Child's Nerv Syst (I992) 8:337-342
BIlNS
9 Springer-Verlag 1992
A proposed grading and scoring system for spina bifida: Spina Bifida Neurological Scale (SBNS) Shizuo Oi 1 and Satoshi Matsumoto 2
1 Department of Neurosurgery, Kobe University, School of Medicine, 7-5-1, Kusunoki-cho, Chuo-ku, Kobe, 650 Japan 2 Shinsuma Hospital, Kobe, Japan Received February 24, 1992
Abstract. Neurological symptoms present in neonates
with spinal dysraphism often progress with growth. A simple, objective scoring system for quantitative analysis of spinal neurological deficits, called the Spina Bifida Neurological Scale (SBNS), is proposed. Scoring is based on (1) motor function, (2) reflexes, and (3) bladder and bowel function. These are each divided into six, four, and five points respectively with respect to the level of spinal funcion. Motor function and reflexes are bilaterally analyzed, and the maximum SBNS score of 15 points reflects a normal spinal neurological state (grade I). This scoring system was correlated with the clinical condition of 89 patients with spina bifida who were graded from I to V. A total score of less than 5 was associated with a nonambulatory state (grade IV or V) in 84.0% of patients, and a score of 5 - 9 was associated with an ambulatory state (grade III) in 93.8% of patients. Scores of 10-14 reflected control of bladder and bowel function (grade II) in all patients. The application of a standardized scoring scheme will assist in the evaluation of patients' clinical status and will enable analysis of chronological changes in neurological function. Key words: Spina bifida - Neurological deficit - Scoring
system - Grading - Tethered cord
Various grading systems have been applied in the field of clinical neurosurgery. These include the Glasgow Coma Scale [6] and other methods of evaluation of the level of consciousness [7, 11, 12, 16], Hunt and Hess grading [5] and the World Federation of Neurological Surgeons subarachnoid hemorrhage grading scale for intracranial aneurysms [2], and grading systems for intracranial arteriovenous malformations [13, 15]. One major benefit of these grading systems is that by means of scoring or grad-
Correspondence to: S. Oi, 2-8 Matsuzono-cho, Nishinomiya-city, 662, Japan
ing they allow quantitative analysis of clinical or neurological conditions and[ description of changes over time. Progressive spinal neurological deficit in patients with spina bifida, in particular during the growth spurt period, is a well-recognized clinical phenomenon [3, 8]. The "tethered cord syndrome" is associated with various conditions [10] including a thickened, tight filum terminale, intraspinal lipoma, intradural fibrous adhesions, diastematomyelia, and adherence of the neural placode following previous closure of a myeloschisis. The syndrome first becomes evident with clinical neurological manifestations, and is confirmed by diagnostic imaging or surgery. Therefore, the patient's neurological status, especially the spinal level of neurological function, in either form of spinal dysraphism, should be objectively followed and always compared with the neonatal status. In order to establish a standardized description of these neurological conditions, we propose a scoring system, the Spina Bifida Neurological Scale (SBNS), that reflects the patient's clinical status and enables analysis of chronological changes of neurological function. The scoring system
Description of the scoring system Evaluation of neurological function and determination of the level of spinal involvement in children are often extremely important. In spina bifida patients the major clinical problems related to the primary lesion are (1) standing, (2) ambulation, and (3) voluntary control of bladder and bowel function. These functions are closely related to the level of spinal involvement. Therefore, the assessment of residual function focused on motor function, reflexes, and bladder and bowel function. Sensory impairment is also a major symptom of spina bifida, but its assessment is difficult in children. Reflex testing, including patellar tendon reflex, Achilles tendon reflex, and anal reflex, will evaluate the sensory function of the afferent component, together with the motor function of the reflex arch.
338
Motor function scale (M.). Since it is difficult to grade muscle strength accurately in children, the scoring was designed to reveal the functioning or nonfunctioning neurological level. M o t o r testing for the neurological level evaluates each possible level of involvement f o r m L 1 - 2 to $2-3 by assessing the action of joints o f the lower limb [1, 4]: hip flexion (T12-L3), hip extension (S1), hip adduction (L2-4), hip abduction (L5), knee extension (L2-4), knee flexion (L5, $1), ankle dorsiflexion (L4, 5), ankle plantar flexion (S1, 2), ankle inversion (L4), and ankle eversion ($1). A score of 1 indicates an intact L1 level and paresis below L2; a score of 2, intact L2; 3, intact L3; 4, intact L4; 5, intact L5; 6, intact $1 and no lower limb weakness. M o t o r function is scored for the lowest intact le,r and on the worse side, if there is a difference between the right and left extremities. The m a x i m u m score for m o t o r function is 6 with intact a m b u l a t o r y function (Table 1). Reflex scale (R). The evaluation o f reflexes in spina bifida patients m a y be used to assess the function of (1) the afferent (sensory) neurons, (2) the intercalated neurons in the spinal cord, and (3) the efferent (motor) neurons. Routinely evaluated reflexes include the patellar tendon reflex (femoral nerve, L2-4), Achilles tendon reflex (tibial nerve, S1-2), and anal reflex (pudendal nerve, $3-4). Complete areflexia is scored 1. Score 2 indicates cases with the patellar tendon reflex normally or weakly present, score 3 a normal or weak Achilles tendon reflex, and score 4 a reduced but present anal reflex. Reflexes are evaluated bilaterally, and the score is assigned for the lowest responding level on the worse side, if one side is worse than the other (Table 2).
Bladder and bowelfunction scale (BB). The bladder problems associated with spina bifida are nearly always of the lower m o t o r neuron type with neurogenic flaccidity of the bladder [14], caused by a lesion o f the sacral portion ($2-4) of the cord of cauda equina [1]. Therefore, evaluation of bladder and bowel control assesses the spinal levels below those evaluated by m o t o r function testing. A score of 1 means there is no control of either bladder or bowel function. A score of 2 represents impaired but partialy controllable function o f either bladder or bowel, score 3 partial control of b o t h bladder and bowel function, score 4 control of one function and partial control of the other, and score 5 indicates intact bladder and bowel function. In infants and neonates, the voiding status cannot be evaluated clinically, and the score in this age group is 1, until they develop voluntary voiding (Table 3).
Table 1. Scoring scale for motor function. --, Complete paresis; +, incomplete paresis; +, intact Functioning Non functioning
C-Th- L1 L2
L2 L3
L3 L4
L4 L5
L5 S1
SI $2
__
+
+
+
+
__
+
+
+
+
_
_
_
+
+
+
+
+
+
+
n~ flexion extension adduction abduction
Knee extension flexion
Ankle dorsiflexion plantarflexion inversion eversion SBNS motor (worse side)
1
2
3
+__
+
+
--
--
"Jr"
_+
+
+
4
5
6
Table 2. Scoring scale for preserved reflexes. - , Absent; +, diminished; +, intact Functioning
L4
L5
S1
$2
$3
Nonfunctioning
C-Th L3 ~L2 L3 L4
L5
S1
S2
$3
$4
Patellar reflex Achilles reflex Anal reflex
.
+ -.
+ +
+ +
+ + +
+ + _+
SBNS reflex (worse side)
1
_+ .
.
.
2
3
4
Table 3. Scoring scale for bladder and bowel function. - , Uncontrollable; +, partially controllable; +, controllable Functioning C - Th L. S1 NonS2 functioning Bladder control Bowel control SBNS BB control (total)
S2
$3
$3
$4
-
-
-I-
_+
_+
+
+
+
-
__
-
_+
+
___
+
+
1
2
3
4
5
Grading of clinical status The SBNS consists of three values, each representing the spinal level of neurological involvement. This level affects the patient's activities of daily living. The clinical status is divided into five grades. Spina bifida grade I represents normal spinal neurological function, spina bifida grade II
represents conditions of voluntary control o f bladder and bowel function, spina bifida grade III indicates problems with ambulation, spina bifida grade IV represents a nona m b u l a t o r y status, and spina bifida grade V indicates a bedridden status.
339 SBNS (total) 15
-0-
-15
15.0
14
-14
13
~
11
-13
5 12,7
11.4
12
-12
OOO [] OO -11
10
10
9
-9
8
-8
7
t
6 5. 43-
(No. of cases) Status
"]• -
4.4
30
-
6.5
7"71
( 7.2
(1) 6.4
n=0
I
i I 42
n=14 n=3
Not ambulatory ~
-7
o
-6 5
o DD
n=8
oo
n=4
n=9
I
n=12
n=7
n=6
n=5
I
n=0
n=3
n=0
n=2
~ Ambulatory but paretic'-~ ,~,Ambulatory but incontinent,~ ~AII intact-~,
-" crutch \ "" or brace " " -1" ~'--"~ tw - r - . ^ . ^ ttt
< total >
n=5
O
-4 3
n=11
Infants
< partial >
Grade ~ ; ' - - " ~
Fig. 1. Grading of activities of daily living and distribution of total scores of the Spina Bifida Neurological Scale. D, Cases with myeloschisis; o, cases with spinal lipoma
The correlation between the scoring system and grades was analyzed in a series of 89 patients followed at the National Kagawa Children's Hospital Myelomeningocele Clinic and at Kobe University Hospital.
Clinical application of the scoring system Eighty-nine cases of spina bifida, 49 cases of myeloschisis, and 40 cases of spinal lipoma were evaluated with the new scoring system. Patient ages ranged from 2 weeks to 47 years (mean 7.8 years). Sixteen patients were under the age of 2 years, and the status of their voluntary control of bladder and bowel function was not evaluated. The total scores in this age group ranged from 3 (completely bedridden) to 11 (maximum score in infants). In the other 73 cases in each group each patient was assigned to one of five grades (I-IV) depending on the status of daily activities. The total SBNS scores were obtained in individual patients with myeloschisis and spinal lipoma. To evaluate the accuracy of the scoring system in predicting the status of each patient's daily activities, the distribution of the total SBNS scores in each grade was analyzed, and the results demonstrated good correlation. In grade V, the bedridden myeloschisis patients had an average total score of 3.0, while in the patients confined to a wheelchair (grade IV) the average total score was 4.4 for rnyeloschisis and 4.2 for spinal lipoma. In grade III, all total scores were greater than 5, except for 2 patients
Table 4. Estimated grade by total SBNS score and probability of accurate grading
Total score in SBNS
Estimated grade"
No. of cases within the estimated grade
Probability (%)
3 4~ 5 6 ~ 10 11 ~ 14 15
V IV III II I
8/8 13/17 30/32 14/14 2/2
100 76.5 93.8 100 100
cases cases cases cases cases
a Grading: grade I, no spinal neurological deficits; grade II, ambulatory but incontinent; grade III, ambulatory but paretic; grade IV, not ambulatory; grade V, completely bedridden
with a score of 4. Paretic patients who were ambulatory without crutches or braces tended to have higher scores than those using aids. For grade II, the scores accurately reflected the patients' voiding status, and patients with scores over 12 had partial control of bladder and bowel function. There were two patients, both with spinal lipoma, with a maximum total score of 15 (Fig. 1). As the results show, if the total score is over 11, the patient should be completely ambulatory but with problems in voiding (grade II; probability 100%). Patients with a total score of 6-10 have definite bladder and bowel problems and varying degrees of paresis and ambulation (grade III; probability 93.8%). A total score below 5 suggests a nonambulatory status, and standing is the major problem in these patients (grade IV; probability 76.5 % ) . " Completely bedridden" is the status with a total score of 3 (grade V; probability 100%; Table 4). The score also gives an estimate of the severity of deficit within each status grade (Fig. 2).
340 Lowest intact level
L1
L2
1
Reflex
L3
I
L4
2
L5
I
Sl
3
$2
I
$4
4
1
Blader. Bowel
S3
I
21314
I
[Total S[3NSwhen symmetrically involved]
M:i:i:i:i:i:i:i:i:i;i:!;i;i;i;!:i:!:!:!:!:!:!:::!:!: !:!:i:i:i:i:!:i:i:i:i:i:i:i:i:i: i:i:i:i:i:i:i:i:i:ili:ilililil ili:iliiii!ii:i:i:!i!iii!i!i!i! i!i!i!i!!i!i!i!i!i!i!iiiii!iiii iiiiiiiiliiii!i!i!iii!i!iii!!!i i!i!i!i!i!i!i!i!iiiiiiiliiii!i! i!i!i!i!i!i!i!i !i::i::i::iiilf:i ::i::i::i::i::i::i!i "!i::i::i!i!i!iii!i!i!i!i!i!iii!iii!iiiiiiiiiiii:i [toga0
. . . . . . . . . .
Estimated clinical status
[
~ Bedridden S t a n d i n g status
Grade~
VN
Ambulatory status
IV N
III~
Illustrative cases
Case 1." Spinal lipoma A 12-year-old boy was admitted because of progressive paraparesis. At 1.5 years of age, he had undergone an initial operation for lumbosacral intraspinal lipoma. He had no objective neurological signs before and after the operation except for total bladder and bowel incontinence (SBNS: M = 6, R = 3, BB = 1; total score = 10). Several months prior to admission he began to develop progressive gait disturbance and was referred to our service in an ambulatory condition using crutches (spina bifida grade III). Neurological examination revealed preservation of hip flexion and knee extension, but paresis of almost all other movements, absence of Achilles and anal reflexes, and total incontinence. The total SBNS score was 5 (M = 3, R = 1, BB = 1). Magnetic resonance (MR) imaging demonstrated a low-set conus with residual lipoma as a continuous structure with the thickened ilium terminale. The patient underwent removal of the lipoma to untether the spinal cord and roots (Fig. 3). Postoperatively, the neurological symptoms dramatically improved. There was total recovery of motor fianction except for weak ankle plantar flexion bilaterally (M = 5). The Achilles tendon reflexes returned weakly, but the anal reflex remained absent with total bladder and bowel incontinence (R=3, BB= 1). The total SBNS score increased to 9, and the patient was able to walk without aids.
Case 2." Thickened tight filum terminale This 18-month-old male was found to have a tail-like sac on the midline of the sacral region at birth. MR imaging demonstrated watery sac contents and a thick ilium terminale attached to the inner surface of the conus. Neurological examination revealed no motor weakness and intact patellar and Achilles tendon reflexes bilaterally, but absent anal reflex and somewhat weak sphincter tonus. The total SBNS score was 9 (M=6, R = 2 , BB= t as an infant). The patient underwent repair of meningomyelocele and an untethering procedure for thickened filum terminale at 5 weeks of age (Fig. 4). The postoperative course was uneventful, and high psychomotor development milestones have been normal. He started walking at 13 months of age, and now has normal ambulation.
Voiding status
II~
1 Normal
I~
Fig. 2. Level of spinal involvement and total SBNS score with estimated clinical status
Neurological examination at 1.5 years of age revealed an intact anal reflex and normal sphincter tonus. The total SBNS score is now 11 (M = 6, R = 4, BB = 1 as a normal infant). With the development of voluntary control of bladder and bowel function, the expected score will be the maximum of 15.
Discussion
It has been increasingly recognized t h a t progressive neurological d e t e r i o r a t i o n m a y o c c u r in o l d e r c h i l d r e n w i t h s p i n a bifida, n o t o n l y in the o c c u l t f o r m b u t also after r e p a i r o f myeloschisis [9]. W h e n a l o w - p l a c e d c o n u s m e d u l l a r i s is i n v a r i a b l y d e m o n s t r a t e d in v a r i o u s neur o i m a g i n g p r o c e d u r e s [9], this m a y be the cause o f the late n e u r o l o g i c a l d e t e r i o r a t i o n in s o m e cases, b u t it m a y also be a n o n s i g n i f i c a n t sign in m a n y o f the n e u r o l o g i c a l l y stable cases. T h e k e y to d i f f e r e n t i a t i o n is p r o p e r e v a l u a t i o n o f s y m p t o m a t o l o g y . E v a l u a t i o n o f the n e u r o l o g i c a l c o n d i t i o n o f i n d i v i d u a l cases w i t h s p i n a b i f i d a requires specific c o n s i d e r a t i o n in the l o n g - t e r m f o l l o w - u p . I n the p a t i e n t s we studied, 14 o f 100 p a t i e n t s ( 1 4 . 0 % ) w h o h a d p r e v i o u s l y u n d e r g o n e s u r g e r y for s p i n a b i f i d a d e v e l o p e d d e l a y e d s y m p t o m ( s ) o f p r o g r e s s i v e spinal n e u r o l o g i c dysf u n c t i o n [9]. T h e incidence o f d e l a y e d n e u r o l o g i c a l deterio r a t i o n was 10.8% in myeloschisis, 14.3% in m e n i n g o cele, a n d 2 1 . 1 % in l i p o m e n i n g o c e l e . A l l these p a t i e n t s e x h i b i t e d a g r a d u a l o n s e t o f s y m p t o m ( s ) , b e g i n n i n g 2 to 20 y e a r s after the initial r a d i c a l s u r g e r y ( m e a n age 10.7 years); the clinical m a n i f e s t a t i o n o f n e u r o l o g i c a l d i s o r d e r most commonly occurring during early childhood (mean age 6.8 years) was a n increase in the m o t o r deficit [9]. P a i n o n s p i n a l flexion was p r e s e n t in three p a t i e n t s o v e r the age o f 15 y e a r s ( m e a n age 17.3 years) [9]. P a n g a n d W i l b e r g e r [10] c o m p a r e d c h i l d h o o d a n d a d u l t cases o f t e t h e r e d c o r d s y n d r o m e a n d f o u n d t h a t p a i n is a m o r e
341
Fig. 3a, b. Case 1: spinal lipoma, operative findings, a Spinal lipoma involving the conus medullaris. Note the reversed course of the cauda equina with marked tethering, b After removal of the lipoma, the conus moved upwards and all nerve roots were fired by the untethering procedure
Fig. 4a, b. Case 2: thickened, tight ilium terminale; operative findings, a Thickened, tight filum terminale in a tail-like sac was incised at the site of attachment. b Upward movement of the untethered thickened filum terminale
c o m m o n presenting complaint in adults, whereas motor deficits and urological symptoms are common in children. Therefore, chronological analysis of the patient's neurological function is important, especially during childhood after the initial treatment of spina bifida, which is usually performed during the neonatal or infantile period. The proposed scoring system is useful in this aspect. There have been several standardized scoring or grading systems of various CNS disorders. The Glasgow Coma Scale [6], Hunt and Hess grading [5], and Spetzler and Martin grading [15] have been suggested as international standards for grading or scoring of the severity of these CNS conditions. Raimondi and Hirschauer [I I] have discussed the specific features of the immature brain with traumatic insults. They stated that the Glasgow Coma
Scale is better for resolution of higher integrative function, and that even a normal infant would not score better than 11. The specific features of immature neurological function should be carefully evaluated. Evaluation of motor function by muscle testing is well established [1, 14]. In adults, it is possible to classify muscle strength according to five grades. Our experience with this scoring system is that evaluation of the lowest intact spinal neurological level is a reasonable means of predicting the level of the functional activities of daily living, and it can be easily performed even in neonates and infants, in whom the total score may also give an accurate prediction of the clinical status after development. Reflex testing appears to be an important examination which can confirm an intact reflex arch and assesses both afferent and efferent neural function. Since qualitative
342 differences in neurological signs appear with growth and maturation of the CNS, a pathological reflex is difficult to assess in this age group. Upper m o t o r neuron disturbance may also be caused by various conditions associated with spina bifida, such as Chiari malformation, hydrocephalus, and other dysgenetic CNS malformations, and these factors may affect the scoring; therefore, the specific profile of each patient should be considered in combination with the score. In evaluating sacral neurological function, bladder and bowel control are important signs. Voluntary control cannot be evaluated during infancy. Therefore, the maximum total score in the spina bifida neurological scale of a normal infant is 11; at 2 years o f age, after p s y c h o m o t o r development, it is 15. The presence of anal wink is the only confirmatory sign in infancy. In summary, SBNS, a newly proposed scoring system for spina bifida, is of great benefit in the evaluation of patients' clinical status and quantitative analysis of chronological changes in their neurological status. The scoring system is also applicable to neonates and infants and may be used to predict their future activities of daily living.
References 1. Chusid JG (1976) Correlative neuroanatomy and functional neurology, 16th edn. Lange, Los Altos, Calif 2. Drake CG (1988) Report of World Federation of Neurological Surgeons Committee on a universal subarachnoid hermorrhage grading scale. J Neurosurg 68:985-986
3. Hoffman HJ, Hendrick EB, Humphreys RP (1976) The tethered spinal cord: its protean manifestations, diagnosis and surgical correction. Child's Brain 2:145-155 4. Hoppenfeld S (1977) Orthopaedic neurology - a diagnostic guide to neurologic levels. Lippincott, Philadelphia 5. Hunt WE, Hess RM (1968) Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14-20 6. Jennett B, Teasdale G (1977) Aspects of coma after severe head injury. Lancet 1:878-881 7. Ohta T, Waga S, Handa H, et al (1974) New grading of level of disordered consciousness (in Japanese). No Shinkei Geka 2:623 -627 8. Oi S, Matsumoto S (1988) Tethered cord syndrome. Neurosurgeons 7:117-132 9. Oi S, Yamada H, Matsumoto S (1990) Tethered cord syndrome versus low-placed conus medullaris in an over-distended spinal cord following initial repair for myelodysplasia. Child's Nerv Syst 6:264-269 10. Pang D, Wilberger JE (1982) Tethered cord syndrome in adults. J Neurosurg 57:32-47 11. Raimondi AJ, Hirschauer J (1984) Head injury in the infants and toddler. Coma scoring and outcoma scale. Child's Brain 11:12-35 12. Sano K, Manaka S, Kitamura K, et al (1983) Statistical studies on evaluation of mild disturbance of consciousness. J Neurosurg 58:223-230 13. Shi YO, Chen XC (1986) A proposed scheme for grading intracranial arteriovenous malformations. J Neurosurg 65:484489 14. Smith ED (1965) Spinal bifida and the total care of spinal myelomenigocele. Thomas, Springfield, Ill 15. Spetzler RF, Martin NA (1986) A proposed grading system for arteriovenous malformations. J Neurosurg 65:476-483 16. Starmark JE, Stalhammer D, Hilmaren E, Bosander B (1988) A comparison of the Glasgow Coma Scale and the reaction level scale (RLS85). J Neurosurg 69:699-706
BIlNS
9 Springer-Verlag 1992
A proposed grading and scoring system for spina bifida: Spina Bifida Neurological Scale (SBNS) Shizuo Oi 1 and Satoshi Matsumoto 2
1 Department of Neurosurgery, Kobe University, School of Medicine, 7-5-1, Kusunoki-cho, Chuo-ku, Kobe, 650 Japan 2 Shinsuma Hospital, Kobe, Japan Received February 24, 1992
Abstract. Neurological symptoms present in neonates
with spinal dysraphism often progress with growth. A simple, objective scoring system for quantitative analysis of spinal neurological deficits, called the Spina Bifida Neurological Scale (SBNS), is proposed. Scoring is based on (1) motor function, (2) reflexes, and (3) bladder and bowel function. These are each divided into six, four, and five points respectively with respect to the level of spinal funcion. Motor function and reflexes are bilaterally analyzed, and the maximum SBNS score of 15 points reflects a normal spinal neurological state (grade I). This scoring system was correlated with the clinical condition of 89 patients with spina bifida who were graded from I to V. A total score of less than 5 was associated with a nonambulatory state (grade IV or V) in 84.0% of patients, and a score of 5 - 9 was associated with an ambulatory state (grade III) in 93.8% of patients. Scores of 10-14 reflected control of bladder and bowel function (grade II) in all patients. The application of a standardized scoring scheme will assist in the evaluation of patients' clinical status and will enable analysis of chronological changes in neurological function. Key words: Spina bifida - Neurological deficit - Scoring
system - Grading - Tethered cord
Various grading systems have been applied in the field of clinical neurosurgery. These include the Glasgow Coma Scale [6] and other methods of evaluation of the level of consciousness [7, 11, 12, 16], Hunt and Hess grading [5] and the World Federation of Neurological Surgeons subarachnoid hemorrhage grading scale for intracranial aneurysms [2], and grading systems for intracranial arteriovenous malformations [13, 15]. One major benefit of these grading systems is that by means of scoring or grad-
Correspondence to: S. Oi, 2-8 Matsuzono-cho, Nishinomiya-city, 662, Japan
ing they allow quantitative analysis of clinical or neurological conditions and[ description of changes over time. Progressive spinal neurological deficit in patients with spina bifida, in particular during the growth spurt period, is a well-recognized clinical phenomenon [3, 8]. The "tethered cord syndrome" is associated with various conditions [10] including a thickened, tight filum terminale, intraspinal lipoma, intradural fibrous adhesions, diastematomyelia, and adherence of the neural placode following previous closure of a myeloschisis. The syndrome first becomes evident with clinical neurological manifestations, and is confirmed by diagnostic imaging or surgery. Therefore, the patient's neurological status, especially the spinal level of neurological function, in either form of spinal dysraphism, should be objectively followed and always compared with the neonatal status. In order to establish a standardized description of these neurological conditions, we propose a scoring system, the Spina Bifida Neurological Scale (SBNS), that reflects the patient's clinical status and enables analysis of chronological changes of neurological function. The scoring system
Description of the scoring system Evaluation of neurological function and determination of the level of spinal involvement in children are often extremely important. In spina bifida patients the major clinical problems related to the primary lesion are (1) standing, (2) ambulation, and (3) voluntary control of bladder and bowel function. These functions are closely related to the level of spinal involvement. Therefore, the assessment of residual function focused on motor function, reflexes, and bladder and bowel function. Sensory impairment is also a major symptom of spina bifida, but its assessment is difficult in children. Reflex testing, including patellar tendon reflex, Achilles tendon reflex, and anal reflex, will evaluate the sensory function of the afferent component, together with the motor function of the reflex arch.
338
Motor function scale (M.). Since it is difficult to grade muscle strength accurately in children, the scoring was designed to reveal the functioning or nonfunctioning neurological level. M o t o r testing for the neurological level evaluates each possible level of involvement f o r m L 1 - 2 to $2-3 by assessing the action of joints o f the lower limb [1, 4]: hip flexion (T12-L3), hip extension (S1), hip adduction (L2-4), hip abduction (L5), knee extension (L2-4), knee flexion (L5, $1), ankle dorsiflexion (L4, 5), ankle plantar flexion (S1, 2), ankle inversion (L4), and ankle eversion ($1). A score of 1 indicates an intact L1 level and paresis below L2; a score of 2, intact L2; 3, intact L3; 4, intact L4; 5, intact L5; 6, intact $1 and no lower limb weakness. M o t o r function is scored for the lowest intact le,r and on the worse side, if there is a difference between the right and left extremities. The m a x i m u m score for m o t o r function is 6 with intact a m b u l a t o r y function (Table 1). Reflex scale (R). The evaluation o f reflexes in spina bifida patients m a y be used to assess the function of (1) the afferent (sensory) neurons, (2) the intercalated neurons in the spinal cord, and (3) the efferent (motor) neurons. Routinely evaluated reflexes include the patellar tendon reflex (femoral nerve, L2-4), Achilles tendon reflex (tibial nerve, S1-2), and anal reflex (pudendal nerve, $3-4). Complete areflexia is scored 1. Score 2 indicates cases with the patellar tendon reflex normally or weakly present, score 3 a normal or weak Achilles tendon reflex, and score 4 a reduced but present anal reflex. Reflexes are evaluated bilaterally, and the score is assigned for the lowest responding level on the worse side, if one side is worse than the other (Table 2).
Bladder and bowelfunction scale (BB). The bladder problems associated with spina bifida are nearly always of the lower m o t o r neuron type with neurogenic flaccidity of the bladder [14], caused by a lesion o f the sacral portion ($2-4) of the cord of cauda equina [1]. Therefore, evaluation of bladder and bowel control assesses the spinal levels below those evaluated by m o t o r function testing. A score of 1 means there is no control of either bladder or bowel function. A score of 2 represents impaired but partialy controllable function o f either bladder or bowel, score 3 partial control of b o t h bladder and bowel function, score 4 control of one function and partial control of the other, and score 5 indicates intact bladder and bowel function. In infants and neonates, the voiding status cannot be evaluated clinically, and the score in this age group is 1, until they develop voluntary voiding (Table 3).
Table 1. Scoring scale for motor function. --, Complete paresis; +, incomplete paresis; +, intact Functioning Non functioning
C-Th- L1 L2
L2 L3
L3 L4
L4 L5
L5 S1
SI $2
__
+
+
+
+
__
+
+
+
+
_
_
_
+
+
+
+
+
+
+
n~ flexion extension adduction abduction
Knee extension flexion
Ankle dorsiflexion plantarflexion inversion eversion SBNS motor (worse side)
1
2
3
+__
+
+
--
--
"Jr"
_+
+
+
4
5
6
Table 2. Scoring scale for preserved reflexes. - , Absent; +, diminished; +, intact Functioning
L4
L5
S1
$2
$3
Nonfunctioning
C-Th L3 ~L2 L3 L4
L5
S1
S2
$3
$4
Patellar reflex Achilles reflex Anal reflex
.
+ -.
+ +
+ +
+ + +
+ + _+
SBNS reflex (worse side)
1
_+ .
.
.
2
3
4
Table 3. Scoring scale for bladder and bowel function. - , Uncontrollable; +, partially controllable; +, controllable Functioning C - Th L. S1 NonS2 functioning Bladder control Bowel control SBNS BB control (total)
S2
$3
$3
$4
-
-
-I-
_+
_+
+
+
+
-
__
-
_+
+
___
+
+
1
2
3
4
5
Grading of clinical status The SBNS consists of three values, each representing the spinal level of neurological involvement. This level affects the patient's activities of daily living. The clinical status is divided into five grades. Spina bifida grade I represents normal spinal neurological function, spina bifida grade II
represents conditions of voluntary control o f bladder and bowel function, spina bifida grade III indicates problems with ambulation, spina bifida grade IV represents a nona m b u l a t o r y status, and spina bifida grade V indicates a bedridden status.
339 SBNS (total) 15
-0-
-15
15.0
14
-14
13
~
11
-13
5 12,7
11.4
12
-12
OOO [] OO -11
10
10
9
-9
8
-8
7
t
6 5. 43-
(No. of cases) Status
"]• -
4.4
30
-
6.5
7"71
( 7.2
(1) 6.4
n=0
I
i I 42
n=14 n=3
Not ambulatory ~
-7
o
-6 5
o DD
n=8
oo
n=4
n=9
I
n=12
n=7
n=6
n=5
I
n=0
n=3
n=0
n=2
~ Ambulatory but paretic'-~ ,~,Ambulatory but incontinent,~ ~AII intact-~,
-" crutch \ "" or brace " " -1" ~'--"~ tw - r - . ^ . ^ ttt
< total >
n=5
O
-4 3
n=11
Infants
< partial >
Grade ~ ; ' - - " ~
Fig. 1. Grading of activities of daily living and distribution of total scores of the Spina Bifida Neurological Scale. D, Cases with myeloschisis; o, cases with spinal lipoma
The correlation between the scoring system and grades was analyzed in a series of 89 patients followed at the National Kagawa Children's Hospital Myelomeningocele Clinic and at Kobe University Hospital.
Clinical application of the scoring system Eighty-nine cases of spina bifida, 49 cases of myeloschisis, and 40 cases of spinal lipoma were evaluated with the new scoring system. Patient ages ranged from 2 weeks to 47 years (mean 7.8 years). Sixteen patients were under the age of 2 years, and the status of their voluntary control of bladder and bowel function was not evaluated. The total scores in this age group ranged from 3 (completely bedridden) to 11 (maximum score in infants). In the other 73 cases in each group each patient was assigned to one of five grades (I-IV) depending on the status of daily activities. The total SBNS scores were obtained in individual patients with myeloschisis and spinal lipoma. To evaluate the accuracy of the scoring system in predicting the status of each patient's daily activities, the distribution of the total SBNS scores in each grade was analyzed, and the results demonstrated good correlation. In grade V, the bedridden myeloschisis patients had an average total score of 3.0, while in the patients confined to a wheelchair (grade IV) the average total score was 4.4 for rnyeloschisis and 4.2 for spinal lipoma. In grade III, all total scores were greater than 5, except for 2 patients
Table 4. Estimated grade by total SBNS score and probability of accurate grading
Total score in SBNS
Estimated grade"
No. of cases within the estimated grade
Probability (%)
3 4~ 5 6 ~ 10 11 ~ 14 15
V IV III II I
8/8 13/17 30/32 14/14 2/2
100 76.5 93.8 100 100
cases cases cases cases cases
a Grading: grade I, no spinal neurological deficits; grade II, ambulatory but incontinent; grade III, ambulatory but paretic; grade IV, not ambulatory; grade V, completely bedridden
with a score of 4. Paretic patients who were ambulatory without crutches or braces tended to have higher scores than those using aids. For grade II, the scores accurately reflected the patients' voiding status, and patients with scores over 12 had partial control of bladder and bowel function. There were two patients, both with spinal lipoma, with a maximum total score of 15 (Fig. 1). As the results show, if the total score is over 11, the patient should be completely ambulatory but with problems in voiding (grade II; probability 100%). Patients with a total score of 6-10 have definite bladder and bowel problems and varying degrees of paresis and ambulation (grade III; probability 93.8%). A total score below 5 suggests a nonambulatory status, and standing is the major problem in these patients (grade IV; probability 76.5 % ) . " Completely bedridden" is the status with a total score of 3 (grade V; probability 100%; Table 4). The score also gives an estimate of the severity of deficit within each status grade (Fig. 2).
340 Lowest intact level
L1
L2
1
Reflex
L3
I
L4
2
L5
I
Sl
3
$2
I
$4
4
1
Blader. Bowel
S3
I
21314
I
[Total S[3NSwhen symmetrically involved]
M:i:i:i:i:i:i:i:i:i;i:!;i;i;i;!:i:!:!:!:!:!:!:::!:!: !:!:i:i:i:i:!:i:i:i:i:i:i:i:i:i: i:i:i:i:i:i:i:i:i:ili:ilililil ili:iliiii!ii:i:i:!i!iii!i!i!i! i!i!i!i!!i!i!i!i!i!i!iiiii!iiii iiiiiiiiliiii!i!i!iii!i!iii!!!i i!i!i!i!i!i!i!i!iiiiiiiliiii!i! i!i!i!i!i!i!i!i !i::i::i::iiilf:i ::i::i::i::i::i::i!i "!i::i::i!i!i!iii!i!i!i!i!i!iii!iii!iiiiiiiiiiii:i [toga0
. . . . . . . . . .
Estimated clinical status
[
~ Bedridden S t a n d i n g status
Grade~
VN
Ambulatory status
IV N
III~
Illustrative cases
Case 1." Spinal lipoma A 12-year-old boy was admitted because of progressive paraparesis. At 1.5 years of age, he had undergone an initial operation for lumbosacral intraspinal lipoma. He had no objective neurological signs before and after the operation except for total bladder and bowel incontinence (SBNS: M = 6, R = 3, BB = 1; total score = 10). Several months prior to admission he began to develop progressive gait disturbance and was referred to our service in an ambulatory condition using crutches (spina bifida grade III). Neurological examination revealed preservation of hip flexion and knee extension, but paresis of almost all other movements, absence of Achilles and anal reflexes, and total incontinence. The total SBNS score was 5 (M = 3, R = 1, BB = 1). Magnetic resonance (MR) imaging demonstrated a low-set conus with residual lipoma as a continuous structure with the thickened ilium terminale. The patient underwent removal of the lipoma to untether the spinal cord and roots (Fig. 3). Postoperatively, the neurological symptoms dramatically improved. There was total recovery of motor fianction except for weak ankle plantar flexion bilaterally (M = 5). The Achilles tendon reflexes returned weakly, but the anal reflex remained absent with total bladder and bowel incontinence (R=3, BB= 1). The total SBNS score increased to 9, and the patient was able to walk without aids.
Case 2." Thickened tight filum terminale This 18-month-old male was found to have a tail-like sac on the midline of the sacral region at birth. MR imaging demonstrated watery sac contents and a thick ilium terminale attached to the inner surface of the conus. Neurological examination revealed no motor weakness and intact patellar and Achilles tendon reflexes bilaterally, but absent anal reflex and somewhat weak sphincter tonus. The total SBNS score was 9 (M=6, R = 2 , BB= t as an infant). The patient underwent repair of meningomyelocele and an untethering procedure for thickened filum terminale at 5 weeks of age (Fig. 4). The postoperative course was uneventful, and high psychomotor development milestones have been normal. He started walking at 13 months of age, and now has normal ambulation.
Voiding status
II~
1 Normal
I~
Fig. 2. Level of spinal involvement and total SBNS score with estimated clinical status
Neurological examination at 1.5 years of age revealed an intact anal reflex and normal sphincter tonus. The total SBNS score is now 11 (M = 6, R = 4, BB = 1 as a normal infant). With the development of voluntary control of bladder and bowel function, the expected score will be the maximum of 15.
Discussion
It has been increasingly recognized t h a t progressive neurological d e t e r i o r a t i o n m a y o c c u r in o l d e r c h i l d r e n w i t h s p i n a bifida, n o t o n l y in the o c c u l t f o r m b u t also after r e p a i r o f myeloschisis [9]. W h e n a l o w - p l a c e d c o n u s m e d u l l a r i s is i n v a r i a b l y d e m o n s t r a t e d in v a r i o u s neur o i m a g i n g p r o c e d u r e s [9], this m a y be the cause o f the late n e u r o l o g i c a l d e t e r i o r a t i o n in s o m e cases, b u t it m a y also be a n o n s i g n i f i c a n t sign in m a n y o f the n e u r o l o g i c a l l y stable cases. T h e k e y to d i f f e r e n t i a t i o n is p r o p e r e v a l u a t i o n o f s y m p t o m a t o l o g y . E v a l u a t i o n o f the n e u r o l o g i c a l c o n d i t i o n o f i n d i v i d u a l cases w i t h s p i n a b i f i d a requires specific c o n s i d e r a t i o n in the l o n g - t e r m f o l l o w - u p . I n the p a t i e n t s we studied, 14 o f 100 p a t i e n t s ( 1 4 . 0 % ) w h o h a d p r e v i o u s l y u n d e r g o n e s u r g e r y for s p i n a b i f i d a d e v e l o p e d d e l a y e d s y m p t o m ( s ) o f p r o g r e s s i v e spinal n e u r o l o g i c dysf u n c t i o n [9]. T h e incidence o f d e l a y e d n e u r o l o g i c a l deterio r a t i o n was 10.8% in myeloschisis, 14.3% in m e n i n g o cele, a n d 2 1 . 1 % in l i p o m e n i n g o c e l e . A l l these p a t i e n t s e x h i b i t e d a g r a d u a l o n s e t o f s y m p t o m ( s ) , b e g i n n i n g 2 to 20 y e a r s after the initial r a d i c a l s u r g e r y ( m e a n age 10.7 years); the clinical m a n i f e s t a t i o n o f n e u r o l o g i c a l d i s o r d e r most commonly occurring during early childhood (mean age 6.8 years) was a n increase in the m o t o r deficit [9]. P a i n o n s p i n a l flexion was p r e s e n t in three p a t i e n t s o v e r the age o f 15 y e a r s ( m e a n age 17.3 years) [9]. P a n g a n d W i l b e r g e r [10] c o m p a r e d c h i l d h o o d a n d a d u l t cases o f t e t h e r e d c o r d s y n d r o m e a n d f o u n d t h a t p a i n is a m o r e
341
Fig. 3a, b. Case 1: spinal lipoma, operative findings, a Spinal lipoma involving the conus medullaris. Note the reversed course of the cauda equina with marked tethering, b After removal of the lipoma, the conus moved upwards and all nerve roots were fired by the untethering procedure
Fig. 4a, b. Case 2: thickened, tight ilium terminale; operative findings, a Thickened, tight filum terminale in a tail-like sac was incised at the site of attachment. b Upward movement of the untethered thickened filum terminale
c o m m o n presenting complaint in adults, whereas motor deficits and urological symptoms are common in children. Therefore, chronological analysis of the patient's neurological function is important, especially during childhood after the initial treatment of spina bifida, which is usually performed during the neonatal or infantile period. The proposed scoring system is useful in this aspect. There have been several standardized scoring or grading systems of various CNS disorders. The Glasgow Coma Scale [6], Hunt and Hess grading [5], and Spetzler and Martin grading [15] have been suggested as international standards for grading or scoring of the severity of these CNS conditions. Raimondi and Hirschauer [I I] have discussed the specific features of the immature brain with traumatic insults. They stated that the Glasgow Coma
Scale is better for resolution of higher integrative function, and that even a normal infant would not score better than 11. The specific features of immature neurological function should be carefully evaluated. Evaluation of motor function by muscle testing is well established [1, 14]. In adults, it is possible to classify muscle strength according to five grades. Our experience with this scoring system is that evaluation of the lowest intact spinal neurological level is a reasonable means of predicting the level of the functional activities of daily living, and it can be easily performed even in neonates and infants, in whom the total score may also give an accurate prediction of the clinical status after development. Reflex testing appears to be an important examination which can confirm an intact reflex arch and assesses both afferent and efferent neural function. Since qualitative
342 differences in neurological signs appear with growth and maturation of the CNS, a pathological reflex is difficult to assess in this age group. Upper m o t o r neuron disturbance may also be caused by various conditions associated with spina bifida, such as Chiari malformation, hydrocephalus, and other dysgenetic CNS malformations, and these factors may affect the scoring; therefore, the specific profile of each patient should be considered in combination with the score. In evaluating sacral neurological function, bladder and bowel control are important signs. Voluntary control cannot be evaluated during infancy. Therefore, the maximum total score in the spina bifida neurological scale of a normal infant is 11; at 2 years o f age, after p s y c h o m o t o r development, it is 15. The presence of anal wink is the only confirmatory sign in infancy. In summary, SBNS, a newly proposed scoring system for spina bifida, is of great benefit in the evaluation of patients' clinical status and quantitative analysis of chronological changes in their neurological status. The scoring system is also applicable to neonates and infants and may be used to predict their future activities of daily living.
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