- Email: [email protected]
Functional prognosis after treatment of spinal radiculomeningeal arteriovenous malformations
ELSEVIER
Spine: Vascular
FUNCTIONAL PROGNOSIS AFTER TREATMENT OF SPINAL RADICULOMENINGEAL ARTERIOVENOUS MALFORMATIONS Michihiro Kohno, M.D., Hiroshi Takahashi, M.D., Chifumi Kitanaka, M.D., Tomio Sasaki, M.D., and Buichi Ishijima, M.D. Department of Neurosurgery, Tokyo Metropolitan Neurological Hospital, and Department of Neurosurgery, University of Tokyo, Tokyo, Japan
Kohno M, Takahashi H, Kitanaka C, Sasaki T, Ishijima B. Functional prognosis after treatment of spinal radiculomeningeal arteriovenous malformations. Surg Neurol 1995;43:453-8. BACKGROUND
We performed surgical treatment successfully in six patients with spinal radiculomeningeal arteriovenous malformation (AVM); however, only four patients showed improvement of gait function postoperatively. METHODS
These experiences prompted us to review the clinical findings and their possible association with the functional outcome in 33 reported cases of radiculomeningeal AVM together with those in our six patients. RESULTS Statistical analysis revealed that the duration from onset of symptoms until diagnosis, the age at the time of treatment, the condition of the deep tendon reflexes (DTR) in the lower extremities, as well as the severity of both gait and urinary disturbance before treatment were significantly correlated with the functional outcome. CONCLUSIONS
A patient under 70 years old, who is treated within 2 years 6 months after the onset, whose gait or urinary disturbance is slight or moderate, and without absence of DTR in the lower extremities, is expected to have a good functional prognosis after treatment. KEY WORDS
Spinal radiculomeningeal arteriovenous malformations, embolization therapy, surgery, functional prognosis, spinal dural arteriooenous fistula.
S
pinal arteriovenous malformations (AVM) are rare [ 11, and the majority of them are radiculomeningeal AVM [8,9,11,14], which is also called
Address reprint requests to: Michihiro Kohno, M.D., Department of Neurosurgery, Tokyo Metropolitan Neurological Hospital, 2-6-l. Musashidai, Fuchu-city, Tokyo 183, Japan. Received February 1.5.1995; accepted January 4, 1995. 0 1995 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
spinal dural AVM [3,5,14] or spinal dural arteriovenous fistula (AVF) [ 11,131. We experienced six patients with spinal radiculomeningeal AVM and performed surgical treatment in all cases. Although interruption of the radiculomedullary vein and coagulation of the nidus were successfully performed, only four patients showed improvement of gait function postoperatively. These experiences prompted us to review the clinical findings and their possible association with the functional outcome in 33 reported cases of radiculomeningeal AVM together with those in our 6 patients. In this paper, we reveal the condition of the patient with radiculomeningeal AVM who can be expected to have a good functional prognosis, and we discuss the selection of treatment based on the functional prognosis.
SUMMARYOFOURSUBJECTS Our initial observations were made in six patients with spinal radiculomeningeal AVM, consisting of five men and one woman, ranging in age from 50 to 81 years (mean, 60.8 years) (Table 1). The age at the onset of symptoms ranged from 49 to 79 years (mean, 57.7 years), and the duration from onset to treatment varied from 5 months to 8 years 8 months (mean, 3 years 3 months). The initial symptoms had included abnormal sensation, muscle weakness, and sensory disturbance of the lower extremities. At the time of diagnosis, gait disturbance due to paraparesis, sensory disturbance of bilateral lower extremities without sacral sparing, urinary disturbance, and constipation were recognized in all patients. In all of these six patients, the radiculomedullary vein which drained the nidus was interrupted dur0090-3019/95/$9.50 SSDI 00903019(95)0005&C
454
II
Surg Neurol 1995;43:453-8
Kohno et al
Summarv of Clinical Findings in Our Six Patients
PATIENT No. AGE/%X 1
2 3 4 5 6
81/M 50/M 59/M 63/M 60/F 52/M
DURATION (ONSET/ TREATMENT) DTR 2Y6M 7M 4Y2M 8Y8M 5M 3Y
H AH A H/A H
NIDUS INITL~L (PFcEozLwIvE, @IDE/ !h'MpTOM SYMPTOMS LEvEL) SURGERY POSTOPERATIVE) AS S AS k AS
P,S,M,D,I P,S,M,D I’,S,M,D,I P,S,M,D,I P,S,M,D P,S,M,D,I
R-T11 L-L1 L-T10 R-T8 LLl R-T6
I
I IJ IJ I
I,C
G4M2-G2M1 G5M3-G2M3 C5M3-G5M3 G5M3-G5M3 G5M3-G4MO G2M3-GlM2
aFunctional grading according to Aminoff and Logue (Table 2). DTR (deep tendon reflexes in the lower extremities). H = hyperactive; A = absent. AS = abnormal sensation in the legs, S = sensory disturbance in the legs, P = paraparesis; M = disturbance of micturition, D = disturbance defecation; I = impotence. Nidus Side R = right; L = left. Level T = thoracic; L = lumbar. Surgery I = interruption of a drainer: E = excision of AVM/AVF on the dura mater, C = coagulation of AVM/AVF on the dura mater.
ing the operation. In three patients, resection or coagulation of the nidus or fistula on the dura mater was also performed. Following surgery, five patients showed improvement of preoperative neurologic deficits, of whom four patients who had been treated within 3 years after onset showed improvement of the gait function. Disturbance of micturition was recognized in all patients preoperatively, and only slight improvement in two patients and much improvement in one patient was shown postoperatively. In all of our cases, postoperative selective spinal angiography showed no filling of abnormally dilated coronal venous plexus. In our patients 3 and 4, the duration from onset until treatment was more than 4 years, and muscular atrophy and absence of deep tendon reflexes (DTR) in the lower extremities were recognized preoperatively; improvement of gait or urinary function was not observed postoperatively. These experiences prompted us to suspect that both the duration from onset until treatment and the DTR status are correlated with the functional outcome in patients with radiculomeningeal AVM.
MATERIALSANDMETHODS We reviewed the clinical findings in 39 cases of radiculomeningeal AVM, including 33 patients reported in the literature and our 6 patients, in order to elucidate whether there were any factors correlated with the functional outcome. The selected cases were restricted to those in which data regarding three or more factors of age, duration from onset until treatment, DTR in the lower extremities, gait function before and after treatment, urinary function before and after treatment, and type of
of
therapy (surgical treatment, embolization or both) were clearly described in the report (Table 2). Reported cases, which include complicating elements such as recurrence or multiple treatment, were excluded. We used the functional grading system of Aminoff and Logue [ 1 ] to evaluate the degree of disability of gait function and micturition (Table 3). The age, grades of gait and micturition disturbance before and after treatment, and the changes in gait and urinary functional status showed normal distribution (with normal probability plot: skewness < 1, kurtosis < 2). The logarithmic values of the duration from onset until treatment also showed normal distribution. Unpaired t test was applied for statistical evaluation, because the number of materials was comparatively small in spite of discontinuous data. Significance was accepted at the 95% probability level. In the analysis related to DTR, we excluded the data for case 38 (our patient 5), in whom the right patellar tendon reflex was exaggerated, while the other DTR in the lower extremities were absent preoperatively. In the comparison of the results of surgical treatment with those of embolization therapy, we excluded the data for two patients (cases 26 and 29) who had undergone both surgery and embolization, and those for case 20, for whom the functional state before and after surgery was not clearly described.
RESULTSOFSTATISTICAL ANALYSIS (1) The duration from onset until treatment was not significantly correlated with the grade of gait func-
Surg Neurol 455 1995;43:453-8
Prognosis of Radiculomeningeal AVM
Summary of Clinical Findings in 39 Patients with Radiculomeningeal AVM
DURATION CASE No.
AGE/ SEX
1.171 2.171
57 M 63 M 72 M 65 M 63 M 42 M 57 M
3. 171 4. (71 5. [71 6. [91 7. [91 8. [91 9. 191
Duration:
Logue
? ?
3
7
?
? ? ?
? 7
? ? H H A
H;A H (Table
R-T1 1 L-L1 L-T10 R-T8 L-L1 R-T6
s s S
S S E E E E E E S S S S S E E E S S S E E E E&S E E E&S S E E E
G3M?-C3M? G5M2-G5M2 G3M2-G?M2 G5M?-G4M? G5M3-G?M3 G5M3-G4MO G4M?-Gl MO G5M?-GOMO G5M?-G3M? G5M?-G4M? G2M?-GlM? GBMl-GlMO GOMO-GOMO G3M3-GlMO G5M3-G5M3 G2M3-G3Ml G2M?-G3M? G2M?-GlM? G5M?-G4M? G?M3-G4M? G5M?-G4M? G5M?-G5M? G4M3-GlM3 GlMl-GlMl G4M3-G4M3 G4M3-G4M3 G4M3-Gl M3 G5M3-G5M3 G5M l-G4M3 G3M2-GlMO G3Ml-G4Ml G5M2-G3M2 G3Ml-GlM2 G4M2-G2Ml G5M3-G2M3 G5M3-G5M3 G5M3-G5M3 G5M3-G4MO G2M3-GlM2
2).
F = female.
M = month;
(deep
Therapy
and
R-T3 L-T6 L-T1 1 L-T10 L-T9 R-HG Ab L-T6 R-T8 L-T12 L-L1 ? L-T5 R-T6,7 R-T9 R-L1 L-L3 R-T5 R-T8 R-Sl? R-T11 L-L2 L-L3 7
THERAPY
artery.
Sex: M = male;
Feeder
to Aminoff
FFEDER
(pREO:ikE, POSTOPERATIVE TREATMENT)
M = micturition.
“Hypogastric
DTR
?
2.5Y 7M 4Y 8.5 Y 5M 3Y
50 M 59 M 63 M 60 F 52 M according
A ? ? ? ? A ? ? ? ? ? H H H A ? ? ? ? A H H ? ?
? 4Y 2Y 3Y 2Y 7M 1Y 10M 5Y 3Y 7M 7Y 2Y 5M 3Y 1Y 1.5 Y 2Y 2Y 4Y 3Y 4Y 8Y 1Y 3Y 3Y 1.5Y 2.5 Y 1.5 Y 10 M 5Y 4M 1.5Y
81 M
Grading
G = gait:
DTR
TREATMENT)
71 F 58 M 72 F 44 M 56 M 29 M 56 M 74 M 60 M 63 M 51 M 68 M 81 M 54 F 56 M 67 F 68 M 70 M 58 M 60 M 70 M 54 F 72 M 62 M 54 M 71 F
10. [9] 11. [9] 12. [ll] 13. [ll] 14. [ll] 15. [ll] 16. [ll] 17. [5] 18. [5] 19. [5] 20. [8] 21. [6] 22. [6] 23. [lo] 24. [lo] 25. [lo] 26. [lo] 27. [lo] 28. [IO] 29. [IO] 30. [lo] 31. [lo] 32. [lo] 33. [lo] Present patients: 34. 1 35. 2 36. 3 37. 4 38. 5 39. 6 ‘Functional
(ONSET/
tendon
R = right;
Y = year.
reflexes
in the
lower
L = left; T = thoracic;
S = surgery;
extremities);
H = hyperactive:
A = absent.
L = lumbar.
E = embolization.
tion before treatment. However, the grade of gait function after treatment in the group of patients who had been treated within 2 years 6 months after onset was significantly better than that in those treated more than 2 years 6 months thereafter @ <
0.05). (2) The change of grade of gait function in the patients treated within 1 year after onset was significantly better than that in those treated more than 1 year after onset @ < 0.05), and that in the patients who were 570 years old at the time of
456
Surg Neurol 1995;43:453-8
El Functional Logue [l]
Grading According
Kohno et al
to Aminoff and
GAIT DISTURBANCE GO: normal Gl: onset of leg weakness, abnormal stance or gait, without restriction of locomotor activity G2: restricted activity, but not requiring support G3: requires one stick for walking G4: requires crutches, walker, or 2 sticks for walking G5: unable to stand, confined to bed or wheelchair
DISTURBANCE OF MICTURITION
MO: normal Ml: mild (hesitancy, urgency, or frequency, altered sensation but continent) M2: moderate (occasional urinary incontinence or retention) M3: severe (total urinary incontinence or persistent retention)
treatment was significantly better than that in those who were ~70 years old at the time of treatment @ < 0.05). (3) There was no correlation between the duration from onset until treatment and the grade of urinary function before treatment. However, the functional grade of micturition after treatment in the patients treated within 2 years after onset was significantly better than that in those treated more than 2 years after onset @ < 0.05). (4) The patients with slight or moderate disturbance of gait function before treatment (grades 0, 1, 2, or 3) showed significantly more marked improvement of gait function after treatment than those with severe disability (grades 4 or 5) @ < 0.001). The change after treatment in urinary function in the patients with slight or moderate disturbance of urinary function (grades 0, 1, and 2) was slightly better than that in those with severe disturbance (grade 3) @ = 0.056). (5) The gait function before and after treatment of the patients with hyperactive DTR was significantly better than patients in whom DTR in the lower extremities were absent @ < 0.05). (6) The patients in whom DTR in the lower extremities were absent showed significantly poorer urinary function before and after treatment than that in the patients with hyperactive DTR 0, < 0.05). (7) There were no correlations among the age, the duration from onset until treatment, and DTR status. (8) The functional grade of gait and urinary disturbances before and after treatment in the patients who underwent surgical treatments did not differ significantly from those in the patients who received embolization therapies.
DISCUSSION CLINICAL FACTORS CORRELATED WITH THE FUNCTIONAL PROGNOSIS Our investigation revealed that the major factors correlated with the functional prognosis are the duration from onset until treatment and the functional grades of gait and urinary disturbance before treatment, as well as the DTR status. However, no correlation was observed between the duration and DTR status, nor between the duration and the functional grade of either gait or urinary disturbance before treatment. Symon et al [14] described that in 46 surgically treated cases the frequency of patients with improvement in gait and urinary function after surgery was higher in the group of moderately disabled patients than in the group of severely disabled patients; they suggested that preoperative neurologic status was correlated with functional prognosis. But they did not refer to the degree of postoperative functional status nor changes of functional grade, and statistical approval was not performed. Rosenblum et al [13] and Oldfield and Doppman [ 121 stated that preoperative muscle strength and functional grade (by Aminoff and Logue [ 11) had a direct relationship to postoperative ones in 26 surgically treated patients, but statistical appraisal was not performed. Aminoff and Logue [l] referred to the relationship between the duration after onset and functional grade of gait in 60 patients with spinal vascular malformations, but it is unknown how many radiculomeningeal AVMs were included. Our study statistically confirmed that the duration from onset until treatment and the functional grades of gait and urinary disturbance before treatment are factors correlated with the functional prognosis. Moreover, we propose that the status of DTR in the lower extremities can be a convenient factor indicating functional prognosis, although absence of DTR in the lower extremities is considered to be a severely disabled condition. Symon et al reported that absent DTR in the lower extremities was recognized in 13 (23.6%) of their 55 patients with radiculomeningeal AVM [ 141. To summarize our study, the patient who can be expected to have a good prognosis in gait function is under 70 years old who is treated within 2 years 6 months after onset or whose gait function before treatment is grades 0, 1, 2 or 3. Although the possibility of improvement is much less than that of gait disturbance, the urinary disturbance in the patient who is treated within 2 years after onset can be expected to improve considerably. The patient
Surg Neurol 457 1995:43:453-g
Prognosis of Radiculomeningeal AVM
with absent DTR in the lower extremities cannot be expected to show marked improvement in either gait or urinary function after treatment, irrespective of the duration from onset until treatment. TREATMENTS The natural history of radiculomeningeal AVM is described to present gradual progression of symptoms, which are irreversible if not treated within 3 years [ 1,121. Hence, some treatment must be applied in order to counter or halt the developing neurologic deficits in patients with radiculomeningeal AVM. Concerning the treatments of radiculomeningeal AVM, it is controversial to select either surgery or embolization therapy [2-51. Recently, the risk of recanalization in embolization therapy has been repeatedly pointed out. Morgan and Marsh [lo] described that recanalization occurred in more than 11 of 18 embolization therapies in 14 patients with radiculomeningeal AVM, and they considered that current polyvinyl alcohol (WA, particulate material) could not expected to have a permanent effect. Hall et al [4] observed recurrent symptoms in two of three patients with radiculomeningeal AVM treated by embolization therapy with PVA, recommended surgery as a curative treatment, and also emphasized the necessity of follow-up angiography after embolization therapy. On the other hand, surgery for radiculomeningeal AVM is said to be permanently effective and involves comparatively easy and safe procedures [4,10,11,14]. The most common operation for radiculomeningeal AVM is interruption of the radiculomedullary vein continuing to the coronal venous plexus and electrocoagulation or resection of the nidus itself if visible [7,9,11,13,14]. Reported surgical results were generally good, but approximately 20%-30% patients show no change postoperatively [ 12,141. Our study reveals that the outcome of surgical treatment shows no marked difference from that of embolization therapy and in the selection of the treatment, the risk of recanalization and the degree of invasion should be considered. There are few reports regarding the operative indications in radiculomeningeal AVM based on the functional prognosis, but Symon et al described that patients diagnosed before the functional disturbance becomes severe are good candidates for operation [ 141. Contrarily, for patients who cannot be expected to have a good functional prognosis or for the poor operative risk patients, embolization therapy, which is less invasive although it carries the risk of recanal-
ization, is considered possible. If recanalization occurs, surgical treatment may be performed in patients who unexpectedly improve after embolization therapy. Finally, we emphasize that it is very important to diagnose this disease early based on the features of the clinical symptoms and magnetic resonance imaging in order to obtain a good functional outcome
tbl. The authors thank Dr. Chikuma Hamada for his valuable advice in statistical management.
REFERENCES 1. Aminoff MJ and Logue V. The prognosis of patients with spinal vascular malformations. Brain 1974;97: 211-8. 2. Cahan LD, Higashida RT, Halbach W, Hieshima GB. 3.
4.
5.
6.
7.
8.
9.
10.
11.
12. 13.
14.
Variants of radiculomeningeal vascular malformations of the spine. J Neurosurg 1987;66:333-7. Doppman JL, Di Chiro G, Dwyer AJ, Frank JL, Oldfield EH. Magnetic resonance imaging of spinal arteriovenous malformations. J Neurosurg 1987;66:830-4. Hall WA, Oldfield EH, Doppman JL. Recanalization of spinal arteriovenous malformations following embolization. J Neurosurg 1989;70:714-20. Hida K, lwasaki Y, Isu T, Akino M, Abe H, et al. Spinal dural AVM: Report of three cases. No Shinkei Geka 1986;14:361-6. (in Japanese) Isu T, Iwasaki Y, Akino M, Koyanagi I, Abe H. Magnetic resonance imaging in cases of spinal dural arteriovenous malformation. Neurosurgery 1989; 24:919-23. Kendall BE and Logue V. Spinal epidural angiomatous malformations draining into intrathecal veins. Neuroradiology 1977;13:181-9. Masaryk TM, Ross JS, Medic MT, Ruff RL, Warren RS, Ratcheson RA. Radiculomeningeal vascular malformations of the spine: MR imaging. Radiology 1987; 164:845-g. Merland JJ, Riche MC, Chiras J. Intraspinal extramedullary arteriovenous fistulae draining into the medullary veins. J Neuroradiol 1980;7:271-320. Morgan MK, Marsh WR. Management of spinal dural arteriovenous malformations. J Neurosurg 1989;70: 832-6. Oldfield EH, Di Chiro G, Quindlen EA, Rieth KG, Doppman JL. Successful treatment of a group of spinal cord arteriovenous malformations by interruption of dural fistula. J Neurosurg 1983;59:1019-30. Oldfield EH, Doppman JL. Spinal arteriovenous malformations. Clin Neurosurg 1988;34:161-83. Rosenblum B, Oldfield EH, Doppman JL, Di Chiro G. Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulas and intradural AVM’s in 81 patients. J Neurosurg 1987;67:795-802. Symon L, Kumaya H, Kendall B. Dural arteriovenous malformation of the spine. J Neurosurg 1984;60:23847.
458
Kohno et al
Surg Neurol 1995;43:453-8
COMMENTARY
This is an interesting article in which our Japanese colleagues have carefully analyzed the literature in relation to dural arteriovenous malformations of the spine and added six cases of their own. One cannot help but admire their industry in attempting to obtain numeric grading retrospectively from the widely differing reported series, but their opinions add weight to those widely held by surgeons who have dealt with this condition for some years. It is clear that the longer the venous stasis is present the less the risk of a satisfactory outcome, and the clear documentation of capillary neovascularization and necrosis in the spinal cord in cases who have died after dural AVM had been present for a number of years, a condition previously known as the Foix-Alajouanine syndrome indicates that venous hemostasis will result in the end in ischemic cord necrosis. No recovery is then possible. In the same way, it is a fairly accepted neurosurgical axiom that the older the patient the less likely satisfactory results are to be achieved, and our Japanese colleagues are to be complimented on documenting this fact so clearly.
wants a good prognosis. Most of it is surgical statistics. 1 would like the authors to be less negative about embolization. It is true that PVA particles are not the material that should be used, because there is almost always recanalization. However, an anatomic cure can be expected with isobutyl cyanoacrylate in a high number of cases. I think it is acceptable to treat these fistulae with acrylic glue and to reserve surgery for the contraindications or failures of endovascular procedures. Gerard Debrun, M.D.
Chicago, Illinois
London, England
In a 20-year personal experience, 1have operated on 76 cases but have not had to operate any in the past 4 years. All of my cases in this last period have been embolized by Dr. Alex Berenstein, with remarkably good results. In a personal communication with Dr. Gazi Yasargil, he mentioned that he had been able to stop operating on these lesions more than 8 years ago. Length and duration of neurologic symptoms and signs have long been recognized as contributing to a poor prognosis. This is almost universal for all neurologic disorders, however.
This is an interesting article that emphasizes the need to detect spinal dural fistulae early if one
Leonard I. Malis, M.D. New York, New York
Lindsay Symon, C.B.E., T.D., F.R.C.S.
Spine: Vascular
FUNCTIONAL PROGNOSIS AFTER TREATMENT OF SPINAL RADICULOMENINGEAL ARTERIOVENOUS MALFORMATIONS Michihiro Kohno, M.D., Hiroshi Takahashi, M.D., Chifumi Kitanaka, M.D., Tomio Sasaki, M.D., and Buichi Ishijima, M.D. Department of Neurosurgery, Tokyo Metropolitan Neurological Hospital, and Department of Neurosurgery, University of Tokyo, Tokyo, Japan
Kohno M, Takahashi H, Kitanaka C, Sasaki T, Ishijima B. Functional prognosis after treatment of spinal radiculomeningeal arteriovenous malformations. Surg Neurol 1995;43:453-8. BACKGROUND
We performed surgical treatment successfully in six patients with spinal radiculomeningeal arteriovenous malformation (AVM); however, only four patients showed improvement of gait function postoperatively. METHODS
These experiences prompted us to review the clinical findings and their possible association with the functional outcome in 33 reported cases of radiculomeningeal AVM together with those in our six patients. RESULTS Statistical analysis revealed that the duration from onset of symptoms until diagnosis, the age at the time of treatment, the condition of the deep tendon reflexes (DTR) in the lower extremities, as well as the severity of both gait and urinary disturbance before treatment were significantly correlated with the functional outcome. CONCLUSIONS
A patient under 70 years old, who is treated within 2 years 6 months after the onset, whose gait or urinary disturbance is slight or moderate, and without absence of DTR in the lower extremities, is expected to have a good functional prognosis after treatment. KEY WORDS
Spinal radiculomeningeal arteriovenous malformations, embolization therapy, surgery, functional prognosis, spinal dural arteriooenous fistula.
S
pinal arteriovenous malformations (AVM) are rare [ 11, and the majority of them are radiculomeningeal AVM [8,9,11,14], which is also called
Address reprint requests to: Michihiro Kohno, M.D., Department of Neurosurgery, Tokyo Metropolitan Neurological Hospital, 2-6-l. Musashidai, Fuchu-city, Tokyo 183, Japan. Received February 1.5.1995; accepted January 4, 1995. 0 1995 by Elsevier Science Inc. 655 Avenue of the Americas, New York, NY 10010
spinal dural AVM [3,5,14] or spinal dural arteriovenous fistula (AVF) [ 11,131. We experienced six patients with spinal radiculomeningeal AVM and performed surgical treatment in all cases. Although interruption of the radiculomedullary vein and coagulation of the nidus were successfully performed, only four patients showed improvement of gait function postoperatively. These experiences prompted us to review the clinical findings and their possible association with the functional outcome in 33 reported cases of radiculomeningeal AVM together with those in our 6 patients. In this paper, we reveal the condition of the patient with radiculomeningeal AVM who can be expected to have a good functional prognosis, and we discuss the selection of treatment based on the functional prognosis.
SUMMARYOFOURSUBJECTS Our initial observations were made in six patients with spinal radiculomeningeal AVM, consisting of five men and one woman, ranging in age from 50 to 81 years (mean, 60.8 years) (Table 1). The age at the onset of symptoms ranged from 49 to 79 years (mean, 57.7 years), and the duration from onset to treatment varied from 5 months to 8 years 8 months (mean, 3 years 3 months). The initial symptoms had included abnormal sensation, muscle weakness, and sensory disturbance of the lower extremities. At the time of diagnosis, gait disturbance due to paraparesis, sensory disturbance of bilateral lower extremities without sacral sparing, urinary disturbance, and constipation were recognized in all patients. In all of these six patients, the radiculomedullary vein which drained the nidus was interrupted dur0090-3019/95/$9.50 SSDI 00903019(95)0005&C
454
II
Surg Neurol 1995;43:453-8
Kohno et al
Summarv of Clinical Findings in Our Six Patients
PATIENT No. AGE/%X 1
2 3 4 5 6
81/M 50/M 59/M 63/M 60/F 52/M
DURATION (ONSET/ TREATMENT) DTR 2Y6M 7M 4Y2M 8Y8M 5M 3Y
H AH A H/A H
NIDUS INITL~L (PFcEozLwIvE, @IDE/ !h'MpTOM SYMPTOMS LEvEL) SURGERY POSTOPERATIVE) AS S AS k AS
P,S,M,D,I P,S,M,D I’,S,M,D,I P,S,M,D,I P,S,M,D P,S,M,D,I
R-T11 L-L1 L-T10 R-T8 LLl R-T6
I
I IJ IJ I
I,C
G4M2-G2M1 G5M3-G2M3 C5M3-G5M3 G5M3-G5M3 G5M3-G4MO G2M3-GlM2
aFunctional grading according to Aminoff and Logue (Table 2). DTR (deep tendon reflexes in the lower extremities). H = hyperactive; A = absent. AS = abnormal sensation in the legs, S = sensory disturbance in the legs, P = paraparesis; M = disturbance of micturition, D = disturbance defecation; I = impotence. Nidus Side R = right; L = left. Level T = thoracic; L = lumbar. Surgery I = interruption of a drainer: E = excision of AVM/AVF on the dura mater, C = coagulation of AVM/AVF on the dura mater.
ing the operation. In three patients, resection or coagulation of the nidus or fistula on the dura mater was also performed. Following surgery, five patients showed improvement of preoperative neurologic deficits, of whom four patients who had been treated within 3 years after onset showed improvement of the gait function. Disturbance of micturition was recognized in all patients preoperatively, and only slight improvement in two patients and much improvement in one patient was shown postoperatively. In all of our cases, postoperative selective spinal angiography showed no filling of abnormally dilated coronal venous plexus. In our patients 3 and 4, the duration from onset until treatment was more than 4 years, and muscular atrophy and absence of deep tendon reflexes (DTR) in the lower extremities were recognized preoperatively; improvement of gait or urinary function was not observed postoperatively. These experiences prompted us to suspect that both the duration from onset until treatment and the DTR status are correlated with the functional outcome in patients with radiculomeningeal AVM.
MATERIALSANDMETHODS We reviewed the clinical findings in 39 cases of radiculomeningeal AVM, including 33 patients reported in the literature and our 6 patients, in order to elucidate whether there were any factors correlated with the functional outcome. The selected cases were restricted to those in which data regarding three or more factors of age, duration from onset until treatment, DTR in the lower extremities, gait function before and after treatment, urinary function before and after treatment, and type of
of
therapy (surgical treatment, embolization or both) were clearly described in the report (Table 2). Reported cases, which include complicating elements such as recurrence or multiple treatment, were excluded. We used the functional grading system of Aminoff and Logue [ 1 ] to evaluate the degree of disability of gait function and micturition (Table 3). The age, grades of gait and micturition disturbance before and after treatment, and the changes in gait and urinary functional status showed normal distribution (with normal probability plot: skewness < 1, kurtosis < 2). The logarithmic values of the duration from onset until treatment also showed normal distribution. Unpaired t test was applied for statistical evaluation, because the number of materials was comparatively small in spite of discontinuous data. Significance was accepted at the 95% probability level. In the analysis related to DTR, we excluded the data for case 38 (our patient 5), in whom the right patellar tendon reflex was exaggerated, while the other DTR in the lower extremities were absent preoperatively. In the comparison of the results of surgical treatment with those of embolization therapy, we excluded the data for two patients (cases 26 and 29) who had undergone both surgery and embolization, and those for case 20, for whom the functional state before and after surgery was not clearly described.
RESULTSOFSTATISTICAL ANALYSIS (1) The duration from onset until treatment was not significantly correlated with the grade of gait func-
Surg Neurol 455 1995;43:453-8
Prognosis of Radiculomeningeal AVM
Summary of Clinical Findings in 39 Patients with Radiculomeningeal AVM
DURATION CASE No.
AGE/ SEX
1.171 2.171
57 M 63 M 72 M 65 M 63 M 42 M 57 M
3. 171 4. (71 5. [71 6. [91 7. [91 8. [91 9. 191
Duration:
Logue
? ?
3
7
?
? ? ?
? 7
? ? H H A
H;A H (Table
R-T1 1 L-L1 L-T10 R-T8 L-L1 R-T6
s s S
S S E E E E E E S S S S S E E E S S S E E E E&S E E E&S S E E E
G3M?-C3M? G5M2-G5M2 G3M2-G?M2 G5M?-G4M? G5M3-G?M3 G5M3-G4MO G4M?-Gl MO G5M?-GOMO G5M?-G3M? G5M?-G4M? G2M?-GlM? GBMl-GlMO GOMO-GOMO G3M3-GlMO G5M3-G5M3 G2M3-G3Ml G2M?-G3M? G2M?-GlM? G5M?-G4M? G?M3-G4M? G5M?-G4M? G5M?-G5M? G4M3-GlM3 GlMl-GlMl G4M3-G4M3 G4M3-G4M3 G4M3-Gl M3 G5M3-G5M3 G5M l-G4M3 G3M2-GlMO G3Ml-G4Ml G5M2-G3M2 G3Ml-GlM2 G4M2-G2Ml G5M3-G2M3 G5M3-G5M3 G5M3-G5M3 G5M3-G4MO G2M3-GlM2
2).
F = female.
M = month;
(deep
Therapy
and
R-T3 L-T6 L-T1 1 L-T10 L-T9 R-HG Ab L-T6 R-T8 L-T12 L-L1 ? L-T5 R-T6,7 R-T9 R-L1 L-L3 R-T5 R-T8 R-Sl? R-T11 L-L2 L-L3 7
THERAPY
artery.
Sex: M = male;
Feeder
to Aminoff
FFEDER
(pREO:ikE, POSTOPERATIVE TREATMENT)
M = micturition.
“Hypogastric
DTR
?
2.5Y 7M 4Y 8.5 Y 5M 3Y
50 M 59 M 63 M 60 F 52 M according
A ? ? ? ? A ? ? ? ? ? H H H A ? ? ? ? A H H ? ?
? 4Y 2Y 3Y 2Y 7M 1Y 10M 5Y 3Y 7M 7Y 2Y 5M 3Y 1Y 1.5 Y 2Y 2Y 4Y 3Y 4Y 8Y 1Y 3Y 3Y 1.5Y 2.5 Y 1.5 Y 10 M 5Y 4M 1.5Y
81 M
Grading
G = gait:
DTR
TREATMENT)
71 F 58 M 72 F 44 M 56 M 29 M 56 M 74 M 60 M 63 M 51 M 68 M 81 M 54 F 56 M 67 F 68 M 70 M 58 M 60 M 70 M 54 F 72 M 62 M 54 M 71 F
10. [9] 11. [9] 12. [ll] 13. [ll] 14. [ll] 15. [ll] 16. [ll] 17. [5] 18. [5] 19. [5] 20. [8] 21. [6] 22. [6] 23. [lo] 24. [lo] 25. [lo] 26. [lo] 27. [lo] 28. [IO] 29. [IO] 30. [lo] 31. [lo] 32. [lo] 33. [lo] Present patients: 34. 1 35. 2 36. 3 37. 4 38. 5 39. 6 ‘Functional
(ONSET/
tendon
R = right;
Y = year.
reflexes
in the
lower
L = left; T = thoracic;
S = surgery;
extremities);
H = hyperactive:
A = absent.
L = lumbar.
E = embolization.
tion before treatment. However, the grade of gait function after treatment in the group of patients who had been treated within 2 years 6 months after onset was significantly better than that in those treated more than 2 years 6 months thereafter @ <
0.05). (2) The change of grade of gait function in the patients treated within 1 year after onset was significantly better than that in those treated more than 1 year after onset @ < 0.05), and that in the patients who were 570 years old at the time of
456
Surg Neurol 1995;43:453-8
El Functional Logue [l]
Grading According
Kohno et al
to Aminoff and
GAIT DISTURBANCE GO: normal Gl: onset of leg weakness, abnormal stance or gait, without restriction of locomotor activity G2: restricted activity, but not requiring support G3: requires one stick for walking G4: requires crutches, walker, or 2 sticks for walking G5: unable to stand, confined to bed or wheelchair
DISTURBANCE OF MICTURITION
MO: normal Ml: mild (hesitancy, urgency, or frequency, altered sensation but continent) M2: moderate (occasional urinary incontinence or retention) M3: severe (total urinary incontinence or persistent retention)
treatment was significantly better than that in those who were ~70 years old at the time of treatment @ < 0.05). (3) There was no correlation between the duration from onset until treatment and the grade of urinary function before treatment. However, the functional grade of micturition after treatment in the patients treated within 2 years after onset was significantly better than that in those treated more than 2 years after onset @ < 0.05). (4) The patients with slight or moderate disturbance of gait function before treatment (grades 0, 1, 2, or 3) showed significantly more marked improvement of gait function after treatment than those with severe disability (grades 4 or 5) @ < 0.001). The change after treatment in urinary function in the patients with slight or moderate disturbance of urinary function (grades 0, 1, and 2) was slightly better than that in those with severe disturbance (grade 3) @ = 0.056). (5) The gait function before and after treatment of the patients with hyperactive DTR was significantly better than patients in whom DTR in the lower extremities were absent @ < 0.05). (6) The patients in whom DTR in the lower extremities were absent showed significantly poorer urinary function before and after treatment than that in the patients with hyperactive DTR 0, < 0.05). (7) There were no correlations among the age, the duration from onset until treatment, and DTR status. (8) The functional grade of gait and urinary disturbances before and after treatment in the patients who underwent surgical treatments did not differ significantly from those in the patients who received embolization therapies.
DISCUSSION CLINICAL FACTORS CORRELATED WITH THE FUNCTIONAL PROGNOSIS Our investigation revealed that the major factors correlated with the functional prognosis are the duration from onset until treatment and the functional grades of gait and urinary disturbance before treatment, as well as the DTR status. However, no correlation was observed between the duration and DTR status, nor between the duration and the functional grade of either gait or urinary disturbance before treatment. Symon et al [14] described that in 46 surgically treated cases the frequency of patients with improvement in gait and urinary function after surgery was higher in the group of moderately disabled patients than in the group of severely disabled patients; they suggested that preoperative neurologic status was correlated with functional prognosis. But they did not refer to the degree of postoperative functional status nor changes of functional grade, and statistical approval was not performed. Rosenblum et al [13] and Oldfield and Doppman [ 121 stated that preoperative muscle strength and functional grade (by Aminoff and Logue [ 11) had a direct relationship to postoperative ones in 26 surgically treated patients, but statistical appraisal was not performed. Aminoff and Logue [l] referred to the relationship between the duration after onset and functional grade of gait in 60 patients with spinal vascular malformations, but it is unknown how many radiculomeningeal AVMs were included. Our study statistically confirmed that the duration from onset until treatment and the functional grades of gait and urinary disturbance before treatment are factors correlated with the functional prognosis. Moreover, we propose that the status of DTR in the lower extremities can be a convenient factor indicating functional prognosis, although absence of DTR in the lower extremities is considered to be a severely disabled condition. Symon et al reported that absent DTR in the lower extremities was recognized in 13 (23.6%) of their 55 patients with radiculomeningeal AVM [ 141. To summarize our study, the patient who can be expected to have a good prognosis in gait function is under 70 years old who is treated within 2 years 6 months after onset or whose gait function before treatment is grades 0, 1, 2 or 3. Although the possibility of improvement is much less than that of gait disturbance, the urinary disturbance in the patient who is treated within 2 years after onset can be expected to improve considerably. The patient
Surg Neurol 457 1995:43:453-g
Prognosis of Radiculomeningeal AVM
with absent DTR in the lower extremities cannot be expected to show marked improvement in either gait or urinary function after treatment, irrespective of the duration from onset until treatment. TREATMENTS The natural history of radiculomeningeal AVM is described to present gradual progression of symptoms, which are irreversible if not treated within 3 years [ 1,121. Hence, some treatment must be applied in order to counter or halt the developing neurologic deficits in patients with radiculomeningeal AVM. Concerning the treatments of radiculomeningeal AVM, it is controversial to select either surgery or embolization therapy [2-51. Recently, the risk of recanalization in embolization therapy has been repeatedly pointed out. Morgan and Marsh [lo] described that recanalization occurred in more than 11 of 18 embolization therapies in 14 patients with radiculomeningeal AVM, and they considered that current polyvinyl alcohol (WA, particulate material) could not expected to have a permanent effect. Hall et al [4] observed recurrent symptoms in two of three patients with radiculomeningeal AVM treated by embolization therapy with PVA, recommended surgery as a curative treatment, and also emphasized the necessity of follow-up angiography after embolization therapy. On the other hand, surgery for radiculomeningeal AVM is said to be permanently effective and involves comparatively easy and safe procedures [4,10,11,14]. The most common operation for radiculomeningeal AVM is interruption of the radiculomedullary vein continuing to the coronal venous plexus and electrocoagulation or resection of the nidus itself if visible [7,9,11,13,14]. Reported surgical results were generally good, but approximately 20%-30% patients show no change postoperatively [ 12,141. Our study reveals that the outcome of surgical treatment shows no marked difference from that of embolization therapy and in the selection of the treatment, the risk of recanalization and the degree of invasion should be considered. There are few reports regarding the operative indications in radiculomeningeal AVM based on the functional prognosis, but Symon et al described that patients diagnosed before the functional disturbance becomes severe are good candidates for operation [ 141. Contrarily, for patients who cannot be expected to have a good functional prognosis or for the poor operative risk patients, embolization therapy, which is less invasive although it carries the risk of recanal-
ization, is considered possible. If recanalization occurs, surgical treatment may be performed in patients who unexpectedly improve after embolization therapy. Finally, we emphasize that it is very important to diagnose this disease early based on the features of the clinical symptoms and magnetic resonance imaging in order to obtain a good functional outcome
tbl. The authors thank Dr. Chikuma Hamada for his valuable advice in statistical management.
REFERENCES 1. Aminoff MJ and Logue V. The prognosis of patients with spinal vascular malformations. Brain 1974;97: 211-8. 2. Cahan LD, Higashida RT, Halbach W, Hieshima GB. 3.
4.
5.
6.
7.
8.
9.
10.
11.
12. 13.
14.
Variants of radiculomeningeal vascular malformations of the spine. J Neurosurg 1987;66:333-7. Doppman JL, Di Chiro G, Dwyer AJ, Frank JL, Oldfield EH. Magnetic resonance imaging of spinal arteriovenous malformations. J Neurosurg 1987;66:830-4. Hall WA, Oldfield EH, Doppman JL. Recanalization of spinal arteriovenous malformations following embolization. J Neurosurg 1989;70:714-20. Hida K, lwasaki Y, Isu T, Akino M, Abe H, et al. Spinal dural AVM: Report of three cases. No Shinkei Geka 1986;14:361-6. (in Japanese) Isu T, Iwasaki Y, Akino M, Koyanagi I, Abe H. Magnetic resonance imaging in cases of spinal dural arteriovenous malformation. Neurosurgery 1989; 24:919-23. Kendall BE and Logue V. Spinal epidural angiomatous malformations draining into intrathecal veins. Neuroradiology 1977;13:181-9. Masaryk TM, Ross JS, Medic MT, Ruff RL, Warren RS, Ratcheson RA. Radiculomeningeal vascular malformations of the spine: MR imaging. Radiology 1987; 164:845-g. Merland JJ, Riche MC, Chiras J. Intraspinal extramedullary arteriovenous fistulae draining into the medullary veins. J Neuroradiol 1980;7:271-320. Morgan MK, Marsh WR. Management of spinal dural arteriovenous malformations. J Neurosurg 1989;70: 832-6. Oldfield EH, Di Chiro G, Quindlen EA, Rieth KG, Doppman JL. Successful treatment of a group of spinal cord arteriovenous malformations by interruption of dural fistula. J Neurosurg 1983;59:1019-30. Oldfield EH, Doppman JL. Spinal arteriovenous malformations. Clin Neurosurg 1988;34:161-83. Rosenblum B, Oldfield EH, Doppman JL, Di Chiro G. Spinal arteriovenous malformations: a comparison of dural arteriovenous fistulas and intradural AVM’s in 81 patients. J Neurosurg 1987;67:795-802. Symon L, Kumaya H, Kendall B. Dural arteriovenous malformation of the spine. J Neurosurg 1984;60:23847.
458
Kohno et al
Surg Neurol 1995;43:453-8
COMMENTARY
This is an interesting article in which our Japanese colleagues have carefully analyzed the literature in relation to dural arteriovenous malformations of the spine and added six cases of their own. One cannot help but admire their industry in attempting to obtain numeric grading retrospectively from the widely differing reported series, but their opinions add weight to those widely held by surgeons who have dealt with this condition for some years. It is clear that the longer the venous stasis is present the less the risk of a satisfactory outcome, and the clear documentation of capillary neovascularization and necrosis in the spinal cord in cases who have died after dural AVM had been present for a number of years, a condition previously known as the Foix-Alajouanine syndrome indicates that venous hemostasis will result in the end in ischemic cord necrosis. No recovery is then possible. In the same way, it is a fairly accepted neurosurgical axiom that the older the patient the less likely satisfactory results are to be achieved, and our Japanese colleagues are to be complimented on documenting this fact so clearly.
wants a good prognosis. Most of it is surgical statistics. 1 would like the authors to be less negative about embolization. It is true that PVA particles are not the material that should be used, because there is almost always recanalization. However, an anatomic cure can be expected with isobutyl cyanoacrylate in a high number of cases. I think it is acceptable to treat these fistulae with acrylic glue and to reserve surgery for the contraindications or failures of endovascular procedures. Gerard Debrun, M.D.
Chicago, Illinois
London, England
In a 20-year personal experience, 1have operated on 76 cases but have not had to operate any in the past 4 years. All of my cases in this last period have been embolized by Dr. Alex Berenstein, with remarkably good results. In a personal communication with Dr. Gazi Yasargil, he mentioned that he had been able to stop operating on these lesions more than 8 years ago. Length and duration of neurologic symptoms and signs have long been recognized as contributing to a poor prognosis. This is almost universal for all neurologic disorders, however.
This is an interesting article that emphasizes the need to detect spinal dural fistulae early if one
Leonard I. Malis, M.D. New York, New York
Lindsay Symon, C.B.E., T.D., F.R.C.S.