontine and extrapontine myelinolysis. We report a case of parkinsonism developing following rapid correction of hyponatremia with radiological evidence of central pontine myelinolysis and changes in the basal ganglia. A 56-year-old man developed drooling and bilateral hand tremors 3 weeks after correction of hyponatremia from 103 to 125 mmol/L over 14 h. He had a prominent 6 Hz resting tremor which worsened with action and mild cogwheel rigidity. Magnetic resonance imaging (MRI) showed changes consistent with central pontine myelinolysis and increased signal on T1weighted images in the putamen bilaterally. His tremor responded well to L-dopa therapy. There have been several other cases of parkinsonism developing after central pontine/extrapontine myelinolysis. Increased signal in the basal ganglia on T1-weighted images has been described in another case of central pontine myelinolysis imaged about the same time after sodium correction as our case. © 2000 Harcourt Publishers Ltd Journal of Clinical Neuroscience (2000) 7(3), 256–259 © 2000 Harcourt Publishers Ltd DOI: 10.1054/ jocn.1999.0192, available online at http://www.idealibrary.com on

Keywords: parkinsonism, hyponatremia, central pontine myelinolysis, extrapontine myelinolysis Received 7 December 1991 Accepted 12 February 1999

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