Follow-up comparison of hydrocephalus with and without myelomeningocele DAVID B. SHURTLEFF,M.D., RICHARD KRONMAL, PH.D., AND ELDON L. FOLTZ, M.D.
Departments of Pediatrics and Biostatistics, University of Washington, Seattle, Washington, and Division of Neurological Surgery, University of California, Irvine, California A series of 454 hydrocephalic patients with and without myelomeningoceleand with and without treatment is reviewed. The survival rates for hydrocephalus alone and for hydrocephalus with myelodysplasia are comparable. The authors reach the conclusion that treatment of the hydrocephalic process and its complications is the most critical therapeutic consideration. Mental retardation is the major unalterable cause for failure to develop independence; some lesser emotional causes can be modified by encouragement. Repeated reassessment of the patient's condition and adjustment are important. Before treatment is started parents or guardians should be fully informed of the child's future potential for independent life and mental development. KEY W O R D S " hydrocephalus 9 myelomeningoeele 9 myelodysplasia 9 shunts 9 mental retardation 9 quality of survival
L
ONG-TERM studies of various types of hydrocephalic patients have contributed little to the relation of diagnosis, selection: treatment and complications to results. 6,9`''xe'xg,~a~,~8,85 The present report reviews our experience with a total of 454 hydrocephalic patients with and without myelodysplasia.
Patient Selection and Classification
Patient Selection
We initially evaluated 348 patients to determine the etiology and anatomic type of hydrocephalus and its state of progression and activity. Initial information included complete history and physical examination, gas contrast roentgenography,9 and venMethod tricular pressure recordings. 12 Some were Data recorded on a 276 separate item IBM studied by radioisotope studies? ,8,",39 computerized record were analyzed by the Physical examination included notes on head Conversational Computer Statistical Service circumference, status of fontanelle, presence (CCSS)? 5 Survival was expressed in charts of sunset sign and prominence of scalp veins. describing life tables computed on an ac- Developmental assessments included tests aptuarial basis? ,~3,~ Autopsy data were ob- propriate for age including the Gesell and tained in 58% of the deceased patients, and Denver Developmental Scales, the Bailey Inwere added for purposes of analysis. fant Score, the Peabody Picture, Draw-a-
J. Neurosurg. / Volume 42 / January, 1975
61
D. B. Shurtleff, R. Kronmal and E. L. Foltz Man, Stanford-Binet and Wechsler Intelligence tests. At this point the decision for or against neurosurgical operative treatment was made. Regardless of this decision, all patients were examined at least yearly. Patients with shunts inserted or with a questionable clinical situation were seen at 3to 6-month intervals. If the original prognosis proved wrong patients were transferred to the appropriate treatment group after full discussion of the probable prognosis with parents. The first shunt procedure in all but a few cases was a ventriculoauriculostomy (VA) using a Pudenz-Heyer system? 6 The infant size (1-mm) cardiac catheter-valve and pumps have been used only during the past 9 years. Shunts were revised because of infection, right heart thrombosis, acute or recurrent obstruction, and for insertion of "high" pressure shunts to avoid aqueductal occlusion.S,27,a2 An additional 106 cases with no evidence of progressive hydrocephalus had no air contrast, pressure or radioisotope studies.
Patient Classification Active Hydrocephalus Treated Surgically. In 1963 we reported a surgical group of 65 patients; 9 that group has increased to 233 patients. Our criteria for inclusion in this group included: 1. Evidence of progressive hydrocephalus as manifested by increased intracranial pressure; ~ increasing ventricular size as indicated by pneumoencephalography, or increasing head size with other confirmatory clinical signs (bulging fontanel, separation of sutures, "sunset sign" or prominent scalp veins) 2. Evidence of a brain mass greater than 60% normal size, or a frontal cerebral mantle at least 1 cm thick 9,85,37 3. Adequate development for age. Brain malfunction was not considered a contraindication to treatment when the child was too young, or when the family, fully cognizant of the child's limited intellectual potential, requested surgery. Active Hydrocephalus not Treated Surgically. This group now includes 115 patients, 67 selected since 1963 and 48 from our original study. Our criteria for inclusion in this group were:
62
1. Enlarging heart or ventricle 2. Evidence of advanced destruction of brain, namely, a frontal mantle less than 1 cm thick or a brain mass less than 60% of normaP ,35,a7 3. Brain malfunction incompatible with reasonable adaptation 4. Some other systemic disease of sufficient severity to preclude survival beyond childhood (for instance, severe congenital heart disease) 5. Evidence for a systemic disease causing both the hydrocephalus and brain destruction (for instance, mucopolysaccharidosis).
Inactive Untreated Hydrocephalus. The condition of patients with ventriculomegaly, low pressure, and a static or normal head growth rate was considered arrested; 17'8~these patients were not assigned to operative or nonoperative groups unless the hydrocephalus became progressive. There were 106 such patients with myelodysplasia and inactive or clinically insignificant hydrocephalus? 9,~,3~ The critical difference between these 106 patients and the previous two groups was the absence of progressing hydrocephalus. Results
The 454 cases comprising this study have been tabulated in Table 1 according to roentgenographic and isotope diagnosis supplemented by postmortem findings. Only two of 106 patients classified as having communicating hydrocephalus under the heading of "myelodysplasia without active hydrocephalus" had roentgenographic studies; they had had previous pneumoencephalography or ventriculography; only 13 of 57 patients with Arnold-Chiari malformation are doing well.
Mortality Table 2 records the cause of death in 142 patients. We attributed acute cardiopulmonary failure and terminal aspiration pneumonitis to pressure on the midbrain from severe untreated hydrocephalus. Uncontrolled hydrocephalus was the commonest cause of death; those without shunts did the worst. Infection was the next most common cause; it appeared in the CSF of the minimally treated myelodysplastic patients and in the blood and CSF of patients with shunts.
J. Neurosurg. / Volume 42 / January, 1975
Hydrocephalus with and without myelomeningocele TABLE !
Clinical summary of 454 cases with hydrocephalus Operation Myelo- No Myelodysplasia dysplasia
Etiology of Hydrocephalus aqueductal stenosis 132 only 80 with Arnold-Chiari 28 with hydranencephaly 24 communicating hydrocephalus 237 etiology obscure 210 after CSF bleeding 14 after CNS infection 13 Amold-Chiari malformation 29 congenital cystic brain disease 10 third ventricle mass or cyst 3 Dandy-Walker syndrome l0 brain anomalies encephalocele 4 other 4 multiple 7 other system anomalies 10 malignant tumor 5 undiagnosed 3 total 454
49 (33) 17 (8)
21 0
49 (29) 0 0 17 (5) 0 0 1 (0)
28 (14) 8 (3) 9 (4) 0 7 (5) 3 (2) 5 (2)
0 0 3 3 0 3 142
4 0 1 2 3 0 91
(0) (0) (1)
No Operation MyeloNo Myelodysplasia dysplasia
(12)
6 11 8
(0) (3)
4 (0) 0 16
24 (3) 0 0 12 (0) 0 0 1 (0)
(2)
0
(1) (0) (0)
1 (0) 2 (0) 0 0 65
Myelodysplasia Without Active Hydrocephalus
5 6 4 0 3 0 3 0 4 2 2 1 0 50
(3) (1) (0)
0 0 104 (69) 0 0 0 0
(1) (0) (0) (0) (0) (0)
0 0 0 1 1 0 106
(o) (o)
Number in parentheses are currently alive and well; all others are dead or non-functional due to mental retardation or severe neurological handicaps.
TABLE 2
Cause of death in 142 patients Cause of Death
Shunt Operation MyeloNo Myelodysplasia dysplasia
hydrocephalus shunt obstruction no shunt terminal pulmonary crisis cardiopulmonary failure cardiac anomaly vena cava & cardiac thrombosis; pulmonary embolization cardiac arrest (anesthesia) pneumocardium (CNS air study) arteriosclerotic heart failure pneumonia laryngeal stridor with Arnold-Chiari infection CSF CSF + septicemia septicemia sudden death with seizures ? etiology progression of tumor trauma. CNS bleeding miscellaneous unknown total
3 3 1
3 -2
1
1
3 1 1 --4
1 ----
2 9 4 1 -1 -0 34
1 6 3 3 2 -3* 2 28
No Shunt Operation MyeloNo Myelodysplasia dysplasia --
--
10
13
1
2
5
--
7
--
1
--
-1
---
1
1
1
--
8
--
14 5 --1
2 -----
1
1
-4 52
-2 28
* One gastric perforation; one electrolyte with V-U shunt; one epiglottitis with H. Influenzae
J. Neurosurg. / Volume 42 / January, 1975
63
D. B. S h u r t l e f f , R . K r o n m a l I00-
a n d E. L. F o l t z
-L o u r e n c e , A r c h . D i s Child 1971 --Treoted U W 1 4 2 P a t l e n t s 1 9 7 3 ....... U n t r e o t e d U,W 6 5 P o t i e n f s 1973
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t~ ~9 8 0 -
~
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~
~
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-
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.
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.
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~Arch. Dis.Child, 1962
7 Age
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15
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18+
FIG. 2. Graph showing survival of our patients with hydrocephalus only and for a mixed series of hydrocephalic patients with and without myelodysplasia reported by Laurence and Coates.
Survival Patients with Hydrocephalus Alone or with Myelodysplasia. Figure 1 shows survival for
three groups of treated patients. The first group included 113 patients with either hydrocephalus alone or hydrocephalus with myelodysplasia (initially reported in 1963).9 The second group included patients with both hydrocephalus and myelodysplasia. Those in the third group had hydrocephalus only. By the age of 10 years there is a surprisingly similar survival expectancy of 60% to 63% for all three groups regardless of the presence of myelodysplasia. The mortality rate was unchanging so that only 54% survived to 15 years of age. Patients with Hydrocephalus Alone. The survival curves for our treated and untreated patients, and for another series of untreated 64
P-
+'%,.,.z
'
'
~
' ~
'
§
'
Age
~
in
'
,'; ' , L s '
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FIG. 3. Graph showing survival of patients with hydrocephalus and myelodysplasia. Broken line = 142 treated patients; dotted line = 65 untreated patients; solid line = a group reported by Laurence and Tew, including some with encephaloceles.
Hydrocephalic Patients with Myelodysplasia. Figure 3 demonstrates survival for 207
s
~Zi;;;;;7"67;: ss H o.ly
L. . . . . .
hydrocephalus patients reported by Laurence and Coates 18 are shown in Fig. 2. Only 9% of our untreated hydrocephalic patients were surviving at the age of 10, whereas 52% of the treated group were alive at 15 years of age. Laurence's comparable group of untreated patients showed a survival rate of 22% at 10 years of age.
I00~1._ l
6oJil
1
,
18+
FIG. 1. Graph showing survival of three groups of treated patients. Solid line indicates figures from our earlier series of hydrocephalic patients with and without myelodysplasia; dotted line indicates hydrocephalic patients with myelodysplasia (this series); broken line indicates patients with hydrocephalus only.
a o t ~ L__; Jil ~--~ . . . . . . . . . . .
" .............
-
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60-
~
~9 4 0 -
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patients with active hydrocephalus plus myelodysplasia. The untreated group of 65 patients had a poor prognosis, but the actively treated group of 142 patients had a better survival rate. One in 10 patients in the untreated group survived to 8 years of age; during this same life span 64% of the treated patients survived. Mortality continued in the untreated group so that one in six of the remaining had died by the age of 15 years; thus only 53% of the original untreated group survived.
Quality of Survival Hydrocephalic Patients without Myelodysplasia. Figure 4 left illustrates the quality
of survival experienced by treated hydrocephalic children; it is the same curve as in Figs. 1 and 2. No normally functioning children between the ages of 2 and 10 years died, but the incidence of death increased sharply in the early teenage years. The proportion of mentally retarded patients diminished from 22% to 13% by the age of 10 years, but then increased to 26% at 14 years.
Hydrocephalic Patients with Myelodysplasia. All of the untreated poor prognosis cases in this group are mentally retarded and
J. Neurosurg. / Volume 42 / January, 1975
Hydrocephalus with and without myelomeningocele lO0-
M R = olive retorded A I W = olive, normol LQ. ronge OEAO
I O 0 "] .~ ~
80 ~
....
DEAD
-
~ 60.
iiiiiililiiiiiiiiiiiii:::~ ~ i]iii]ii];:ii!iil;:i!]::il]iiiiiii:~:~:!:!:!:!:~:i:i:~:~:~:~:~:~ ..............
........................................ i,~,,,,~:?~:~
:::::::::::::::::::::::::::::::::::::::::::::: :::::::::::::::::::::::::::::::::::::::::::::::::::::::::::
~- 6 0 -
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"~ 4 0 .
201
~
'~
-
A/W
N 20-
Age
in
years
Age
in
years
FIG. 4. Graphs showing quality of survival of patients treated with ventriculoauricular sunts. Left." Patients with hydrocephalus only. Number of cases = 91. Right: Patients with hydrocephalus and myelodysplasia. Number of cases = 142. MR = alive, retarded; A/W = alive, normal IQ range. in custodial care. The comparable results among the treated patients are shown in Fig. 4 right. Between the ages of 2 and 15 years the proportion with normal intellect varied from 60% to 40% but showed little change, while the initial 30% of retarded survivors decreased to 13% during the same life span. Patients with Myelodysplasia Alone. In a group of 106 good prognosis myelodysplastic patients with clinically insignificant or static hydrocephalus, 89% survived at 1 year of age, but 15% of these patients were retarded. The only death in this group after the age of 1 year was due to cardiovascular decompensation in a 73-year-old man. The relationship of the neurological level of effective motor function to survival and functional capacity is charted in Figs. 5 and 6. Patients with neuromotor function above L-2 have been combined because there were no obvious differences between patients with lesions at high lumbar and thoracic levels. All 248 cases of myelodysplasia, whether with surgical or natural arrest of hydrocephalus, are included. Hydrocephalus is therefore not a significant factor in the results for this group. Low lesions obviously were associated with a favorable survival rate and a higher percentage of patients with normal intellect. IQ tests were used for definition of potential function or "mental retardation" (Figs. 4 and 5). Since these designations do not adequately describe the actual function of adult patients, we have charted the current function of 91 teenage and adult patients in Fig. 6. To be classified "independent," a patient had to be totally self-sufficient as a housewife, wage earner, or be in the appropriate grade in
J. Neurosurg. / Volume 42 / January, 1975
school. All three partially independent adults with L-3 or lower level lesions had normal IQ scores but were emotionally disturbed and living on welfare. The other two partially independent young adults, both with T-12 level lesions, were recently graduated from school. Three patients with thoracic level lesions are totally independent. Two of the three dependent adults are severely retarded and the third is of normal intellect but with severe musculoskeletal deformities. More teenagers with high level lesions (95%) are partially or totally dependent than are their adult counterparts (50%). Only 24 of the teenagers are shunt-dependent; five of these are retarded and totally dependent, while six others are partially independent. Of the teenagers not treated with a shunt, 11 are totally dependent; six of the latter have normal intellects but have acquired secondary incapacitating deformities. Eight (20%) of the teenagers who do not have shunts are partially dependent. Discussion Our 106 cases with insignificant or "arrested" hydrocephalus 16,~ associated with myelodysplasia may represent a mixed group with Arnold-Chiari (Type II) malformation and either aqueductal stenosis or kinking? .25 The diagnoses in Tables 1 and 2 are otherwise accurate. This study includes a relatively smaller number of patients with unoperated aqueductal stenosis and communicating hydrocephalus without myelodysplasia than that of our report of 1963.9 Some of the differences in 65
D. B. Shurtleff, R. Kronmal and E. L. Foltz
Fro. 5. Graphs showing quality of survival in relation to the level of myelodysplasia. Upper Left: Thoracic and high lumbar (L1-2) levels. Upper Right: Middle to low lumbar (L3-5) levels. Lower Left." Sacral level and no neurological loss group. MR = alive, retarded; A/W = alive, normal IQ range.
the two series represent a policy change. Since completion of our first study, we have attempted to avoid the complications of unnecessary surgery to preserve the intellects of children with actively progressive hydrocephalus. The details of our psychological observations have been summarized and differ little from other reports of decreased performance IQ tests as compared to relative verbal facility?.n The factors responsible for our poor results seem equally related to diagnosis, 83,3',s7 pathophysiology,5,7,s'~4`~s'~*'25's* and the complications of treatment.*,~~ The relatively poor prognosis for patients with Arnold-Chiari malformation is due to the fact that these children were referred only when either the family or custodial care staff requested help in the prevention of unmanageable head enlargement. We believe the early mortality characteristic in all the survival charts is related to shunting difficulties, central nervous system infections, or other systemic diseases such as pulmonary hyaline membrane disease or cardiopulmonary failure. There is a better survival outlook for patients with low level myelodysplasia than for patients with higher level lesions. These differences may reflect a greater incidence of "natural arrest" among patients with low 66
level lesions; in the patients with high lesions the difference may be due to a combination of retardation and some factor in our selection process. More brain malformation and mental retardation have been reported in patients with high as compared to low level myelodysplastic lesions?,19,2~ Our series includes patients who may have become retarded before we saw them, but this possibility is not particularly significant since
Fro. 6. Block chart showing relation of present function in teenage and adult patients to level of myelodysplasia. J. Neurosurg. / Volume 42 / January, 1975
Hydrocephalus with and without myelomeningocele an increased incidence of mental retardation has been described in a group seen soon after birth. 2~ The survival of mentally retarded and hydrocephalic patients for years after withdrawal or cessation of surgical treatment, or without any treatment at all, clearly illustrates the hazard of informing parents that severely hydrocephalic or grossly malformed infants will die in "a short time." Even with careful selection, only one in five untreated patients survives to the age of 1 year, one in seven to the age of 2 years, and one in 10 to 10 years. If a child lives with untreated congenital hydrocephalus to 3 years of age, his chance of dying before he is 10 years old is 5% or one in 20. On the other hand, even with preselection and complete medical and surgical therapy only 50% of our patients survived for 15 years. The differences between this survival rate and the lower one reported by Laurence and Tew le'x9 can be explained by the fact that the latter include newborns and patients with encephaloceles; our series excludes practically all such patients. Although knowledge of the chances for survival or mental retardation help in the decision for or against early surgical intervention, these data do not adequately predict the potential adult performance of infants born with myelodysplasia. The information in Fig. 6 suggests that treatment keeps many patients alive. We have 65 patients aged 13 to 19 years old, and only 26 between 20 and 80 years old. The apparently better chances for survival for our teenagers may represent medical and surgical advances as well as social attitudes toward the value of treatment. Among patients with low level lesions, the proportion of dependent to independent patients is the same regardless of age. The much higher dependency rate among our teenagers (95%) compared to adults (50%) may reflect a later developmental pattern, a need for longer dependency before the young adult with severe paralysis can achieve independence. Many of these patients with high level lesions also have mild to moderate mental retardation. The future of these marginal cases remains in doubt. Among the adults in our series there are a number who could become socially adjusted except for their emotional problems. Three men and eight women, two with only minimal urinary control, have had what they describe J. Neurosurg. / Volume 42 / January, 1975
as "normal" sexual relations despite urine soilage and complete lack of genital sensation. Four other men remain celibate because of embarrassment associated with urine incontinence. Sex-related emotional problems and renal deterioration are the most significant complications among our adult patients. In our teenage patients, both of these problems are being avoided by appropriate urinary tract management. Acknowledgments Cynthia Shurtleff and Dorothy Klinger provided invaluable service in putting the clinical data into computer records. References 1. Atkinson JR, Foltz EL: Intraventricular "RISA" as a diagnostic aid in pre- and postoperative hydrocephalus. J Neurasurg 19:159-166, 1962 2. Badell-Ribera A, Shulman K, Paddick N: The relationship of non-progressive hydrocephalus to intellectual functioning in children with spina bifida cystica. Pediatrics 37:787-793, 1966 3. Bligh A, Shurtleff DB, Leach KG, et al: Isotope cisternography using ~gmTc labeled human albumin in spina bifida cystica, in Harbert JC (ed): Cisternography and Hydrocephalus: a Symposium. Springfield, Ill, Charles C Thomas, 1972, pp 397-412 4. Brocklehurst G, Gleave JRW, Lewin WS: Early closure of myelomeningocele, with special reference to left movement. Br Med J 1:666-669, 1967 5. Emery JL: Kinking of the medulla in children with acute cerebral oedema and hydrocephalus and its relationship to the dentate ligaments. J Nenrol Nenrosurg Psyehiat 30:267-275, 1967 6. Fisher RG, Uihlein A, Keith HM: Spina bifida and cranium bifidum: Study of 530 cases. Proc Mayo Clin 27:443-454, 1968 7. Foltz EL: Hydrocephalus: the value of treatment. South Med J 61:443-454, 1968 8. Foltz EL, Shurtleff DB: Conversion of communicating hydrocephalus to stenosis or occlusion of the aqueduct during ventricular shunt. J Neurosurg 24:520-529, 1966 9. Foltz EL, Shurtleff DB: Five-year comparative study of hydrocephalus in children with and without operation (113 cases). J Neurnsurg 20:1064-1079, 1963 10. Friedman S, Zita-Gozum C, Chatten J: Pulmonary vascular changes complicating ventriculovascular shunting for hydrocephalus. J Pediatr 64:305-314, 1964 11. Hagberg B, Sjorgen I: The chronic brain syndrome of infantile hydrocephalus.A follow-up 67
D. B. Shurtleff, R. Kronmal and E. L. Foltz
12.
13. 14. 15.
16. 17. 18.
19.
20.
21.
22. 23.
24. 25. 26.
27.
28. 68
study of 63 spontaneously arrested cases. Am J Dis Child 112:189-196, 1966 Hayden PW, Shurtleff DB, Foltz EL: Ventricular fluid pressure recordings in hydrocephalic patients. Arch Neural 23:147-154, 1970 Hill B (ed): Principles of Medical Statistics, New York, Oxford Univ Press, 1961, r 7, pp 220-236 Jasper PL, Merrill RE: Hydrocephalus and myelomeningocele: central nervous system infection. Am J Dis Child 110:652-657, 1965 Kronmal RA, Bender L, Mortensen J: A conversational statistical system for medical records. J Royal Statistical Sac Series C 19:82-92, 1970 Laurence KM: Natural history of spina bifida cystica. Proc R Sac Med 53:1055-1056, 1960 Laurence KM: RE: What is arrested hydrocephalus? J Pediatr 60:471, 1962 (Letter to editor) Laurence KM, Coates S: The natural history of hydrocephalus. Detailed analysis of 182 unoperated cases. Arch Dis Child 37:345-362, 1962 Laurence KM, Tew BJ: Natural history of spina bifida cystica and cranium bifidum cysticum. Major central nervous system malformations in South Wales, Part IV. Arch Dis Child 46:127-138, 1971 Lorber J: Results of treatment of myelomeningocele: an analysis of 524 unselected cases, with special reference to possible selection for treatment. Dev Med Child Neural 13:279-303, 1971 Lorber J: Systematic ventriculographic studies in infants born with meningomyelocele and encephalocele. The incidence and development of hydrocephalus. Arch Dis Child 36:381-389, 1961 Matson DD: Surgical treatment of myelomeningocele. Pediatr 42:225-227, 1968 McCullough DC, Luessenhop A J: Evaluation of photoscanning of the diffusion of intrathecal RISA in infantile and childhood hydrocephalus. J Neurosurg 30:673-678, 1969 Morley AR: Laryngeal stridor, Arnold-Chiari malformation and medullary haemorrhages. Dev Med Child Neural 11:471-474, 1969 Peach B: The Arnold-Chiari malformation; morphogenesis. Arch Neural 12:527-535, 1965 Pudenz RH, Russel FE, Hurd HH, et al: Ventriculo-auriculostomy. A technique for shunting cerebrospinal fluid into the right auricle. Preliminary report. J Neurosurg 14:171-179, 1957 Scarff JE: Treatment of hydrocephalus: an historical and critical review of methods and results. J Neural Neurosurg Psychlat 26:1-26, 1963 Schwidde JT: Spina bifida. Survey of two hun-
29.
30. 31. 32. 33.
34.
35.
36.
37.
38.
39.
dred twenty-five encephaloceles, meningoceles and myelomeningoceles. Am d Dis Child 84:35-51, 1952 Sella A, Foltz EL, Shurtleff DB: A three year developmental study of treated and untreated hydrocephalic children, d Pediatr 69:887, 1966 (abstract) Schick RW, Matson DD: What is arrested hydrocephalus? J Pediatr 58:791-799, 1961 Shurtleff DB: Timing of learning. Phys Ther 46:136-148, 1966 Shurtleff DB, Christie D, Foltz EL: Ventriculoauriculostomy-associated infection: a 12year study. J Neurosurg 35:686-694, 1971 Shurtleff DB, Eliason BC, Oakland JA: Congenital brain cysts in infancy: diagnosis, treatment, and follow-up. Teratology 7: 183-190, 1973 Shurtleff DB, Foltz EL: Comparative study of meningomyelocele repair or cerebrospinal fluid shunt as primary treatment in spina bifida. Dev Med Child Neural Suppl 13:57-64, 1967 Shurtleff DB, Foltz EL: Ten year follow-up of 267 myelomeningocele patients, in American Academy of Orthopedic Surgeons, Symposium on Myelomeningocele, St Louis, CV Mosby Co, 1972, pp 282-293 Shurtleff DB, Foltz EL, Chapman JT: Ventriculo-skull distance. Its reliability as an estimate of "cerebral mantle" in the normocephalic child. Am J Dis Child 111: 262-266, 1966 Shurtleff DB, Foltz EL, Loeser JD: Hydrocephalus: a definition of its progression and relationship to intellectual function, diagnosis and complications. Am J Dis Child 125:688-693, 1973 Shurtleff DB, Hayden PW: The treatment of hydrocephalus with isosorbide, an oral hyperosmotic agent. J Clin Pharmacol 12: 108-114, 1972 Shurtleff DB, Hayden PW, Weeks R, et al: Temporary treatment of hydrocephalus and myelodysplasia with isosorbide: preliminary report. J Pediatr 83:651, 1973
This study was supported in part by the National Foundation-March of Dimes, National Institutes of Health Grant FR-37, Public Health Service Grant 99480, Children's Orthopedic Hospital and Medical Center Study R-24-3, and Birth Defects Bequest. This paper was presented in part before the American Association of Neurological Surgeons, Boston, Massachusetts, April 19, 1972. Address reprint requests to: David B. Shurtleff, M.D., Department of Pediatrics, University of Washington School of Medicine, 1959 Pacific Avenue NE, Seattle, Washington 98195.
J. Neurosurg. / Volume 42 / January, 1975
Departments of Pediatrics and Biostatistics, University of Washington, Seattle, Washington, and Division of Neurological Surgery, University of California, Irvine, California A series of 454 hydrocephalic patients with and without myelomeningoceleand with and without treatment is reviewed. The survival rates for hydrocephalus alone and for hydrocephalus with myelodysplasia are comparable. The authors reach the conclusion that treatment of the hydrocephalic process and its complications is the most critical therapeutic consideration. Mental retardation is the major unalterable cause for failure to develop independence; some lesser emotional causes can be modified by encouragement. Repeated reassessment of the patient's condition and adjustment are important. Before treatment is started parents or guardians should be fully informed of the child's future potential for independent life and mental development. KEY W O R D S " hydrocephalus 9 myelomeningoeele 9 myelodysplasia 9 shunts 9 mental retardation 9 quality of survival
L
ONG-TERM studies of various types of hydrocephalic patients have contributed little to the relation of diagnosis, selection: treatment and complications to results. 6,9`''xe'xg,~a~,~8,85 The present report reviews our experience with a total of 454 hydrocephalic patients with and without myelodysplasia.
Patient Selection and Classification
Patient Selection
We initially evaluated 348 patients to determine the etiology and anatomic type of hydrocephalus and its state of progression and activity. Initial information included complete history and physical examination, gas contrast roentgenography,9 and venMethod tricular pressure recordings. 12 Some were Data recorded on a 276 separate item IBM studied by radioisotope studies? ,8,",39 computerized record were analyzed by the Physical examination included notes on head Conversational Computer Statistical Service circumference, status of fontanelle, presence (CCSS)? 5 Survival was expressed in charts of sunset sign and prominence of scalp veins. describing life tables computed on an ac- Developmental assessments included tests aptuarial basis? ,~3,~ Autopsy data were ob- propriate for age including the Gesell and tained in 58% of the deceased patients, and Denver Developmental Scales, the Bailey Inwere added for purposes of analysis. fant Score, the Peabody Picture, Draw-a-
J. Neurosurg. / Volume 42 / January, 1975
61
D. B. Shurtleff, R. Kronmal and E. L. Foltz Man, Stanford-Binet and Wechsler Intelligence tests. At this point the decision for or against neurosurgical operative treatment was made. Regardless of this decision, all patients were examined at least yearly. Patients with shunts inserted or with a questionable clinical situation were seen at 3to 6-month intervals. If the original prognosis proved wrong patients were transferred to the appropriate treatment group after full discussion of the probable prognosis with parents. The first shunt procedure in all but a few cases was a ventriculoauriculostomy (VA) using a Pudenz-Heyer system? 6 The infant size (1-mm) cardiac catheter-valve and pumps have been used only during the past 9 years. Shunts were revised because of infection, right heart thrombosis, acute or recurrent obstruction, and for insertion of "high" pressure shunts to avoid aqueductal occlusion.S,27,a2 An additional 106 cases with no evidence of progressive hydrocephalus had no air contrast, pressure or radioisotope studies.
Patient Classification Active Hydrocephalus Treated Surgically. In 1963 we reported a surgical group of 65 patients; 9 that group has increased to 233 patients. Our criteria for inclusion in this group included: 1. Evidence of progressive hydrocephalus as manifested by increased intracranial pressure; ~ increasing ventricular size as indicated by pneumoencephalography, or increasing head size with other confirmatory clinical signs (bulging fontanel, separation of sutures, "sunset sign" or prominent scalp veins) 2. Evidence of a brain mass greater than 60% normal size, or a frontal cerebral mantle at least 1 cm thick 9,85,37 3. Adequate development for age. Brain malfunction was not considered a contraindication to treatment when the child was too young, or when the family, fully cognizant of the child's limited intellectual potential, requested surgery. Active Hydrocephalus not Treated Surgically. This group now includes 115 patients, 67 selected since 1963 and 48 from our original study. Our criteria for inclusion in this group were:
62
1. Enlarging heart or ventricle 2. Evidence of advanced destruction of brain, namely, a frontal mantle less than 1 cm thick or a brain mass less than 60% of normaP ,35,a7 3. Brain malfunction incompatible with reasonable adaptation 4. Some other systemic disease of sufficient severity to preclude survival beyond childhood (for instance, severe congenital heart disease) 5. Evidence for a systemic disease causing both the hydrocephalus and brain destruction (for instance, mucopolysaccharidosis).
Inactive Untreated Hydrocephalus. The condition of patients with ventriculomegaly, low pressure, and a static or normal head growth rate was considered arrested; 17'8~these patients were not assigned to operative or nonoperative groups unless the hydrocephalus became progressive. There were 106 such patients with myelodysplasia and inactive or clinically insignificant hydrocephalus? 9,~,3~ The critical difference between these 106 patients and the previous two groups was the absence of progressing hydrocephalus. Results
The 454 cases comprising this study have been tabulated in Table 1 according to roentgenographic and isotope diagnosis supplemented by postmortem findings. Only two of 106 patients classified as having communicating hydrocephalus under the heading of "myelodysplasia without active hydrocephalus" had roentgenographic studies; they had had previous pneumoencephalography or ventriculography; only 13 of 57 patients with Arnold-Chiari malformation are doing well.
Mortality Table 2 records the cause of death in 142 patients. We attributed acute cardiopulmonary failure and terminal aspiration pneumonitis to pressure on the midbrain from severe untreated hydrocephalus. Uncontrolled hydrocephalus was the commonest cause of death; those without shunts did the worst. Infection was the next most common cause; it appeared in the CSF of the minimally treated myelodysplastic patients and in the blood and CSF of patients with shunts.
J. Neurosurg. / Volume 42 / January, 1975
Hydrocephalus with and without myelomeningocele TABLE !
Clinical summary of 454 cases with hydrocephalus Operation Myelo- No Myelodysplasia dysplasia
Etiology of Hydrocephalus aqueductal stenosis 132 only 80 with Arnold-Chiari 28 with hydranencephaly 24 communicating hydrocephalus 237 etiology obscure 210 after CSF bleeding 14 after CNS infection 13 Amold-Chiari malformation 29 congenital cystic brain disease 10 third ventricle mass or cyst 3 Dandy-Walker syndrome l0 brain anomalies encephalocele 4 other 4 multiple 7 other system anomalies 10 malignant tumor 5 undiagnosed 3 total 454
49 (33) 17 (8)
21 0
49 (29) 0 0 17 (5) 0 0 1 (0)
28 (14) 8 (3) 9 (4) 0 7 (5) 3 (2) 5 (2)
0 0 3 3 0 3 142
4 0 1 2 3 0 91
(0) (0) (1)
No Operation MyeloNo Myelodysplasia dysplasia
(12)
6 11 8
(0) (3)
4 (0) 0 16
24 (3) 0 0 12 (0) 0 0 1 (0)
(2)
0
(1) (0) (0)
1 (0) 2 (0) 0 0 65
Myelodysplasia Without Active Hydrocephalus
5 6 4 0 3 0 3 0 4 2 2 1 0 50
(3) (1) (0)
0 0 104 (69) 0 0 0 0
(1) (0) (0) (0) (0) (0)
0 0 0 1 1 0 106
(o) (o)
Number in parentheses are currently alive and well; all others are dead or non-functional due to mental retardation or severe neurological handicaps.
TABLE 2
Cause of death in 142 patients Cause of Death
Shunt Operation MyeloNo Myelodysplasia dysplasia
hydrocephalus shunt obstruction no shunt terminal pulmonary crisis cardiopulmonary failure cardiac anomaly vena cava & cardiac thrombosis; pulmonary embolization cardiac arrest (anesthesia) pneumocardium (CNS air study) arteriosclerotic heart failure pneumonia laryngeal stridor with Arnold-Chiari infection CSF CSF + septicemia septicemia sudden death with seizures ? etiology progression of tumor trauma. CNS bleeding miscellaneous unknown total
3 3 1
3 -2
1
1
3 1 1 --4
1 ----
2 9 4 1 -1 -0 34
1 6 3 3 2 -3* 2 28
No Shunt Operation MyeloNo Myelodysplasia dysplasia --
--
10
13
1
2
5
--
7
--
1
--
-1
---
1
1
1
--
8
--
14 5 --1
2 -----
1
1
-4 52
-2 28
* One gastric perforation; one electrolyte with V-U shunt; one epiglottitis with H. Influenzae
J. Neurosurg. / Volume 42 / January, 1975
63
D. B. S h u r t l e f f , R . K r o n m a l I00-
a n d E. L. F o l t z
-L o u r e n c e , A r c h . D i s Child 1971 --Treoted U W 1 4 2 P a t l e n t s 1 9 7 3 ....... U n t r e o t e d U,W 6 5 P o t i e n f s 1973
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t~ ~9 8 0 -
~
~'9 8 0 H+ a-raM
60-
~
~
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-
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9
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,
,
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,
,
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.
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.
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~Arch. Dis.Child, 1962
7 Age
. . . . . . . . .
9 in
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15
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18+
FIG. 2. Graph showing survival of our patients with hydrocephalus only and for a mixed series of hydrocephalic patients with and without myelodysplasia reported by Laurence and Coates.
Survival Patients with Hydrocephalus Alone or with Myelodysplasia. Figure 1 shows survival for
three groups of treated patients. The first group included 113 patients with either hydrocephalus alone or hydrocephalus with myelodysplasia (initially reported in 1963).9 The second group included patients with both hydrocephalus and myelodysplasia. Those in the third group had hydrocephalus only. By the age of 10 years there is a surprisingly similar survival expectancy of 60% to 63% for all three groups regardless of the presence of myelodysplasia. The mortality rate was unchanging so that only 54% survived to 15 years of age. Patients with Hydrocephalus Alone. The survival curves for our treated and untreated patients, and for another series of untreated 64
P-
+'%,.,.z
'
'
~
' ~
'
§
'
Age
~
in
'
,'; ' , L s '
years
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FIG. 3. Graph showing survival of patients with hydrocephalus and myelodysplasia. Broken line = 142 treated patients; dotted line = 65 untreated patients; solid line = a group reported by Laurence and Tew, including some with encephaloceles.
Hydrocephalic Patients with Myelodysplasia. Figure 3 demonstrates survival for 207
s
~Zi;;;;;7"67;: ss H o.ly
L. . . . . .
hydrocephalus patients reported by Laurence and Coates 18 are shown in Fig. 2. Only 9% of our untreated hydrocephalic patients were surviving at the age of 10, whereas 52% of the treated group were alive at 15 years of age. Laurence's comparable group of untreated patients showed a survival rate of 22% at 10 years of age.
I00~1._ l
6oJil
1
,
18+
FIG. 1. Graph showing survival of three groups of treated patients. Solid line indicates figures from our earlier series of hydrocephalic patients with and without myelodysplasia; dotted line indicates hydrocephalic patients with myelodysplasia (this series); broken line indicates patients with hydrocephalus only.
a o t ~ L__; Jil ~--~ . . . . . . . . . . .
" .............
-
-~
0
I
60-
~
~9 4 0 -
L..~
-
patients with active hydrocephalus plus myelodysplasia. The untreated group of 65 patients had a poor prognosis, but the actively treated group of 142 patients had a better survival rate. One in 10 patients in the untreated group survived to 8 years of age; during this same life span 64% of the treated patients survived. Mortality continued in the untreated group so that one in six of the remaining had died by the age of 15 years; thus only 53% of the original untreated group survived.
Quality of Survival Hydrocephalic Patients without Myelodysplasia. Figure 4 left illustrates the quality
of survival experienced by treated hydrocephalic children; it is the same curve as in Figs. 1 and 2. No normally functioning children between the ages of 2 and 10 years died, but the incidence of death increased sharply in the early teenage years. The proportion of mentally retarded patients diminished from 22% to 13% by the age of 10 years, but then increased to 26% at 14 years.
Hydrocephalic Patients with Myelodysplasia. All of the untreated poor prognosis cases in this group are mentally retarded and
J. Neurosurg. / Volume 42 / January, 1975
Hydrocephalus with and without myelomeningocele lO0-
M R = olive retorded A I W = olive, normol LQ. ronge OEAO
I O 0 "] .~ ~
80 ~
....
DEAD
-
~ 60.
iiiiiililiiiiiiiiiiiii:::~ ~ i]iii]ii];:ii!iil;:i!]::il]iiiiiii:~:~:!:!:!:!:~:i:i:~:~:~:~:~:~ ..............
........................................ i,~,,,,~:?~:~
:::::::::::::::::::::::::::::::::::::::::::::: :::::::::::::::::::::::::::::::::::::::::::::::::::::::::::
~- 6 0 -
..............................
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i}iiliiP4ai!i]iiiililiJii
"~ 4 0 .
201
~
'~
-
A/W
N 20-
Age
in
years
Age
in
years
FIG. 4. Graphs showing quality of survival of patients treated with ventriculoauricular sunts. Left." Patients with hydrocephalus only. Number of cases = 91. Right: Patients with hydrocephalus and myelodysplasia. Number of cases = 142. MR = alive, retarded; A/W = alive, normal IQ range. in custodial care. The comparable results among the treated patients are shown in Fig. 4 right. Between the ages of 2 and 15 years the proportion with normal intellect varied from 60% to 40% but showed little change, while the initial 30% of retarded survivors decreased to 13% during the same life span. Patients with Myelodysplasia Alone. In a group of 106 good prognosis myelodysplastic patients with clinically insignificant or static hydrocephalus, 89% survived at 1 year of age, but 15% of these patients were retarded. The only death in this group after the age of 1 year was due to cardiovascular decompensation in a 73-year-old man. The relationship of the neurological level of effective motor function to survival and functional capacity is charted in Figs. 5 and 6. Patients with neuromotor function above L-2 have been combined because there were no obvious differences between patients with lesions at high lumbar and thoracic levels. All 248 cases of myelodysplasia, whether with surgical or natural arrest of hydrocephalus, are included. Hydrocephalus is therefore not a significant factor in the results for this group. Low lesions obviously were associated with a favorable survival rate and a higher percentage of patients with normal intellect. IQ tests were used for definition of potential function or "mental retardation" (Figs. 4 and 5). Since these designations do not adequately describe the actual function of adult patients, we have charted the current function of 91 teenage and adult patients in Fig. 6. To be classified "independent," a patient had to be totally self-sufficient as a housewife, wage earner, or be in the appropriate grade in
J. Neurosurg. / Volume 42 / January, 1975
school. All three partially independent adults with L-3 or lower level lesions had normal IQ scores but were emotionally disturbed and living on welfare. The other two partially independent young adults, both with T-12 level lesions, were recently graduated from school. Three patients with thoracic level lesions are totally independent. Two of the three dependent adults are severely retarded and the third is of normal intellect but with severe musculoskeletal deformities. More teenagers with high level lesions (95%) are partially or totally dependent than are their adult counterparts (50%). Only 24 of the teenagers are shunt-dependent; five of these are retarded and totally dependent, while six others are partially independent. Of the teenagers not treated with a shunt, 11 are totally dependent; six of the latter have normal intellects but have acquired secondary incapacitating deformities. Eight (20%) of the teenagers who do not have shunts are partially dependent. Discussion Our 106 cases with insignificant or "arrested" hydrocephalus 16,~ associated with myelodysplasia may represent a mixed group with Arnold-Chiari (Type II) malformation and either aqueductal stenosis or kinking? .25 The diagnoses in Tables 1 and 2 are otherwise accurate. This study includes a relatively smaller number of patients with unoperated aqueductal stenosis and communicating hydrocephalus without myelodysplasia than that of our report of 1963.9 Some of the differences in 65
D. B. Shurtleff, R. Kronmal and E. L. Foltz
Fro. 5. Graphs showing quality of survival in relation to the level of myelodysplasia. Upper Left: Thoracic and high lumbar (L1-2) levels. Upper Right: Middle to low lumbar (L3-5) levels. Lower Left." Sacral level and no neurological loss group. MR = alive, retarded; A/W = alive, normal IQ range.
the two series represent a policy change. Since completion of our first study, we have attempted to avoid the complications of unnecessary surgery to preserve the intellects of children with actively progressive hydrocephalus. The details of our psychological observations have been summarized and differ little from other reports of decreased performance IQ tests as compared to relative verbal facility?.n The factors responsible for our poor results seem equally related to diagnosis, 83,3',s7 pathophysiology,5,7,s'~4`~s'~*'25's* and the complications of treatment.*,~~ The relatively poor prognosis for patients with Arnold-Chiari malformation is due to the fact that these children were referred only when either the family or custodial care staff requested help in the prevention of unmanageable head enlargement. We believe the early mortality characteristic in all the survival charts is related to shunting difficulties, central nervous system infections, or other systemic diseases such as pulmonary hyaline membrane disease or cardiopulmonary failure. There is a better survival outlook for patients with low level myelodysplasia than for patients with higher level lesions. These differences may reflect a greater incidence of "natural arrest" among patients with low 66
level lesions; in the patients with high lesions the difference may be due to a combination of retardation and some factor in our selection process. More brain malformation and mental retardation have been reported in patients with high as compared to low level myelodysplastic lesions?,19,2~ Our series includes patients who may have become retarded before we saw them, but this possibility is not particularly significant since
Fro. 6. Block chart showing relation of present function in teenage and adult patients to level of myelodysplasia. J. Neurosurg. / Volume 42 / January, 1975
Hydrocephalus with and without myelomeningocele an increased incidence of mental retardation has been described in a group seen soon after birth. 2~ The survival of mentally retarded and hydrocephalic patients for years after withdrawal or cessation of surgical treatment, or without any treatment at all, clearly illustrates the hazard of informing parents that severely hydrocephalic or grossly malformed infants will die in "a short time." Even with careful selection, only one in five untreated patients survives to the age of 1 year, one in seven to the age of 2 years, and one in 10 to 10 years. If a child lives with untreated congenital hydrocephalus to 3 years of age, his chance of dying before he is 10 years old is 5% or one in 20. On the other hand, even with preselection and complete medical and surgical therapy only 50% of our patients survived for 15 years. The differences between this survival rate and the lower one reported by Laurence and Tew le'x9 can be explained by the fact that the latter include newborns and patients with encephaloceles; our series excludes practically all such patients. Although knowledge of the chances for survival or mental retardation help in the decision for or against early surgical intervention, these data do not adequately predict the potential adult performance of infants born with myelodysplasia. The information in Fig. 6 suggests that treatment keeps many patients alive. We have 65 patients aged 13 to 19 years old, and only 26 between 20 and 80 years old. The apparently better chances for survival for our teenagers may represent medical and surgical advances as well as social attitudes toward the value of treatment. Among patients with low level lesions, the proportion of dependent to independent patients is the same regardless of age. The much higher dependency rate among our teenagers (95%) compared to adults (50%) may reflect a later developmental pattern, a need for longer dependency before the young adult with severe paralysis can achieve independence. Many of these patients with high level lesions also have mild to moderate mental retardation. The future of these marginal cases remains in doubt. Among the adults in our series there are a number who could become socially adjusted except for their emotional problems. Three men and eight women, two with only minimal urinary control, have had what they describe J. Neurosurg. / Volume 42 / January, 1975
as "normal" sexual relations despite urine soilage and complete lack of genital sensation. Four other men remain celibate because of embarrassment associated with urine incontinence. Sex-related emotional problems and renal deterioration are the most significant complications among our adult patients. In our teenage patients, both of these problems are being avoided by appropriate urinary tract management. Acknowledgments Cynthia Shurtleff and Dorothy Klinger provided invaluable service in putting the clinical data into computer records. References 1. Atkinson JR, Foltz EL: Intraventricular "RISA" as a diagnostic aid in pre- and postoperative hydrocephalus. J Neurasurg 19:159-166, 1962 2. Badell-Ribera A, Shulman K, Paddick N: The relationship of non-progressive hydrocephalus to intellectual functioning in children with spina bifida cystica. Pediatrics 37:787-793, 1966 3. Bligh A, Shurtleff DB, Leach KG, et al: Isotope cisternography using ~gmTc labeled human albumin in spina bifida cystica, in Harbert JC (ed): Cisternography and Hydrocephalus: a Symposium. Springfield, Ill, Charles C Thomas, 1972, pp 397-412 4. Brocklehurst G, Gleave JRW, Lewin WS: Early closure of myelomeningocele, with special reference to left movement. Br Med J 1:666-669, 1967 5. Emery JL: Kinking of the medulla in children with acute cerebral oedema and hydrocephalus and its relationship to the dentate ligaments. J Nenrol Nenrosurg Psyehiat 30:267-275, 1967 6. Fisher RG, Uihlein A, Keith HM: Spina bifida and cranium bifidum: Study of 530 cases. Proc Mayo Clin 27:443-454, 1968 7. Foltz EL: Hydrocephalus: the value of treatment. South Med J 61:443-454, 1968 8. Foltz EL, Shurtleff DB: Conversion of communicating hydrocephalus to stenosis or occlusion of the aqueduct during ventricular shunt. J Neurosurg 24:520-529, 1966 9. Foltz EL, Shurtleff DB: Five-year comparative study of hydrocephalus in children with and without operation (113 cases). J Neurnsurg 20:1064-1079, 1963 10. Friedman S, Zita-Gozum C, Chatten J: Pulmonary vascular changes complicating ventriculovascular shunting for hydrocephalus. J Pediatr 64:305-314, 1964 11. Hagberg B, Sjorgen I: The chronic brain syndrome of infantile hydrocephalus.A follow-up 67
D. B. Shurtleff, R. Kronmal and E. L. Foltz
12.
13. 14. 15.
16. 17. 18.
19.
20.
21.
22. 23.
24. 25. 26.
27.
28. 68
study of 63 spontaneously arrested cases. Am J Dis Child 112:189-196, 1966 Hayden PW, Shurtleff DB, Foltz EL: Ventricular fluid pressure recordings in hydrocephalic patients. Arch Neural 23:147-154, 1970 Hill B (ed): Principles of Medical Statistics, New York, Oxford Univ Press, 1961, r 7, pp 220-236 Jasper PL, Merrill RE: Hydrocephalus and myelomeningocele: central nervous system infection. Am J Dis Child 110:652-657, 1965 Kronmal RA, Bender L, Mortensen J: A conversational statistical system for medical records. J Royal Statistical Sac Series C 19:82-92, 1970 Laurence KM: Natural history of spina bifida cystica. Proc R Sac Med 53:1055-1056, 1960 Laurence KM: RE: What is arrested hydrocephalus? J Pediatr 60:471, 1962 (Letter to editor) Laurence KM, Coates S: The natural history of hydrocephalus. Detailed analysis of 182 unoperated cases. Arch Dis Child 37:345-362, 1962 Laurence KM, Tew BJ: Natural history of spina bifida cystica and cranium bifidum cysticum. Major central nervous system malformations in South Wales, Part IV. Arch Dis Child 46:127-138, 1971 Lorber J: Results of treatment of myelomeningocele: an analysis of 524 unselected cases, with special reference to possible selection for treatment. Dev Med Child Neural 13:279-303, 1971 Lorber J: Systematic ventriculographic studies in infants born with meningomyelocele and encephalocele. The incidence and development of hydrocephalus. Arch Dis Child 36:381-389, 1961 Matson DD: Surgical treatment of myelomeningocele. Pediatr 42:225-227, 1968 McCullough DC, Luessenhop A J: Evaluation of photoscanning of the diffusion of intrathecal RISA in infantile and childhood hydrocephalus. J Neurosurg 30:673-678, 1969 Morley AR: Laryngeal stridor, Arnold-Chiari malformation and medullary haemorrhages. Dev Med Child Neural 11:471-474, 1969 Peach B: The Arnold-Chiari malformation; morphogenesis. Arch Neural 12:527-535, 1965 Pudenz RH, Russel FE, Hurd HH, et al: Ventriculo-auriculostomy. A technique for shunting cerebrospinal fluid into the right auricle. Preliminary report. J Neurosurg 14:171-179, 1957 Scarff JE: Treatment of hydrocephalus: an historical and critical review of methods and results. J Neural Neurosurg Psychlat 26:1-26, 1963 Schwidde JT: Spina bifida. Survey of two hun-
29.
30. 31. 32. 33.
34.
35.
36.
37.
38.
39.
dred twenty-five encephaloceles, meningoceles and myelomeningoceles. Am d Dis Child 84:35-51, 1952 Sella A, Foltz EL, Shurtleff DB: A three year developmental study of treated and untreated hydrocephalic children, d Pediatr 69:887, 1966 (abstract) Schick RW, Matson DD: What is arrested hydrocephalus? J Pediatr 58:791-799, 1961 Shurtleff DB: Timing of learning. Phys Ther 46:136-148, 1966 Shurtleff DB, Christie D, Foltz EL: Ventriculoauriculostomy-associated infection: a 12year study. J Neurosurg 35:686-694, 1971 Shurtleff DB, Eliason BC, Oakland JA: Congenital brain cysts in infancy: diagnosis, treatment, and follow-up. Teratology 7: 183-190, 1973 Shurtleff DB, Foltz EL: Comparative study of meningomyelocele repair or cerebrospinal fluid shunt as primary treatment in spina bifida. Dev Med Child Neural Suppl 13:57-64, 1967 Shurtleff DB, Foltz EL: Ten year follow-up of 267 myelomeningocele patients, in American Academy of Orthopedic Surgeons, Symposium on Myelomeningocele, St Louis, CV Mosby Co, 1972, pp 282-293 Shurtleff DB, Foltz EL, Chapman JT: Ventriculo-skull distance. Its reliability as an estimate of "cerebral mantle" in the normocephalic child. Am J Dis Child 111: 262-266, 1966 Shurtleff DB, Foltz EL, Loeser JD: Hydrocephalus: a definition of its progression and relationship to intellectual function, diagnosis and complications. Am J Dis Child 125:688-693, 1973 Shurtleff DB, Hayden PW: The treatment of hydrocephalus with isosorbide, an oral hyperosmotic agent. J Clin Pharmacol 12: 108-114, 1972 Shurtleff DB, Hayden PW, Weeks R, et al: Temporary treatment of hydrocephalus and myelodysplasia with isosorbide: preliminary report. J Pediatr 83:651, 1973
This study was supported in part by the National Foundation-March of Dimes, National Institutes of Health Grant FR-37, Public Health Service Grant 99480, Children's Orthopedic Hospital and Medical Center Study R-24-3, and Birth Defects Bequest. This paper was presented in part before the American Association of Neurological Surgeons, Boston, Massachusetts, April 19, 1972. Address reprint requests to: David B. Shurtleff, M.D., Department of Pediatrics, University of Washington School of Medicine, 1959 Pacific Avenue NE, Seattle, Washington 98195.
J. Neurosurg. / Volume 42 / January, 1975
