British Journal of Neurosurgery
ISSN: 0268-8697 (Print) 1360-046X (Online) Journal homepage: http://www.tandfonline.com/loi/ibjn20
Spinal Arteriovenous Malformations and Subarachnoid Haemorrhage Reginald H. Shephard To cite this article: Reginald H. Shephard (1992) Spinal Arteriovenous Malformations and Subarachnoid Haemorrhage, British Journal of Neurosurgery, 6:1, 5-12, DOI: 10.3109/02688699209002895 To link to this article: http://dx.doi.org/10.3109/02688699209002895
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British Journal of Neurosurgery (1992) 6 , 5-12
ORIGINAL ARTICLE
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Spinal arteriovenous malformations and subarachnoid haemorrhage REGINALD H. SHEPHARD
Trent Regional Department of Neurosurgery, Queen3 University Hospital, Nottingham, UK
Abstract Seventy patients with spinal arteriovenous malformations (AVMs) referred to the author over a 25-year period (1958-82), were equally divided between congenital, intradural and acquired, dural lesions. Amongst the intradural AVMs, were 22 with subarachnoid haemorrhage (SAH), a presenting feature in 18. The clinical findings in these 22 patients are tabulated, the radiological and operative findings indicated, and an account given of the overall outcome. Early operation is recommended, with a good prognosis and pevention of further haemorrhage in most cases. An extended follow-up has been maintained. The influence of menstruation, pregnancy and the puerperium on AVM symptoms is described.
Key words: Spinal arteriovenous malformation, subarachnoid haemorrhage, pregnancy.
‘le coup de poignard’ of Michon; by cervical, brachial or sciatic radicular pains and a painful stiff neck. Cerebral symptoms occur with severe bleeds and cervical lesions. Opisthotonus and coma may supervene, and clinically, it may not be possible to differentiate spinal from cranial SAH.
Introduction Intraspinal arteriovenous malformations (AVMs) are now classified into two main types: those in the intradural space (congenital) and those of the dura (acquired). Rosenblum et d . , l in a report on 81 cases, made this distinction: of 54 intradural lesions, 28 presented with subarachnoid haemorrhage (SAH). The differences between the two types of AVM are listed in Table I. Subarachnoid haemorrhage from other conditions is not considered here and this paper does not concern dural, acquired AVMs. The description of these is included in other papers.*-’ Intradural AVMs presenting in other ways will be the subject of another paper.
Incidence Spinal SAH, described by Wyburn-Mason? Henson and Croft,l0 and as a distinct clinical entity by Fincher,” is rare compared with cranial SAH. In Walton’s review12 of 312 patients with SAH, the origin was spinal in only three, only one of whom had an AVM. There are few early reports of significant numbers of cases of SAH from spinal AVMs. In a number of papers4*8-10J2-33 from 1900 to 1979, of 227 patients with AVMs, only 47 had
Onset Spinal SAH usually declares itself with dramatic suddenness: by extremely severe back pain, 5
6
Reginald H. Shephard TABLE I. Comparison of patients with intradural and dural AVMs
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Age: mean (years) Sex: M / F History: mean (years) SAH: incidence Other features Segmental cutaneous haemangioma Expanded spinal canal Asymmetrical limb growth Other lesions (cerebral angioma and spinal haemangioblastoma)
proven SAH. In these 47, the sex was recorded in 27 (15 males, 12 females), age in 28 (mean of 28 years), and outcome in 23. Eight patients died and in only four was there a good result. Only two were followed up, each for 2 years. Since 1979, larger series have been described, including series of 1834 (now part of this series), 28l (52% SAH), and 233s (36% SAH) patients. The present study confirms the high incidence of SAH (63%) in spinal intradural AVMs. Patients with SAH were much younger than those with the dural lesion (Table 1). There was a preponderance of females with spinal SAH and AVM in this series (Table I). This has not been reported previously, a higher incidence in men having been recorded in most series. For example, Rosenblum et al. in their cases] stated that 70% of subdural AVMs were in males, although a separate analysis of the SAH cases was not done. However, as dural AVMs are much more common in males (85% in Rosenblum et al. and 80% in this series), there is a ‘loading factor’ in favour of males when the two main types of AVM are not differentiated.
Duration of history In the 47 cases up to 1979, the duration of history (mean of 25 cases) was 4.5 years, compared with 8.5 years in this series (and 2 years for the dural AVMs).
Intradural AVM
Dural AVM
28
54
16/19 7.5
2817 2
(with SAH) 8.5 22 (of 35)
None (of 35)
3 (all with SAH) 9 (4 with SAH) 5 (4 with SAH)
2 (both with SAH)
Clinical material in this series Of 70 patients with intraspinal AV 4s referred in 25 years, 35 had subdural lesions and 22 of these sustained SAH. Table I1 summarizes the principal clinical features. Additional features are referred to in the text and brief notes made on five further cases. Of the 22 cases who sustained SAH, myelography was performed in 21 and angiography in 19. In three early cases, classification, based on the criteria of Rosenblum et al.’ is retrospective. The AVMs were in the cervical region in four patients, upper dorsal in four, mid- or low-dorsal in seven, dorsi-lumbar in six and in the whole canal in one.
Case reports Case 8
A 27-year-old woman presented with right hemiplegia. She had sustained four SAHs at 13, 17, 19 and 27 years of age, the second with coma and right hemiplegia which failed to recover completely. AVM at C1 was diagnosed. X-ray therapy proved ineffective. Hemiparesis did not change with the third and fourth haemorrhages. Epilepsy was present for 3 years prior to admission. Angiogram confirmed C1/2 AVM (Figs 1 and 2). Following total excision, normal life was resumed including an uneventful pregnancy. The patient was followed up for 18 years.
F M F M F F F F F M F M F M M M M F F F F F
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
13 20 28 38 44 17 20 27 30 24 36 35 13 28 54 17 25 4 37 23 20 41
Age (years)
2Y 14 Y 8 Y 2Y 22 Y 29 Y 4Y 24 Y Months 2 wks 24 Y 48 h 2 wks Days Weeks 9Y
lY
8 Y 10 Y 12 Y 20 Y 41 Y
History 2 3 3 1 1 1 2 4 1 1 3 1 2 4 1 1 1 2 1 2 1 1
A. p’plegia A. p’plegia A. p’plegia A. p’paresis B-Sec. Synd B-Sec. Synd A. p’paresis R. h’paresis A. p’plegia Pain:Retn Q’paresis C. p’plegia A. p’plegia S. loss right arm S. level T6 Coma, p’paresis R. h’paresis Coma, q’paresis A. p’paresis Minimal A. p’paresis Weak left leg
No. of Symptom(s) at SAHs presentation
MSSp MSSp M
M
S S
MSSp MSSp MSSp MSSp MS MS MS M MSSp SSP MS MSSp MSSp
Deficit
5 N
N N N 3 Died N N 3 N
1
5
1
5 1 5 N
4 N N
N N
5 4 1 1 2 1 5 4 4 5 4 N 2 N 3 5 3 N
N
5
Post-op.
5
Pre-op.
Gait
3 2 2 3 N N 1 N 3 2 N 3 2 N 2 N N 3 1 1 2 N 6 5 2 2
N 3 N
-
N
11 10 4 7 13 8 8 12
-
27 23 18 12 16 21 15 18
Follow-up (years)
-
N
N
1 3 N N N N 3 1 N 3 N N N
2 N
Post-op.
Sphincter Pre-op.
Results (grade)
A, acute; p’plegia, paraplegia; B-Sec. Synd, Brown-Sequard Syndrome; R. h’paresis, right hemiparesis; Retn, retention of urine; Qparesis, quadriparesis; C, chronic; p’pparesis, paraparesis; Mymotor; S, sensory, Sp, sphincter. Functional grading of gait and bladder sphincter ( L o p e et d s ) : Bladder Gait N. Normal N. Normal 1. Mild hesitancy, urgency, frequency 1. Onset leg weakness 2. Restricted activity 2. Moderate: occasional incontinence, or retention 3. Severe: total incontinence, persistent retention 3. Support for walking 4. Crutches or 2 sticks 5. Unable to stand, confined to bed or wheelchair
Sex
Case no.
TABLE 11. List of the 22 patients with SAH
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8
Reginald H. Shephard earlier. Investigation at that time had shown expansion of the canal (at T 1 lJ2,Ll). Laminectomy with a provisional diagnosis of tumour revealed a yellow-stained AVM with arachnoditis. One year before the present admission the patient had had a weak leg and precipitancy of micturition (worse 2 days before a period). Angiography showed abnormal vessels at T12,Ll. At operation, a thrombosed aneurysmal varix (2.0 x 1.0 x 1.0 cm) was revealed, consisting of an old laminated clot and thick pigmented collagenous walls, and incorporating angiomatous vessels. After excision the patient’s symptoms subsided (Fig. 3).
Multiple haemorrhages As with cranial AVMs, the spinal lesions may result in several bleeds; a mean of 2 in 35 of the 47 earlier reported cases (in the series of Rosenblum et al.’ and also in this series). Recurrent haemorrhage is the most common FIG. 1. Case 8. AVM at C1/2 level vertebral angiography. cause of death.9J2*1s*L6 In this series, 10 patients had multiple haemorrhages (Table 11) with severe later bleeds in cases 1, 2 and 18 (see Results). Case 14 A 28-year-old man presented with sensory loss in the right arm. He had sustained his first SAH at the age of 4 years. Spinal AVM was diagnosed by myelography and limited laminectomy. Three further SAHs occurred at yearly intervals, at 26, 27 and 28 years of age, each after sexual intercourse, with collapse after the last incident. On examination right segmental (T4,5) cutaneous angioma (Fig. 4) papilloedema was found. Investigation of the expanded spinal canal by myelography, subclavian and selective spinal angiography showed a large upper dorsal AVM with multiple feeders. At C7-T5 laminectomy “a fearsome looking AVM with arachnoiditis” was seen. After excision of the AVM, the patient made a good recovery and was able to lead a normal life.
Case 22 A 41-year-old woman presented with a weak left leg. Left sciatica had occurred 8 years
SAH from AVM in pregnancy, puerperium and menstruation As with cranial AVMsP6 symptoms of spinal intradural AVM may be associated with the above conditions, but SAH has been rarely reported and was not described in DelmasMarsalet;’ N e ~ m a nand ~ ~ Newquist and Ma~field:~or in the three cases in Rosenblum et al.’ The cases described below are from the present series.
Pregnancy Case 3. A 28-year-old woman presented with acute paraplegia. She had complained of weak legs at the ages of 16, 18 and 21 (first pregnancy). The weakness was transient and recovery complete. Leg weakness recurred at age 24 during the second pregnancy, with incomplete recovery. The first SAH with paraparesis occurred during the third preg-
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Spinal arteriovenous malformations
FIG.2. Case 8. AVM at C1/2 level: operative photograph.
9
FIG. 3. Case 14. Segmental naevus on right side of trunk.
FIG.4. Case 22. (a) and (b) Operative appearances after excision.
10
Reginald H. Shephard
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nancy. Caesarean section and sterilization were then performed. At age 28, a second SAH occurred with paraplegia. Partial removal of an AVM filling the whole canal was performed.
Case 5. A 44-year-old woman presented with Brown-Sequard Syndrome. At age 18 a weak right leg persisted and increased transiently with the first two of four pregnancies. SAHs occurred at ages 41 and 44, the first with transient coma and persisting pain and themal sense loss in the left leg. Puerperium Case 9. A 30-year-old woman presented with acute paraplegia. At age 22, she became transiently paraplegic 3 months after the birth of her first baby. When aged 30 and 3 months, after the birth of her fourth baby, she had an SAH with flaccid paraplegia, which persisted after removal of an AVM of the conus medullaris. Menstruation Aggravation of spinal AVM symptoms has been reported p r e v i o ~ s l y . ~Case ~ . ~3~ in Kunc and B r e P had six SAHs in 7 years, “bleeding predominantly during menstruation”. Neither of the two women in Martin et aL40 had SAH but other symptoms were worse during menstruation. In case 22 in this series, symptoms were worse for 2 days before each period, and in case 3, 18 months after operation the paraparesis worsened with a monthly periodicity, reverting to the less severe state after giving ovarian hormone.
Treatment The only effective treatment is by operative removal of the AVM in whole or in part,22,25,26,41 or interruption of its blood supply by operation or artificial embolizat i ~ n . ~ Treatment ’-~~ by decompression or Xirradiation is largely i n e f f e c t i ~ e . ’ ~In . ~ ~this series, operations were performed on all patients: three in case 20, two in cases l, 6 and 13
and one in the remaining cases. Total removal was achieved in 11,partial in six and occlusion of feeders in four.
Results Pre- and post-operative grading of motor and sphincter function is shown in Table 11. One patient (case 18) with a combined AVM of the cord and medulla oblongata had a fatal peroperative haemorrhage. Ignoring advice, three women became pregnant after incomplete excision of AVMs, with worsening paraparesis in one (case 13), and a second SAH in one (case 20). The third (case 6) became pregnant a year after operation, declined to have a Caesarean section but nevertheless did well, and remains so in the 23rd year of follow-up (as is her son). She did, however, heed advice not to have more children. Pregnancies in two women after complete removals were uneventful. Follow-up was maintained in all survivors except case 9. The condition at the end of follow-up was worse in three patients, unchanged in two, and improved in 15. Thirteen were leading normal lives, some with slight residual signs. Five had recurrent symptoms1Jv13.16.21 at 6, 10, 5, 7, and 2 years after operation. The gait grade (Table 11) changed to 4 (case l), 3 (case 3) and 4 (case 13). Cases 16 and 21 had recurrent SAHs; the former recovered without operation and the latter had an operation elsewhere.
Discussion The present series has shown a high incidence in the y0ung,3~.~O a female preponderance and, in most patients, a long history (Table I). The tendency towards multiple haemorrhages and increasing disability with later incidents is apparent. There is a clear relation between pregnancy, etc. and symptoms of AVM (including SAH). Such may be due to variations in circulating oestrogen and progesterone with change in the size of the AVM or in the blood flow through it relative to the cord circ~lation.~~~~~
Spinal arteriovenous malformations
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Conclusions The operative management of the patients in this series of spinal SAH from intradural AVMs has improved their prognosis. They have been largely protected from recurrent bleeding and so of any risk to life. There have been four recurrent haemorrhages during follow-up of 20 patients for a mean of 10 years, compared with 31 bleeds in the same 20 patients during the pre-operative 10 years. Cases 1, 3, 13 and 16 with recurrent symptoms between 5 and 10 years after operation indicate a need for reasonable periods of follow-up. Shorter periods might have led to the assumption of a more favourable prognosis than in fact proved to be the case. In the absence of follow-up studies, evaluation of the later results of previous reported cases of AVM with haemorrhage has not been possible. From the relation between pregnancy and menstruation and symptoms of intradural AVMs, the importance of investigating spinal neurological symptoms in young women is clear, as is appropriate advice concerning the risks of pregnancy in the presence of an AVM.
Acknowledgements The author wishes to thank the neurologists and neurosurgeons who referred their patients and Dr Roger Whitaker for his skill in performing most of the myelographic and angiographic examinations. Thanks are also due to the staff of the Department of Medical Illustration, Derby Royal Infirmary for photographic assistance and to Dr Jatin Vaidya for his encouragement to write this paper.
Address for correspondence: R. H. Shephard, The Oaks, 776 Wollaton Road, Nottingham NG8 2AP, UK. References 1 Rosenblum B, Oldfield EH, Doppman JL, Dichiro G. Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulas and intradural AVMs in 81 patients. J Neurosurg 1987; 67:795-802.
11
2 Aminoff MJ, Logue V. Clinical features of spinal vascular malformations. Brain 1974; 97:197-210. 3 Aminoff MJ, Barnard RO, L o p e V. The pathophysiology of spinal vascular malformations. J Neurol Sci 1974; 23~255-63. 4 Aminoff MJ, Logue V. The prognosis of patients with spinal vascular malformations. Brain 1974; 97:211-18. 5 Logue V, Aminoff MJ, Kendall BE. Results of surgical treatment for patients with a spinal angioma. J Neurol Neurosurg Psychiat 1974; 1074-8 1. 6 Oldfield EH, Di Chiro G, Quindlen EA et al. Successful treatment of a group of spinal cord arteriovenous malformations by interruption of dural fistula. J Neurosurg 1983; 59:1019-30. 7 Symon L, Kuyama H, Kendall B. Dural arteriovenous malformations of spine. J Neurosurg 1984; 60238-47. 8 Michon P. Le coup de poignard rachidien: symptome initial de certaines hbmorragies sous-arachnoidiennes: essai sur les hemorragies meningees spinales. Presse Med 1928; 36964-6. 9 Wyburn-Mason R. Vascular Abnormalities and Tumours of the Spinal Cord and its Membranes. London: Henry Kimpton 1943. 0 Henson RA, Croft PB. Spontaneous spinal subarachnoid haemorrhae. Q J Med 1956; 97:63-66. 1 Fincher EF. Spontaneous subarachnoid hemorrhage in intradural tumors of the lumbar sac: a clinical syndrome. J Neurosurg 1951; 8576-84. 2 Walton JN. Subarachnoid haemorrhage. Edinburgh E. S. Livingstone 1956. 13 Balch A. A case of angioma of the spinal cord with recurrent haemorrhage. Br Med J 1990; 11:1707-8. 14 Frey L. Btude anatoma-clinique d‘un cas d’anburisme cirsoide de la moelle Cpinikre. Ann Anat Pathol 1928; 5:971-9. 15 Robertson EG.A case of arterial angioma of the spinal cord. Med J Aust 1938; 2:384. 16 Gilbert I. Angioma venosum racernosum with angiomatous lesions of skin and omentum. Br Med J 1952; 1:468-70. 17 Clark JMP. Traumatic haematomyellia from rupture of intramedullary angioma: report of a case. J Bone Jt Surg 1954; 36B:418-22. 18 Hook 0, Lidvall H. Arteriovenous aneurysms of the spinal cord. J Neurosurg 1958; 1584-91. 19 Newman MJD. Racemose angioma of the spinal cord. Q J Med 1959; 28:97-108. 20 Odom GL. Vascular lesions of the spinal cord malformations, spinal subarachnoid and extradural haemorrhage. Clin Neurosurg 1960; 8:196-234. 2 1 Antoni N. Spinal vascular malformations (angiomas) and myelomalacia. Neurology 1962; 12:795-804. 22 Shephard RH. Observations on intradural spinal angioma: treatment by excision. Neurochirurgia 1963; 6:58-74. 23 Hopkins CA, Wilkie FL, Voris DC. Extramedullary aneurysm of the spinal cord. J Neurosurg 1966; 24: 1021-3. 24 Bailey WL, Sperl MP. Angiomas of the cervical spinal cord. J Neurosurg 1969; 30560-8. 25 Kunc Z, Bret J. Diagnosis and treatment of vascular malformations of the spinal cord. J Neurosurg 1969; 30~436-45.
12
Reginald H. Shephard
26 Krayenbiihl H, YaSargil MG, McClintock HC. Treat-
27
28
29
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30 31 32 33 34 35
ment of spinal cord vascular malformations by surgical excision. J Neurosurg 1969; 30:427-35. Kaufman HH, Ommaya AK, Di Chiro G et al. Compression v. “steal”: the pathogenesis of symptoms in AVMs of the spinal cord. Arch Neurol 1970; 23~173-8. Herdt JR, Dichiro G, Doppman JL. Combined arterial and arteriovenous aneurysms of the spinal cord. Radiology 1971; 99589-93. Ludv J, Ringkjop R. Intraspinal vascular malformations. J Oslo City Hospitals 1973; 23:3-13. Pia HW. Diagnosis and treatment of spinal angiomas. Acta Neurochirurgia 1973; 28:l-12. Kaplan P, Hollenberg RD, Fraser FC. A spinal arteriovenous malformation with hereditary cutaneous hemangiomas. Am J Dis Child 1976; 130:1329-31. Parkinson D, West M. Spontaneous SAH, first from intracranial and then from intraspinal AVM: case report. J Neurosurg 1977; 47:965-8. Avman N, Ozkal E, Gokben B. Aneurysm and AVM of the spinal cord. Case report. Surg Neurol 1979; 11:5-6. Shephard RH, Vaidya JP. Spinal SAH; 30 cases; mainly from AVMs. J Neurol Neurosurg Psychiat 1979; 42:962. Scarff TB, Reigel DH. Arteriovenous malformations of
36 37 38
39
40 41 42 43 44
the spinal cord in children. Child’s Brain 1979; 5:341-51. Robinson JL, Hall CJ, Sedzimir CB. Subarachnoid hemorrhage in pregnancy. J Neurosurg 1972; 36:27-33. Delmas-Marsalet P. Poussees evolutives gravidiques et image lipiodolee characteristique des hemangiomes medullaires. Pr Med 1941; 49:964-5. Newman MJD. Spinal angioma with symptoms in pregnancy. J Neurol Neurosurg Psychiat 1958; 21:38-41. Newquist RE, Mayfield FH. Spinal angioma presenting during pregnancy. J Neurosurg 1960; 17541-5. Martin RA, Howard FM et al. Spinal cord vascular malformations with symptoms during menstruation. J Neurosurg 1977; 47:626-9. Djindjian R. Embolization of angiomas of the spinal cord. Surg Neurol 1975; 4:411-20. Theron J, Cosgrove R et al. Spinal AVMs advances in therapeutic embolization. Radiology 1986; 158: 163-9. Hall W, Oldfield E, Doppman JL. Recanalization of spinal AVMs following embolization. J Neurosurg 1989; 70714-20. Eldridge PR, Holland IM, Punt JA. Spinal arteriovensous malformations in children. Br J Neurosurg 1989; 3:393-7.
ISSN: 0268-8697 (Print) 1360-046X (Online) Journal homepage: http://www.tandfonline.com/loi/ibjn20
Spinal Arteriovenous Malformations and Subarachnoid Haemorrhage Reginald H. Shephard To cite this article: Reginald H. Shephard (1992) Spinal Arteriovenous Malformations and Subarachnoid Haemorrhage, British Journal of Neurosurgery, 6:1, 5-12, DOI: 10.3109/02688699209002895 To link to this article: http://dx.doi.org/10.3109/02688699209002895
Published online: 06 Jul 2009.
Submit your article to this journal
Article views: 10
View related articles
Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ibjn20 Download by: [University of California, San Diego]
Date: 15 April 2016, At: 23:26
British Journal of Neurosurgery (1992) 6 , 5-12
ORIGINAL ARTICLE
Downloaded by [University of California, San Diego] at 23:26 15 April 2016
Spinal arteriovenous malformations and subarachnoid haemorrhage REGINALD H. SHEPHARD
Trent Regional Department of Neurosurgery, Queen3 University Hospital, Nottingham, UK
Abstract Seventy patients with spinal arteriovenous malformations (AVMs) referred to the author over a 25-year period (1958-82), were equally divided between congenital, intradural and acquired, dural lesions. Amongst the intradural AVMs, were 22 with subarachnoid haemorrhage (SAH), a presenting feature in 18. The clinical findings in these 22 patients are tabulated, the radiological and operative findings indicated, and an account given of the overall outcome. Early operation is recommended, with a good prognosis and pevention of further haemorrhage in most cases. An extended follow-up has been maintained. The influence of menstruation, pregnancy and the puerperium on AVM symptoms is described.
Key words: Spinal arteriovenous malformation, subarachnoid haemorrhage, pregnancy.
‘le coup de poignard’ of Michon; by cervical, brachial or sciatic radicular pains and a painful stiff neck. Cerebral symptoms occur with severe bleeds and cervical lesions. Opisthotonus and coma may supervene, and clinically, it may not be possible to differentiate spinal from cranial SAH.
Introduction Intraspinal arteriovenous malformations (AVMs) are now classified into two main types: those in the intradural space (congenital) and those of the dura (acquired). Rosenblum et d . , l in a report on 81 cases, made this distinction: of 54 intradural lesions, 28 presented with subarachnoid haemorrhage (SAH). The differences between the two types of AVM are listed in Table I. Subarachnoid haemorrhage from other conditions is not considered here and this paper does not concern dural, acquired AVMs. The description of these is included in other papers.*-’ Intradural AVMs presenting in other ways will be the subject of another paper.
Incidence Spinal SAH, described by Wyburn-Mason? Henson and Croft,l0 and as a distinct clinical entity by Fincher,” is rare compared with cranial SAH. In Walton’s review12 of 312 patients with SAH, the origin was spinal in only three, only one of whom had an AVM. There are few early reports of significant numbers of cases of SAH from spinal AVMs. In a number of papers4*8-10J2-33 from 1900 to 1979, of 227 patients with AVMs, only 47 had
Onset Spinal SAH usually declares itself with dramatic suddenness: by extremely severe back pain, 5
6
Reginald H. Shephard TABLE I. Comparison of patients with intradural and dural AVMs
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Age: mean (years) Sex: M / F History: mean (years) SAH: incidence Other features Segmental cutaneous haemangioma Expanded spinal canal Asymmetrical limb growth Other lesions (cerebral angioma and spinal haemangioblastoma)
proven SAH. In these 47, the sex was recorded in 27 (15 males, 12 females), age in 28 (mean of 28 years), and outcome in 23. Eight patients died and in only four was there a good result. Only two were followed up, each for 2 years. Since 1979, larger series have been described, including series of 1834 (now part of this series), 28l (52% SAH), and 233s (36% SAH) patients. The present study confirms the high incidence of SAH (63%) in spinal intradural AVMs. Patients with SAH were much younger than those with the dural lesion (Table 1). There was a preponderance of females with spinal SAH and AVM in this series (Table I). This has not been reported previously, a higher incidence in men having been recorded in most series. For example, Rosenblum et al. in their cases] stated that 70% of subdural AVMs were in males, although a separate analysis of the SAH cases was not done. However, as dural AVMs are much more common in males (85% in Rosenblum et al. and 80% in this series), there is a ‘loading factor’ in favour of males when the two main types of AVM are not differentiated.
Duration of history In the 47 cases up to 1979, the duration of history (mean of 25 cases) was 4.5 years, compared with 8.5 years in this series (and 2 years for the dural AVMs).
Intradural AVM
Dural AVM
28
54
16/19 7.5
2817 2
(with SAH) 8.5 22 (of 35)
None (of 35)
3 (all with SAH) 9 (4 with SAH) 5 (4 with SAH)
2 (both with SAH)
Clinical material in this series Of 70 patients with intraspinal AV 4s referred in 25 years, 35 had subdural lesions and 22 of these sustained SAH. Table I1 summarizes the principal clinical features. Additional features are referred to in the text and brief notes made on five further cases. Of the 22 cases who sustained SAH, myelography was performed in 21 and angiography in 19. In three early cases, classification, based on the criteria of Rosenblum et al.’ is retrospective. The AVMs were in the cervical region in four patients, upper dorsal in four, mid- or low-dorsal in seven, dorsi-lumbar in six and in the whole canal in one.
Case reports Case 8
A 27-year-old woman presented with right hemiplegia. She had sustained four SAHs at 13, 17, 19 and 27 years of age, the second with coma and right hemiplegia which failed to recover completely. AVM at C1 was diagnosed. X-ray therapy proved ineffective. Hemiparesis did not change with the third and fourth haemorrhages. Epilepsy was present for 3 years prior to admission. Angiogram confirmed C1/2 AVM (Figs 1 and 2). Following total excision, normal life was resumed including an uneventful pregnancy. The patient was followed up for 18 years.
F M F M F F F F F M F M F M M M M F F F F F
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
13 20 28 38 44 17 20 27 30 24 36 35 13 28 54 17 25 4 37 23 20 41
Age (years)
2Y 14 Y 8 Y 2Y 22 Y 29 Y 4Y 24 Y Months 2 wks 24 Y 48 h 2 wks Days Weeks 9Y
lY
8 Y 10 Y 12 Y 20 Y 41 Y
History 2 3 3 1 1 1 2 4 1 1 3 1 2 4 1 1 1 2 1 2 1 1
A. p’plegia A. p’plegia A. p’plegia A. p’paresis B-Sec. Synd B-Sec. Synd A. p’paresis R. h’paresis A. p’plegia Pain:Retn Q’paresis C. p’plegia A. p’plegia S. loss right arm S. level T6 Coma, p’paresis R. h’paresis Coma, q’paresis A. p’paresis Minimal A. p’paresis Weak left leg
No. of Symptom(s) at SAHs presentation
MSSp MSSp M
M
S S
MSSp MSSp MSSp MSSp MS MS MS M MSSp SSP MS MSSp MSSp
Deficit
5 N
N N N 3 Died N N 3 N
1
5
1
5 1 5 N
4 N N
N N
5 4 1 1 2 1 5 4 4 5 4 N 2 N 3 5 3 N
N
5
Post-op.
5
Pre-op.
Gait
3 2 2 3 N N 1 N 3 2 N 3 2 N 2 N N 3 1 1 2 N 6 5 2 2
N 3 N
-
N
11 10 4 7 13 8 8 12
-
27 23 18 12 16 21 15 18
Follow-up (years)
-
N
N
1 3 N N N N 3 1 N 3 N N N
2 N
Post-op.
Sphincter Pre-op.
Results (grade)
A, acute; p’plegia, paraplegia; B-Sec. Synd, Brown-Sequard Syndrome; R. h’paresis, right hemiparesis; Retn, retention of urine; Qparesis, quadriparesis; C, chronic; p’pparesis, paraparesis; Mymotor; S, sensory, Sp, sphincter. Functional grading of gait and bladder sphincter ( L o p e et d s ) : Bladder Gait N. Normal N. Normal 1. Mild hesitancy, urgency, frequency 1. Onset leg weakness 2. Restricted activity 2. Moderate: occasional incontinence, or retention 3. Severe: total incontinence, persistent retention 3. Support for walking 4. Crutches or 2 sticks 5. Unable to stand, confined to bed or wheelchair
Sex
Case no.
TABLE 11. List of the 22 patients with SAH
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Reginald H. Shephard earlier. Investigation at that time had shown expansion of the canal (at T 1 lJ2,Ll). Laminectomy with a provisional diagnosis of tumour revealed a yellow-stained AVM with arachnoditis. One year before the present admission the patient had had a weak leg and precipitancy of micturition (worse 2 days before a period). Angiography showed abnormal vessels at T12,Ll. At operation, a thrombosed aneurysmal varix (2.0 x 1.0 x 1.0 cm) was revealed, consisting of an old laminated clot and thick pigmented collagenous walls, and incorporating angiomatous vessels. After excision the patient’s symptoms subsided (Fig. 3).
Multiple haemorrhages As with cranial AVMs, the spinal lesions may result in several bleeds; a mean of 2 in 35 of the 47 earlier reported cases (in the series of Rosenblum et al.’ and also in this series). Recurrent haemorrhage is the most common FIG. 1. Case 8. AVM at C1/2 level vertebral angiography. cause of death.9J2*1s*L6 In this series, 10 patients had multiple haemorrhages (Table 11) with severe later bleeds in cases 1, 2 and 18 (see Results). Case 14 A 28-year-old man presented with sensory loss in the right arm. He had sustained his first SAH at the age of 4 years. Spinal AVM was diagnosed by myelography and limited laminectomy. Three further SAHs occurred at yearly intervals, at 26, 27 and 28 years of age, each after sexual intercourse, with collapse after the last incident. On examination right segmental (T4,5) cutaneous angioma (Fig. 4) papilloedema was found. Investigation of the expanded spinal canal by myelography, subclavian and selective spinal angiography showed a large upper dorsal AVM with multiple feeders. At C7-T5 laminectomy “a fearsome looking AVM with arachnoiditis” was seen. After excision of the AVM, the patient made a good recovery and was able to lead a normal life.
Case 22 A 41-year-old woman presented with a weak left leg. Left sciatica had occurred 8 years
SAH from AVM in pregnancy, puerperium and menstruation As with cranial AVMsP6 symptoms of spinal intradural AVM may be associated with the above conditions, but SAH has been rarely reported and was not described in DelmasMarsalet;’ N e ~ m a nand ~ ~ Newquist and Ma~field:~or in the three cases in Rosenblum et al.’ The cases described below are from the present series.
Pregnancy Case 3. A 28-year-old woman presented with acute paraplegia. She had complained of weak legs at the ages of 16, 18 and 21 (first pregnancy). The weakness was transient and recovery complete. Leg weakness recurred at age 24 during the second pregnancy, with incomplete recovery. The first SAH with paraparesis occurred during the third preg-
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Spinal arteriovenous malformations
FIG.2. Case 8. AVM at C1/2 level: operative photograph.
9
FIG. 3. Case 14. Segmental naevus on right side of trunk.
FIG.4. Case 22. (a) and (b) Operative appearances after excision.
10
Reginald H. Shephard
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nancy. Caesarean section and sterilization were then performed. At age 28, a second SAH occurred with paraplegia. Partial removal of an AVM filling the whole canal was performed.
Case 5. A 44-year-old woman presented with Brown-Sequard Syndrome. At age 18 a weak right leg persisted and increased transiently with the first two of four pregnancies. SAHs occurred at ages 41 and 44, the first with transient coma and persisting pain and themal sense loss in the left leg. Puerperium Case 9. A 30-year-old woman presented with acute paraplegia. At age 22, she became transiently paraplegic 3 months after the birth of her first baby. When aged 30 and 3 months, after the birth of her fourth baby, she had an SAH with flaccid paraplegia, which persisted after removal of an AVM of the conus medullaris. Menstruation Aggravation of spinal AVM symptoms has been reported p r e v i o ~ s l y . ~Case ~ . ~3~ in Kunc and B r e P had six SAHs in 7 years, “bleeding predominantly during menstruation”. Neither of the two women in Martin et aL40 had SAH but other symptoms were worse during menstruation. In case 22 in this series, symptoms were worse for 2 days before each period, and in case 3, 18 months after operation the paraparesis worsened with a monthly periodicity, reverting to the less severe state after giving ovarian hormone.
Treatment The only effective treatment is by operative removal of the AVM in whole or in part,22,25,26,41 or interruption of its blood supply by operation or artificial embolizat i ~ n . ~ Treatment ’-~~ by decompression or Xirradiation is largely i n e f f e c t i ~ e . ’ ~In . ~ ~this series, operations were performed on all patients: three in case 20, two in cases l, 6 and 13
and one in the remaining cases. Total removal was achieved in 11,partial in six and occlusion of feeders in four.
Results Pre- and post-operative grading of motor and sphincter function is shown in Table 11. One patient (case 18) with a combined AVM of the cord and medulla oblongata had a fatal peroperative haemorrhage. Ignoring advice, three women became pregnant after incomplete excision of AVMs, with worsening paraparesis in one (case 13), and a second SAH in one (case 20). The third (case 6) became pregnant a year after operation, declined to have a Caesarean section but nevertheless did well, and remains so in the 23rd year of follow-up (as is her son). She did, however, heed advice not to have more children. Pregnancies in two women after complete removals were uneventful. Follow-up was maintained in all survivors except case 9. The condition at the end of follow-up was worse in three patients, unchanged in two, and improved in 15. Thirteen were leading normal lives, some with slight residual signs. Five had recurrent symptoms1Jv13.16.21 at 6, 10, 5, 7, and 2 years after operation. The gait grade (Table 11) changed to 4 (case l), 3 (case 3) and 4 (case 13). Cases 16 and 21 had recurrent SAHs; the former recovered without operation and the latter had an operation elsewhere.
Discussion The present series has shown a high incidence in the y0ung,3~.~O a female preponderance and, in most patients, a long history (Table I). The tendency towards multiple haemorrhages and increasing disability with later incidents is apparent. There is a clear relation between pregnancy, etc. and symptoms of AVM (including SAH). Such may be due to variations in circulating oestrogen and progesterone with change in the size of the AVM or in the blood flow through it relative to the cord circ~lation.~~~~~
Spinal arteriovenous malformations
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Conclusions The operative management of the patients in this series of spinal SAH from intradural AVMs has improved their prognosis. They have been largely protected from recurrent bleeding and so of any risk to life. There have been four recurrent haemorrhages during follow-up of 20 patients for a mean of 10 years, compared with 31 bleeds in the same 20 patients during the pre-operative 10 years. Cases 1, 3, 13 and 16 with recurrent symptoms between 5 and 10 years after operation indicate a need for reasonable periods of follow-up. Shorter periods might have led to the assumption of a more favourable prognosis than in fact proved to be the case. In the absence of follow-up studies, evaluation of the later results of previous reported cases of AVM with haemorrhage has not been possible. From the relation between pregnancy and menstruation and symptoms of intradural AVMs, the importance of investigating spinal neurological symptoms in young women is clear, as is appropriate advice concerning the risks of pregnancy in the presence of an AVM.
Acknowledgements The author wishes to thank the neurologists and neurosurgeons who referred their patients and Dr Roger Whitaker for his skill in performing most of the myelographic and angiographic examinations. Thanks are also due to the staff of the Department of Medical Illustration, Derby Royal Infirmary for photographic assistance and to Dr Jatin Vaidya for his encouragement to write this paper.
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