Idiopathic normal-pressure hydrocephalus. Neurosurgical Service, Massachusetts General Hospital, Boston, Massachusetts

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1 J Neurosurg 52: , 1980 Idiopathic normal-pressure hydrocephalus Results of shunting in 62 patients PETER McL. BLACK, M.D., PH.D. Neurosurgical Service, Massachusetts General Hospital, Boston, Massachusetts v' Of 62 patients given shunts for normal-pressure hydrocephalus of idiopathic type, 46.8% showed some improvement and 27.4% enjoyed virtually complete recovery. The best clinical predictor of good response was the complete triad of memory difficulty, gait disorder, and urine incontinence; 61.2% of patients with this combination of symptoms improved. Gait disturbance alone was also accompanied by improvement in two of three patients. An "obstructive" cisternographic radioisotope pattern was not significantly different from a "normal" pattern in predicting a response to shunting. Computerized tomography (CT) showing large ventricles and little atrophy predicted improvement in 11 out of 13 patients. There were five deaths within 3 months of shunting. The complication rate was 35.4%; subdural collections, shunt malfunction, and postoperative seizures constituted the most frequent complications. These data suggest that continued investigation for better predictions of shunt response is important, but that in the meantime the clinical pattern and cranial CT pattern are the most satisfactory guides to improvement after shunting. KEy WOADS 9 normal-pressure hydrocephalus 9 cerebrospinal fluid shunt 9 dementia I DIOPATHIC normal-pressure hydrocephalus (NPH) is a well recognized cause of dementia and gait disturbance in the elderly. 1 Occasionally, its successful treatment by cerebrospinal fluid (CSF) shunting will transform a hopelessly bedridden and demented patient into a normal human being. More often, such treatment will allow a severely disabled person to achieve significant self-help. Despite examples of improvement after treatment, there is still significant doubt as to which patients should be shunted and what the general results of shunting are. A number of papers have addressed this issue in the last 10 years. Early reports that supported particular diagnostic tests have been supplanted by series with statistically adequate numbers in the last 2 or 3 years, and a consensus appears to be emerging. ~'1~ It therefore seemed appropriate to study, retrospectively, the series of patients shunted for idiopathic NPH at our hospital since the syndrome was first described. Clinical Material and Methods The records of 62 patients who received shunts for NPH at the Massachusetts General Hospital between 1959 and 1977 were reviewed extensively. Some of these patients were included in Ojemann's earlier series, 15 but were re-evaluated completely for the present study. A report on 43 patients has been published in the European literature by Black and Sweet. ~ Patients with known subarachnoid hemorrhage, head trauma, brain tumor, or other recognized specific causes of hydrocephalus were excluded from this investigation. Although precise criteria for shunting varied from surgeon to surgeon, the minimum criteria included enlarged ventricles, a clinical syndrome of dementia and/or gait disturbance, and lumbar puncture pressure under 180 mm H20. Charts were examined for an account of gait difficulty, slowed mentation, bizarre behavior, memory difficulty, incontinence, forced laughing or crying, J. Neurosurg. / Volume 52 / March, ]

2 P. McL. Black paranoia, hallucination, calculation difficulties, aphasia, seizures, hemiparesis, and parkinsonian symptoms. Gait difficulty was considered "severe" if the patient was unable to stand or walk at all or required constant assistance in walking. "Moderate" disability consisted of the ability to walk alone but with a sense of insecurity, a visibly unstable gait, and frequent falls. "Mild" or no disability implied a gait with small or normal steps. Patients had "severe" memory difficulty if they were disoriented, "moderate" if they had noticeable difficulty in daily affairs, and "mild" if they had difficulty demonstrable only on testing. Incontinence was considered either present or absent. Patients were graded by function as follows, using Stein and Langfitt's classification: TM Grade 0, no deficit recognizable by the patient, or his physician or family; Grade I, slight deficit but able to function independently at home; Grade II, some supervision required at home; Grade III, significant impairment requiring some custodial care; Grade IV, full custodial care necessary. The results of cisternographic study classified as "typical NPH" included ventricular entry of isotope, delayed clearance, and failure of convexity ascent at 72 hours. 8,~4 Other patterns were: "'normal" (no ventricular entry, full convexity ascent), and "mixed" (any other pattern). Cranial computerized tomograpby (CT) scan reports were reviewed for comments regarding ventricular enlargement and gyral atrophy; our goal was to assess what the neuroradiologist's reading would predict. Ventricles were considered "enlarged" or "normal." Gyral atrophy was noted as "present" or "absent." Pneumoencephalograms (PEG's) were measured for maximum frontal horn width, callosal angle (junction of the roofs of the frontal horn in the anteroposterior projection), and ascent of air over the convexities. Two methods were used to grade postoperative change: a change in Stein and Langfitt's grading classification, t" and a more detailed categorization by result, as follows: Excellent: resumed pre-illness activity without deficit Good: resumed pre-illness activity with moderate deficit Fair: improved, but no return to previous work Transient: temporary major improvement Poor: no change or worse Dead: deceased within 6 weeks of surgery or as a result of surgery. The general category "improved" was used to include patients with excellent, good, fair, or transient improvement. "No response" described patients who were unchanged or worse. Specific data were obtained by postoperative evaluation in the hospital and at follow-up office appointments, as well as by discussion with patients' families. If any doubt existed about improvement, the patient was put into the lower of the two grades considered. The follow-up period ranged from 9 weeks to 75 months, with a mean of 36.5 months. Fifteen factors were evaluated as possible predictors of shunt outcome: the patient's age; presence of the "classical triad" of dementia, gait disturbance, and incontinence; presence of dementia, gait disturbance, or incontinence, each by itself; preponderance of gait difficulty over other symptoms; memory difficulty greater than gait difficulty; lumbar puncture pressure over 100 mm H20; ventricular span over 55 mm on pneumoencephalography; absence of convexity air on PEG; dilation of cerebral sulci on PEG; cisternographic scan showing ventricular entry and delayed isotope clearance; cisternographic scan showing a mixed pattern; CT scan showing ventricular dilation without sulcal enlargement; CT scan showing ventricular dilation with sulcal enlargement. For statistical analysis, chi-square (x 2) testing was used for factors noted merely as "present" or "absent." Factors directly measured were compared by Student's t-test. When there were fewer than five patients in a group, X 2 with Yates' correction for small numbers was used.' Results Characteristics of the Population There were 62 patients, 32 women and 30 men. The mean age was 67.8 years and the median age 68 years. Fifty-six of these patients had some degree of memory impairment, 53 had gait disturbance, and 34 had urine incontinence. The gait disturbance was most often seen as a short shuffling gait with unsteadiness on turning. Thirtyfour patients had this picture of slowed gait with 4- to 6-inch steps. Four had ataxia without shuffling. Five patients were bedridden, I0 required assistance while walking. Frequent falls were characteristic. Forced laughing or crying, aphasia, paranoia, hallucination, bizarre behavior, or seizures preoperatively were rare, each occurring in one or two patients only. Isotope cisternography was performed in 36 patients, but was technically unsatisfactory in three. The scans in 11 patients had a picture of ventricular entry, delayed clearance, and absence of convexity flow, thought to be typical of NPH; nine were normal; and 13 had a mixed picture. Forty patients had preoperative PEG's; 23 had maximum frontal horn width over 55 mm, whereas in nine it was less than 55 mm; in eight, no specific measurement was cited, and the films could not be reviewed. In 22 patients, CT scans were performed pre- and postoperatively. The preoperative scans showed marked or moderate atrophy as well as enlargement of all ventricles in nine patients. 372 J. Neurosurg. / Volume 52 / March, 1980

3 Idiopathic normal-pressure hydrocephalus Factors Associated with Outcome of Shunting The general results showed that 46.8% of patients were considered improved to some extent by a shunting procedure: 27.4% were able to return to normal work with mild or no deficit, 14.5% had "fair" improvement, and 4.8% were worse; 40.3% were unchanged (Table 1). Stein and Langfitt 18 required an improvement by one functional grade for a patient to be considered a shunt responder. By these criteria, 33% of our patients were shunt responders, and 67% were not. Seven patients (9%) improved by two or more functional grades. Prediction of a Good Response In our attempt to predict a good response, we excluded five patients who died before adequate evaluation could be carried out. Further, the groups used were "improved" versus "not improved" groups; thus, "excellent," "good," and "fair" results were combined in an "improved" group. Among clinical factors, the age of the patient, degree of deficit, and duration of disability were all irrelevant to shunt outcome. The presence of mild memory difficulty, significant gait difficulty, and incontinence (the "classical triad" of Adams, et al., a) was the best clinical guarantee of good outcome; of 31 patients with this constellation, 38.7% returned to normal activity, and 22.6% more made some recovery: a total of 61.2% improved. Nineteen patients without incontinence had only 10.5% good improvement and 21.1% fair, with a total of 31.6% improvement generally. Two of three patients with gait trouble as their only symptom improved markedly; the one patient with dementia as his only deficit did not. Patients with dementia as the predominant symptom did not fare differently overall than those with predominantly gait disturbance in improvement of some kind. However, more patients with primarily gait disturbance returned to normal than those with dementia as their major problem. Patients in whom dementia and gait disturbance were considered equal did more poorly than those with a predominance of one or the other (Table 2). Among radiological examinations (Table 3), the PEG was useful primarily to show ventricular dilation. The callosal angle and presence of dilated sulci were not predictive of a good result. Four of five patients who deteriorated after PEG improved after shunting; however, there was in general no significant difference in shunt response between those with adverse reactions to PEG and those without. The cisternographic radioisotope study showed a pattern typical of NPH in 11 patients; 73% of these improved. A normal pattern, in nine patients, had a 55% improvement rate. The mixed pattern had 31% improvement. These differences were not significant by X 2 testing. TABLE 1 Categories of improvement after shunting in 62 patients with idiopathic normal-pressure hydrocephalus Category Percent excellent (return to normal activity) 12.9 good (normal activity, slight deficit) 14.5 fair (improvement but not to normal) 14.5 transient improvement 4.8 total improved 46.7 unchanged 40.3 worse 4.8 dead 8.1 total unchanged or worse 53.2 The CT scan showed enlarged ventricles with little atrophy in 13 patients; 85% of those improved. Of nine patients with significant atrophy, only 33% improved. These are significant differences (x 2, p < 0.05) (Table 4). Predicting a Poor Response Thirteen of 19 patients with dementia and gait disturbance alone had little response to shunting (p < 0.05, Eight of nine patients with maximum ventricular span of less than 55 mm had no response (p < 0.01, x2). Six of nine patients with sulcal enlargement on CT had no response. Complications of Shunting Procedures Among the 62 primary procedures, there were 57 ventriculoatrial and five ventriculoperitoneal shunts. All but two involved a medium-pressure Hakim valve. There were 74 shunt procedures in all, including revisions or ligations. Seven shunts required revision, four of them electively, because shunt films showed the ventricular catheter in suboptimal position. One patient fell and developed an acute subdural hematoma several weeks after the shunt; six others had delayed subdural collections that required drainage and/or shunt ligation. All the chronic collections were treated satisfactorily. Four patients without preoperative seizures had seizures within the first 6 months of shunting, all easily controlled with anticonvulsant drugs. Three patients had transient neurological disturbances: diplopia, tremor, and aphasia. Two developed pneumonia, and one with a ventriculoperitoneal shunt had transient pulmonary edema of unknown cause. There were five deaths within 3 months of surgery. Three occurred within the first month: a myocardial infarction the day after operation, multiple pulmonary emboli, and aspiration pneumonia following continued obtundation after a shunt. Two patients died later: one had a left middle cerebral infarct 5 days postoperatively and died several weeks later; the other J. Neurosurg. / Volume 52 / March,

4 TABLE 2 The effect of clinical factors on shunt outcome in idiopathic normal-pressure hydrocephalus (deaths excluded) P. McL. Black Good or No. of Excellent Fair Total No Clinical Factors Patients Response Response Improved Response No. Percent factors present: the triad (dementia, gait difficulty, & incontinence) dementia & gait disturbance gait disturbance only dementia only 1 insufficient data 3 duration of symptoms: over 1 year months to 1 year less than 3 months duration unknown 13 prominence of gait disturbance: gait difficulty main problem dementia main problem gait & dementia equal insufficient data 3 degree of disability" dementia severe moderate none gait disturbance severe moderate mild none urine incontinence with without No. Percent No. Percent No. Percent 22, was found to be unresponsive after a shunt revision and never recovered. Discussion The Syndrome of Idiopathic Normal-Pressure Hydrocephalus Although there is disagreement about the best predictors of shunt response in patients with idiopathic NPH, there appears to be general agreement about what constitutes the syndrome. Conceptually, it is said to result from an obstruction to convexity cerebrospinal fluid (CSF) flow with resultant chronic ventricular enlargement) Clinically, it is a syndrome marked by one or more of the triad of dementia, gait disturbance, and incontirience, with radiological ventricular enlargement and no severe gyral atrophy; and a lumbar puncture pressure less than 180 mm H20. There should also be no known cause for these findings. By these criteria all patients shunted in this series had some form of idiopathic NPH. They therefore represent a typical group of patients whom neurologists or neurosurgeons might consider shunting. A recent series from the Mayo Clinic supports the similarity of the population of patients with idiopathic NPH at two large centers? ~ In general, it is a relatively rare disorder of older people seen about l0 times a year on a large neurosurgical service. General Results The results reported after shunting for idiopathic NPH varied widely in the early years of the syndrome depending upon the selection criteria used for shunting and the assessment scale used for evaluation. Early reports with small numbers may have been overly optimistic. Using a variety of criteria, it now seems that 20% to 30% of patients will be markedly improved after a shunt, and that 40% to 70% will be improved to some extent. ~,8,1~176 These figures, which agree with our improvement rates of 27.4% and 46.8%, respectively, are remarkably consistent over a large number of clinical reports. They suggest that marked improvement, which at times may seem almost miraculous, is 374 J. Neurosurg. / Volume 52 / March, 1980

5 Idiopathic normal-pressure hydrocephalus TABLE 3 Pneumoencephalographic and cisternographic findings in patients with idiopathic normal-pressure hydrocephalus* Excellent Fair or Radiographic Studies No. of Cases or Good Response Transient Response Total Improved No Response to Shunt Signifi- No. Percent No. Percent (percent) No. Percent cancer Pneumoencephalogram ventricle span (max) over 55 mm N.S. under 55 mm 9 1 I callosal angle over 120 ~ I N.S. under 120 ~ cerebral sulci dilated N.S. nondilated reaction to PEG severe mild N.S. none Cisternogram "typical" of NPH N.S. "normal" N.S. mixed pattern N.S. unsatisfactory 3 *Deaths resulting from shunting have been excluded. tn.s. = not significant. still achievable in only one-quarter of patients who are being shunted. Predicting Good Shunt Outcome Recent studies suggest that neurosurgeons lack predictors of good shunt outcome. Stein and Langfitt's observations 18 on 23 patients eschewed any clinical or radiological features as reliable. However, their criteria for shunt placement were less stringent than those used here. Their results were graded by functional improvement, which may not be the most relevant method, and their numbers were small. Laws and Mokri 12 and Shenkin and Greenberg x7 have published reports of larger patient groups. From these series, there appears to be some consensus about predictive factors. The Clinical Picture. Two points emerge in the analysis of clinical factors in predicting shunt outcome. One is that having the classical triad of idiopathic NPH appears to increase the chances of good results from shunting: in the Mayo Clinic experience, 74% of 19 patients with the triad showed some improvement. 12 In our series, 19 of 31 patients with it (67.2%) improved. This compares with 31.6% improving with dementia and gait disturbance alone. This significant difference suggests that the original triad was the appropriate clinical picture, and that better results are seen overall if operation is restricted to patients with all three components. TABLE 4 Computerized cranial tomography findings and results of shunting in patients with idiopathic normal-pressure hydrocephalus Excellent Fair or Computerized No. of or Good Transient No Total Signifi- Tomography Cases Response Response Response Improved cance* Findings (percent) No. Percent No. Percent No. Percent ventricle enlargement with little or no sulcal enlargement 13 5 ventricle enlargement with concomitant sulcal enlargement 9 2 *N.S. = not significant p < N.S. J. Neurosurg. / Volume 52 / March,

6 A possible exception is predominant gait disturbance. We do not have enough patients without gait difficulty to estimate whether it is necessary to have gait disturbance to achieve success; Jacobs has suggested that it is. a~ However, it does appear that our series agrees with others in suggesting that prominent gait disturbance predicts a good outcome) '~ The role of incontinence in our series should be underscored; without it, only 31% improved. Our finding that age, duration of symptoms, and degree of disability before the shunt did not affect the outcome agrees with other reports, a~ Shenkin and Greenberg's claim that duration of symptoms was not important is of interest because it reflected a change from their experience with smaller to larger series, and emphasizes the importance of having adequate numbers.17 Radiographic Findings. The PEG, once important in demonstrating the ventricular enlargement of idiopathic NPH, did not appear to be generally useful in predicting shunt response. Our finding that the callosal angle was not helpful agrees with the other large series, 1~176 although smaller series found it useful. We found, as did Salmon TM and Greenberg, et al., 6 that marked ventricular dilation (over 55 mm) gave slightly better results. Somewhat surprising was our finding, which also agreed with Salmon's work, that the presence of atrophy on PEG did not prevent a good result. We did not assess temporal-horn dilation. The radioiodinated serum albumin (RISA) study tended to reflect outcome of shunting in a general way; patients with a study showing ventricular stasis and failed convexity ascent did better than those with a more normal pattern. However, these differences did not reach statistical significance. The CT scan has largely replaced the PEG for assessment of ventricular size. Our data suggest that CT scanning holds significant promise in the prediction of shunt outcome. We relied on the reading of various neuroradiologists in the present study to assess sulcal dilation and ventricular enlargement: their reading is that marked atrophy makes significant difference, as do enlarged ventricles. This agrees with previous reports that CT may predict shunt results, 7 although Laws and Mokri TM believed that atrophy was not a significant predictor of poor response. It would be economical and satisfying to be able to use the CT scan to predict the results of shunting as accurately as with other more cumbersome techniques. The present data suggest that this will be possible. Pressure Measurements. A single lumbar puncture pressure appears unhelpful in prognostication except to establish that such pressure is sometimes in the normal range. Good results were comparable for patients with an opening pressure of less than 100 mm H~O and for patients with an opening pressure of over 100 mm H20. This may reflect the limited reliability of a single pressure reading in revealing the CSF dynamics. P. McL. Black Several authors have suggested that continuous pressure monitoring might be useful in prediction of shunting outcome: a,~9 however, the studies are not controlled, nor are there enough to make statements about its usefulness. In six patients in our series such pressure monitoring was quite unhelpful) Conclusions There seems to be general agreement that patients with minimally enlarged ventricles are not likely to be helped by shunt placement. 1,6,9,~1,~8 There is also agreement amongst most neurosurgeons that patients with dementia alone are less likely to respond to shunting, although there are enough exceptions to make this an unreliable guideline. 2,~1,18 The reported incidence of complications of shunt surgery in this elderly population should give pause to anyone who feels he has nothing to lose by shunting an elderly patient. Our incidence of 35.4% compares closely with 37.5% reported by Laws and Mokri, 1~ 41% by Udvarhelyi, et al., 2~ and 32.8% by Greenberg, et al. 6 The major complication is shunt malfunction, which should be suspected in any patients whose ventricles do not diminish in size postoperatively, and whose lumbar puncture pressure remains above 80 mm H20. Cranial CT scanning has made this possibility much easier to assess, and also helps to pick up the second complication, subdural collection. This can usually be treated by shunt ligation, but remains an important source of morbidity) '1~'~3 McCullough and Fox la have outlined the pressure differentials that may lead to it. Seizures, unknown in mechanism, are frequent enough to suggest the use of anticonvulsant prophylaxis, although this has not been our practice. Transient neurological disturbance may be related either to shunt catheter placement or to sudden changes in CSF dynamics. The operative deaths are primarily effects of anesthesia in this elderly and sometimes fragile population. They are again a reminder that an operation that promises hope can sometimes result in tragedy, and that the search for better prognostic criteria is an exceedingly important one in the surgical treatment of idiopathic NPH. Acknowledgments I would like to thank Dr. Nicholas Zervas, Chief of the Neurosurgical Service, Massachusetts General Hospital, who provided encouragement and help in the preparation of this manuscript, and Dr. William H. Sweet, former Chief of that service, who extracted chart data on 28 of the 62 patients as part of an earlier paper. References 1. Adams RD, Fisher CM, Hakim S, et al: Symptomatic occult hydrocephalus with "normal" cerebrospinal fluid pressure. A treatable syndrome. N Engl J Med 273: , J. Neurosurg. / Volume 52 /March, 1980

7 Idiopathic normal-pressure hydrocephalus 2. Black PM, Sweet WH: Normal pressure hydrocephalus -- idiopathic type selection of patients for shunting procedures, in W~illenweber R, Brock M, Hamer J (eds): Lumbar Disc. Adult Hydrocephalus. Vol 4: Advances in Neurosurgery. Berlin/Heidelberg/New York: Springer-Verlag, 1977, pp 106-I10 3. Chawla JC, Hulme A, Cooper R: Intracranial pressure in patients with dementia and communicating hydrocephalus. J Neurosurg 40: , Croxton FE: Elementary Statistics with Applications in Medicine and Biological Sciences. New York: Dover, Fisher CM: The clinical picture in occult hydrocephalus. Clin Neurosurg 24: , Greenberg JO, Shenkin HA, Adam R: Idiopathic normal pressure hydrocephalus -- a report of 73 patients. J Neurol Neurosurg Psychiatry 40: , Gunasekera L, Richardson AE: Computerized axial tomography in idiopathic hydrocephalus. Brain 100: , Heinz ER, Davis DO, Karp HR: Abnormal isotope cisternography in symptomatic occult hydrocephalus. A correlative isotopic-neuroradiological study in 130 subjects. Radiology 95: , Illingworth RD: Subdural haematoma after the treatment of chronic hydrocephalus by ventriculocaval shunts. J Neurol Neurosurg Psychiatry 33:95-99, Jacobs L, Conti D, Kinkel W, et al: "Normal-pressure" hydrocephalus. Relationship of clinical and radiographic findings to improvement following shunt surgery. JAMA 235: , Jacobs L, Kinkel W: Computerized axial transverse tomography in normal pressure hydrocephalus. Neurology 26: , Laws ER Jr, Mokri B: Occult hydrocephalus. Results of shunting correlated with diagnostic tests. Cliu Neurosurg 24: , McCullough DC, Fox JL: Negative intracranial pressure hydrocephalus in adults with shunts and its relationship to the production of subdural hematoma. J Neurosurg 40: , McCullough DC, Harbert JC, Di Chiro G, et al: Prognostic criteria for cerebrospinal fluid shunting from isotope cisternography in communicating hydrocephalus. Neurology 20: , Ojemann RG: Normal pressure hydrocephalus. Clio Neurosurg 18: , Salmon JH: Adult hydrocephalus. Evaluation of shunt therapy in 80 patients. J Neurusurg 37: , Shenkin HA, Greenberg J, Bouzarth WF, et al: Ventricular shunting for relief of senile symptoms. JAMA 225: , Stein SC, Langfitt TW: Normal pressure hydrocephalus. Predicting the results of cerebrospinal fluid shunting. J Neurosurg 41: , Sym0n L, Hinzpeter T: The enigma of normal pressure hydrocephalus: tests to select patients for surgery and to predict shunt function. Clin Neurosurg 24: , Udvarhelyi GB, Wood JH, James AE Jr, et al: Results and complications in 55 shunted patients with normal pressure hydrocephalus. Surg Neuroi 3: , 1975 Address reprint requests to: Peter McL. Black, M.D., Neurosurgical Service, Massachusetts General Hospital, Boston, Massachusetts J. Neurosurg. / Volume 52 / March,

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