Brain (1974) 97, 211-218

THE PROGNOSIS OF PATIENTS WITH SPINAL VASCULARMALFORMATIONS

BY

M. J. AMINOFF AND VALENTINE LOGUE{From the National Hospital for Nervous Diseases, Maida Vale Hospital, London W9, and

the Institute of Neurology, Queen Square, London WC1)

THE natural history of spinal vascular malformations has not been studied indetail, nor has the prognosis for severe disablement or premature death beenestablished. Without this information, the need for surgical treatment mustremain speculative. It was to determine these points that the present study wasundertaken.

PATIENTS AND METHODS

The 60 patients reported in our previous paper (Aminoff and Logue, 1974) have been used.Many had continued to return for regular follow-up here or at their local hospital after thediagnosis had been established. In other cases, inquiry was made of their general practitioner or topatients themselves. In those patients who had died, efforts were made to get details of theirterminal illness and, when available, the autopsy report.

In some instances, laminectomy had been performed to confirm the diagnosis or to try to"decompress" the spinal cord. There was no benefit from such procedures, and this accords withthe experience of others (Arseni and Samitca, 1959; Newman, 1959; Krayenbuhl, Yasargil andMcClintock, 1969; Ommaya, Di Chiro and Doppman, 1969; Beraud, 1972). We have, therefore,included data derived from the subsequent progress of these patients in our analysis of the naturalhistory of the disorder. Some of them had other corrective operations such as excision of themalformation or ligation of its feeding arteries; in these cases the subsequent clinical course hasnot been included in the data we have analysed.

In making this study, we have assumed for practical purposes that the degree of disability providesa useful index of the course of the disease, so we have assessed the degree of disability in ourpatients on two or more occasions. Disturbances of gait were common, due to weakness and/orloss of balance. We have graded these as (1) onset of leg weakness, abnormal stance or gait, withoutrestriction of locomotory activity; (2) restricted exercise tolerance; (3) requires one stick or somesupport for walking; (4) requires crutches or 2 sticks for walking; (5) unable to stand, confined tobed or wheelchair. Disturbances of micturition have been classified as mild—hesitancy, urgency orfrequency; moderate—occasional urinary incontinence or retention; severe—total urinaryincontinence or persistent retention. Disordered control of defalcation has been similarlyclassified as mild—constipation; moderate—occasional fecal incontinence or severe intractableconstipation; severe—fascal incontinence.

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212 M. J. AMINOFF AND V. LOGUE

RESULTS

The mean duration of the history in our 60 patients was eight years to the time ofthe study, surgical treatment, death or loss of contact with the patient.

GaitIn patients with a progressive history, the mean interval between the first symptom

of any sort and the greatest, persistent gait disorder was 5-7 years.

In several instances, however, vague pain in the back or legs was present for several years beforethe development of symptoms more definitely attributable to the presence of a spinal angioma;this has led to some lengthening of our mean interval, so we have preferred to relate progression ofdisability to the onset of leg weakness or disturbed gait, whichever was earlier, since this was usuallyrecalled with certainty and can more justifiably be attributed to the spinal angioma.

The greatest, persistent disorder of gait which was known to have developed withinsix months and three years of the onset of disability is indicated in fig. 1, A and B,while the greatest disability during the period of follow-up is shown in fig. lc. It canbe seen that at six months, 56 per cent of patients had no restriction of activity, butby three years this had occurred in all but 9 per cent. Again, 19 per cent of ourpatients were severely disabled (Grades 4 or 5 as denned above) within six monthsand this had risen to 50 per cent by three years (Table 1).

6050

o/o 40Cases 30

20100

I I3 4 5 1 2 3 4 5Grade of Disability

Fio. 1.—Severity of gait disorder, A, Six months after its onset; B, At or within three years of itsonset; c, Within the period of follow-up.

TABLE I.—DISTURBANCE OF WALKING IN RELATION TO AGE

No. of patientsDisabilityGrade 1Grade 2Grade 3Grade 4Grade S

Total

No. of observations

Total No.of patients

60Per cent cases

At At or within6 months

562046

3 years9

212013

Patients youngerthan 41 years

Per cent casesAt At or within

6 months 3 years28-5 —28-5 28-5— 14

Patients aged41-60 years

Per cent casesAt At or within At

6 months 3 years 6 months9 60

21 2021 —9 20

Patients olderthan 61 years

16Per cent cases

60207

At or within3 years

12191925

13

99

37

100

43

100

57

99-5

13

100

40

100

—

100

25

100

52«t 56* 30t 33 15t 16

T h e number of observations is less than the number of patients because there was no deficit in 2 patients and in 2 other patientsdisturbed gait was only transient.

tThe number of observations is less than number of patients because in some instances it was not possible to classify the disabilityof patients within the time indicated.

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THE PROGNOSIS OF PATIENTS WITH SPINAL VASCULAR MALFORMATIONS 213

These results might be taken to relate solely to the duration of follow-up, butfurther examination of our data showed that this was not the case. Thus 33 of ourpatients eventually became seriously disabled (Grades 4 or 5) during the course offollow-up and of these 15 (45 per cent) had developed their greatest disability withinone year of the onset of weakness, as had 50 per cent of patients remaining mildlydisabled (Grades 2 or 3). Disability reached its greatest after a mean interval of twoand a half years in those with mild (Grades 2 or 3) ultimate incapacity and threeand a quarter years in the more severely disabled (Grades 4 or 5) patients. The dataseem to indicate not only the progression of disability with time, but also that suchprogression is of variable extent. It is often rapid, so that disability reached itsmaximum within one year in about half of our cases. The following case is exemplary.

Case 1.—(NH 83069), aged 59, gave a six-month history of urgency and frequency of micturition,and of increasing difficulty in walking, so that she was confined to bed for two weeks befoieadmission. There had also been paraesthesije in both legs for two months. Examination showed acomplete paresis of both legs, with absent tendon reflexes and bilateral extensor plantar responses.There was loss of vibration and joint position sense in both legs. Myelography suggested thepresence of an angioma in the lower dorsal region and this was confirmed at laminectomy. She diedin hospital three months later.

A contrast is provided by the next case.

Case 2.—(MVH 267785), aged 61, was admitted with a twenty-year history of weakness andstiffness in the right leg which had slowly and progressively worsened until he was able to walk onlyfifty yards, with the aid of sticks. There had been increasing numbness of the right leg for twoyears and of the left for four months. Examination showed signs of a combined upper and lowermotor neuron lesion in the legs, accompanied by some sensory loss. Myelographic appearancessuggested the presence of an angioma which was confirmed at operation.

In the clinical course described as characteristic by Wyburn-Mason (1943) thesymptoms were discontinuous and progressed by a series of "apoplectiform" stageswith intervening periods of partial or complete remission. The clinical course ofthe disorder did not have this "typical" pattern in any of our 60 patients (Aminoffand Logue, 1974) although in several patients there was some fluctuation ofsymptoms against a background of steadily increasing disability.

In our series, presenting symptoms were of acute onset in 12 patients (20 percent), in 5 of whom they then worsened progressively. In the other 7 patients,neurological disability developed acutely, but had not further progressed at the timeof diagnosis (Aminoff and Logue, 1974). These 7 patients have now been followedfor a mean of ten years (range four to seventeen years) from that time. One of thesepatients has had no weakness or disturbance of gait in the seventeen years that shehas been under supervision. Two patients presented with an acute paraparesis fromwhich they made an excellent recovery; they have since led an unrestricted life for fiveand eight years respectively, although the latter has had a brief episode of transientdysaesthesia during this time. Two other patients who presented with an acuteparaparesis have remained severely disabled, confined to a wheelchair for four andsix years. The remaining 2 patients whose disability developed acutely have shown

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214 M. J. AM1N0FF AND V. LOGUE

little change over the subsequent thirteen and sixteen years, and each is able to getabout with the help of a walking stick. None of these 7 patients has had any otheracutely disabling neurological disturbance over the period of follow-up.

Influence of sex.—There were 12 female and 48 male patients in our series. Of thefemale patients, 3 (25 per cent) presented with an acute, non-progressive neurologicalincident compared with 4 (8 per cent) of the male patients.

There were 9 women with a persisting disturbance of gait, in 8 of whom it evolvedgradually, while in the other it developed acutely. Of these 9 patients, 4 (44 per cent)were severely disabled within six months and 6 (66 per cent) within three years. Thecorresponding figures for the male patients were 7 per cent and 32 per cent respectively.This therefore suggests that female patients with spinal angioma fare less well thanmales.

Age.—Comparison of the general outcome in terms of functional disabilityrevealed no significant difference between our group of 33 patients aged 41 to 60years and our group of 16 patients older than 61 years at the time of diagnosis; 48per cent of the former and 50 per cent of the latter were severely disabled (Grades4 or 5) within three yeais, but the degree of incapacity was greater among theyounger age group (Table I).

Eleven patients were less than 41 years old at the time of diagnosis. An acute,non-progressive neurological disturbance was the presenting incident in 4 (36 per cent)of these patients and in only 5 (10 per cent) of the 49 older patients in this series.There were 7 patients in this age-group who developed a permanent disturbance ofgait and of these 3 (43 per cent) were confined to bed or wheelchair within six monthsand 4 (57 per cent) within three years (Table I). This is a much higher incidencethan in the series as a whole, and may well relate to the more equal sex distributionin this group (Aminoff and Logue, 1974) in contrast to the male preponderance inolder age groups.

Myelographic location of malformation.—In the great majority of our patients,myelography indicated that the malformation was located at the lower dorsal levelof the vertebral column, at least in part. In only 6 of our patients was the myelographicabnormality restricted to higher levels and in only 4 patients to lower levels (Aminoffand Logue, 1974). In view of these small numbers and the difficulties inherent in theinterpretation of myelographic results, we have not attempted to determine themanner in which the apparent location of the malformation influences the naturalhistory.

Angiography.—In 12 of our patients, the spinal angioma was outlinedangiographically. We were unable to correlate the natural history and prognosis ofthe disorder with any specific features revealed at angiography.

Intermittent claudication.—Recurrent symptoms clearly related to exercise, andrelieved by rest, occurred in 19 of our patients (Aminoff and Logue, 1974). The

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THE PROGNOSIS OF PATIENTS WITH SPINAL VASCULAR MALFORMATIONS 215

development of claudicatory symptoms was not related to age. Thus, only 6 of the19 patients were in the oldest of our three age groups. In no case did the claudicatorysymptoms presage an acute neurological incident of any sort nor the permanentenhancement of pre-existing symptoms. They occurred usually during the course of aprogressively increasing disability and in no way influenced the outcome.

Blood pressure.—Most of our patients were over 40 years of age at the time ofdiagnosis. This suggested that the development of symptoms might relate to thelevel of blood pressure. Only one patient, however, had a casual diastolic bloodpressure higher than 110 mmHg at the time of diagnosis although 3 patients gave apast history of hypertension. The casual blood pressure did not, therefore, seem toinfluence the natural history of the disorder.

Subarachnoid HaemorrhageThis occurred in 6 (10 per cent) of our patients, in 3 as an initial manifestation,

and in another as the terminal event. Recurrent haemorrhage occurred in only oneof these cases.

Disturbances of MicturitionAs described in our earlier paper, disturbances of micturition were common, but

with no clear pattern of development.

In 56 patients with such symptoms, disability was mild in 18 (32 per cent), moderatein 12 (21 per cent) and severe in 26 (47 per cent). In 64 per cent of our patients,symptoms did not become progressively more disabling within the time limits of ourinvestigation. Of the patients with moderately or severely disabling sysmptoms,however, approximately half had initially developed symptoms of lesser severity.When symptoms became progressively more disabling, they usually did so rapidly(Table II).

TABLE II.—DEVELOPMENT OF SEVERE DISTURBANCE OF MICTURITION

Non-progressiveSymptoms severely disabling from their onset 12

ProgressiveSymptoms severely disabling within 1 year or onset 6

1-2 years after onset 42-3 years after onset 13-4 years after onset 14-5 years after onset 0more than 5 years after onset 2

26"Severe" is taken to imply total urinary incontinence or persistentretention, as defined in the text. "Onset*' is taken as the initial disturbanceof micturition.

Disturbances of DefcecationThere were 42 patients who developed such symptoms during the period of the

study, and these were mild in 19 (45 per cent), moderate in 15 (36 per cent), andsevere in 8 (19 per cent).

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216 M. J. AMINOFF AND V. LOGUE

Of the 8 patients with severely disabling symptoms, these arose de novo in 5 cases,and in the other 3 after constipation had been troublesome for several years. Allpatients with disturbances of defecation had also a disturbance of micturition,although such symptoms did not necessarily develop at the same time. Moreoverthe development of these symptoms bore no constant temporal relationship to thedevelopment of disability in walking.

In general, the greater the degree of somatic disability, the greater was thelikelihood of an accompanying disturbance in the control of micturition anddefffication.

DeathOf our patients, 20 are known to have died, but in 7 cases the cause of death is

unknown and in another 3 cases it was unrelated to the spinal vascular pathology. Ofthe remainder, 9 patients died from complications of chronic paraplegia—uremia in7 cases, bronchopneumonia in one and pulmonary embolus in one—and onepatient from a spinal subarachnoid haemorrhage.

DISCUSSION

For this investigation we considered various scoring systems for rating neurologicalsigns and their progression, but the relationship of individual neurological signs tothe degree of disability is often indirect and tenuous. A patient's total disabilityis not represented by the sum of his individual physical signs: an extensor plantarresponse may be of considerable clinical significance, but in itself neither indicatesthe extent of, nor necessarily relates to, any functional disability. Furthermore thedirect comparison of patients in useful terms is not accomplished by comparingthe sum of their individual neurological signs. We therefore decided against theapplication of scoring methods such as those of Alexander (1951) and Kurtzke (1961)which have failed to obtain acceptance by most neurologists because of theircomplexity. Instead, we have used a classification based upon loss of function,which has the merit of immediate clinical relevance, but neglects symptoms such aspain or paraesthesiae. The comparison of such symptoms in different patients, or inindividual patients at different times, is hazardous, because their subjective natureprecludes a uniform manner of assessment.

It is evident from our study that once leg weakness or disturbance of gait hasdeveloped, it often progresses with great rapidity until the patient is severelydisabled. Fortunately, the risks of premature death—previously a common sequelto chronic paraplegia—have been much reduced by recent advances in the long-termcare of these patients.

Within three years of the onset of functional impairment in the legs, 50 per centof our patients were severely disabled (Grades 4 or 5). Severe incapacity occurredmore commonly among female or young patients, but we were unable to identify anyspecific prognostic indicators.

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THE PROGNOSIS OF PATIENTS WITH SPINAL VASCULAR MALFORMATIONS 2 1 7

It is well known that patients with spinal vascular malformations may remainasymptomatic for many years. However, in 20 per cent of our patients, presentingsymptoms, disabling in themselves, were of acute onset and in a further 8 per centa severe, acute, neurological incident occurred during the course of the disorder.Similarly, Gross and Ralston (1959) reported that in 3 of their 10 patients with spinalvascular malformations, initial symptoms were disabling and of sudden onset.Furthermore, in the series of Newman (1959), 11 out of 19 patients were completelyunable to walk within periods ranging from six months to four years after firstnoticing leg weakness. As in our experience, the rate of deterioration was usuallysteadily progressive, with significant remission occurring in only one case.

These observations make it difficult to adopt any suggestion of therapeuticcomplacency in the management of patients with spinal vascular malformations.They justify the need for surgical aid to improve the long-term prognosis. In ourexperience, excision of the fistula will usually halt the progressive deterioration ofpatients and in some instances leads to clinical improvement. There is a small risk,however, that surgery will itself produce a significant and permanent deterioration.Detailed analysis of our surgical results will be published separately.

The 19 per cent of cases who will be severely disabled (Grades 4 and 5) within sixmonths if untreated will have usually singled themselves out within one or twomonths of the onset of symptoms by their rapid progression. We propose that surgeryshould not be delayed in these patients as each passing month will worsen theeventual outcome. An additional 31 per cent of cases will, if untreated, becomeseverely disabled within three years (making a total of 50 per cent of cases sodisabled by this time); these patients may be safely watched for several monthsproviding that the pattern has not already become clear by the rate of progression,but again the benefit of surgery should be considered early. There remains a group ofpatients whose symptoms increase very slowly, if at all; surgery may not benecessary in this group unless the rate of progression increases or the cumulativedisability becomes restrictive, as in our Case 2. It must be remembered, however,that the untreated patient runs the risk of an acute deterioration or subarachnoidhaemorrhage, and this must be balanced against the surgical morbidity.

SUMMARY

A series of 60 patients with spinal vascular malformations was studied todetermine the prognosis in untreated cases. The mean duration of history was eightyears. Severe locomotor disability developed in 19 per cent of patients within sixmonths of the onset of any functional impairment in the legs and had developed in 50per cent within three years, when only 9 percent of patients were capable of unrestrictedwalking. Severe incapacity seemed to occur more commonly in female or youngpatients but we were unable to identify any other prognostic guides. Disturbancesof micturition or defalcation were frequent and often severely disabling, but bore no

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218 M. J. AMINOFF AND V. LOGUE

constant temporal relationship to the development of locomotor disability. In 12(20 per cent) of our cases, initial symptoms were of acute onset and in 5 they thenworsened progressively; the other 7 patients were followed up for a mean of ten yearsand no further disabling neurological incidents occurred. The implications of ourobservations, and their relevance to the management of patients with spinal vascularmalformations, are discussed.

ACKNOWLEDGMENTS

We thank the Physicians and Surgeons of the National Hospitals for Nervous Diseases, QueenSquare and Maida Vale, for allowing us to study the medical records of patients under their care.

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evaluation of therapeutic response. A.M.A. Archs Neurol. Psychiatry, 66, 253-271.AMINOFF, M. J., and LOGUE, V. (1974) Clinical features of spinal vascular malformations. Brain, 97,197 -210.ARSENI, C , and SAMITCA, D. C. (1959) Vascular malformations of the spinal cord. Ada psychiat. scand.,

34, 10-17.BERAUD, R. (1972) Vascular malformations of the spinal cord. In: "Handbook of Clinical Neurology."

Edited by P. J. Vinken and G. W. Bruyn. Amsterdam: North Holland, vol. 12, pp. 548-555.GROSS, S. W., and RALSTON, B. L. (1959) Vascular malformations of the spinal cord. Surgery Gynec.

Obstet., 108, 673-678.KRAYENBUHL, H., YASARGIL, M. G., and MCCLINTOCK, H. G. (1969) Treatment of spinal cord vascular

malformations by surgical excision. / . Neurosurg., 30, 427-435.KURTZKE, J. F. (1961) On the evaluation of disability in multiple sclerosis. Neurology, Minneap., 11,686-694.NEWMAN, M. J. D. (1959) Racemose angioma of the spinal cord. Q. Jl Med., 28, 97-108.OMMAYA, A. K.., D I CHIRO, G., and DOPPMAN, J. (1969) Ligation of arterial supply in the treatment of

spinal cord arteriovenous malformations. / . Neurosurg., 30, 679-692.WYBURN-MASON, R. (1943) "The Vascular Abnormalities and Tumours of the Spinal Cord and its

Membranes." London: Kimpton.

{Received July 19,1973)

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