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(Stroke. 1996;27:24-29.)
© 1996 American Heart Association, Inc.
Articles |
Vascular Risk Factors and Arteriosclerotic Disease in Idiopathic Normal-Pressure Hydrocephalus of the Elderly
From the Departments of Neurosurgery (J.K.K., J.P.R., J.J.B.) and Neurology (D.W.D., T.M.) and the Institute of Medical Biometry and Medical Informatics (W.V.), Albert-Ludwigs-Universität, Freiburg, and the Department of Neurology (D.W.D.), Medizinische Universität zu Lübeck, Lübeck, Germany.
Correspondence to Joachim K. Krauss, MD, Department of Neurosurgery, Baylor College of Medicine, 6560 Fannin, Suite 944, Houston, TX 77030.
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Abstract |
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 Top Abstract IntroductionSubjects and Methods Results Discussion References |
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Background and Purpose There is some evidence from previous studies that idiopathic normal-pressure hydrocephalus (NPH) of the elderly might be linked to vascular leukoencephalopathy. The purpose of this study was to examine the prevalence and impact of vascular risk factors and vascular diseases in idiopathic NPH compared with a control cohort.
Methods The prevalence of arterial hypertension; diabetes mellitus; hypercholesterolemia; hyperlipidemia; smoking; obesity; and cardiac, cerebrovascular, and other arteriosclerotic diseases was assessed in 65 patients with idiopathic NPH. The findings were compared with those of 70 patients with comparable age distribution. To describe the differences of the prevalences of vascular risk factors, odds ratios were obtained by univariate and multivariate analyses.
Results The univariate analysis revealed significant associations between idiopathic NPH and arterial hypertension (prevalence, 54 of 65 [83%]; control group, 25 of 70 [36%]; P<.001) and diabetes mellitus (prevalence, 31 of 63 [49%]; control group, 20 of 70 [29%]; P<.015) but not with other vascular risk factors. After multivariate regression analysis, only hypertension remained significantly associated with NPH (P<.0001). There was also a significant association between NPH and cardiac (P<.001), cerebral arteriosclerotic (P=.007), and other arteriosclerotic diseases (P=.001). A positive association was found between the severity of clinical symptoms of NPH and the presence of hypertension, especially for gait disturbance. The presence of hypertension was not related to the duration of NPH.
Conclusions Our data show a highly significant association between idiopathic NPH and arterial hypertension. Arterial hypertension might be involved in the pathophysiological mechanisms promoting idiopathic NPH.
Key Words: arteriosclerosis • elderly • hydrocephalus • hypertension • risk factors
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Introduction |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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The diagnosis of NPH is raised in hydrocephalic patients presenting with gait disturbance with or without dementia and/or urinary urgency or incontinence.1 2 Approximately 30% to 70% of cases are secondary to known causes such as subarachnoid hemorrhage, meningitis, or head trauma.3 4 The etiology of idiopathic NPH of elderly patients, however, remains unclear and is the subject of controversial debate.5 6 7 While defective CSF absorption has been considered to be the priming event in the pathophysiology of idiopathic NPH, there is little evidence from recent investigations to support this hypothesis.8
The benefit of shunt surgery is contingent on the preoperative selection of patients.9 The differential diagnosis between NPH and vascular encephalopathy may be problematic, as Binswanger's encephalopathy and idiopathic NPH share common clinical features.10 On the other hand, several cases with coexisting hypertensive cerebrovascular disease and idiopathic NPH have been reported.11 12 13 14 Furthermore, it has been postulated that vascular lesions of the deep white matter might actually cause idiopathic NPH.5 11
The occurrence of vascular risk factors has occasionally been reported in elderly patients with idiopathic NPH. However, few studies have determined their frequency.3 15 16 17 18 Graff-Radford and Godersky15 reported that arterial hypertension was prevalent in 14 of 19 patients with idiopathic NPH and in 38 of 142 control subjects, which differed significantly. Casmiro et al16 found a statistically significant difference for arterial hypertension, diabetes, and ischemic heart disease in a group of 17 patients with idiopathic NPH compared with control subjects. However, only 4 of 17 patients were subsequently shunted.
Since the relative frequency of vascular risk factors and arteriosclerotic disease in shunt-responsive idiopathic NPH of the elderly has not been assessed in a large series of patients, we investigated the prevalence and impact of certain vascular risk factors and cardiac and arteriosclerotic diseases in a group of 65 patients suffering from idiopathic NPH and compared the findings with those of a control cohort with comparable age distribution.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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One hundred eighteen patients with chronic adult hydrocephalus were examined between January 1989 and November 1994 at the Department of Neurosurgery to identify those who might benefit from shunting. Cranial CT and MR scans were routinely obtained. All patients were submitted to overnight recordings of intracranial CSF pressure and hydrodynamic studies in which the bolus technique was used.19 Further investigations included removal of CSF by lumbar puncture or ventricular drainage, dynamic MR investigations,20 21 polysomnography,22 and transcranial Doppler monitoring.23 24
The diagnosis of idiopathic NPH was made in 65 patients who fulfilled the following diagnostic criteria: clinical presentation of NPH consisting of gait disturbance with or without dementia and/or urinary incontinence, ventricular enlargement, and the absence of cortical atrophy. Flattening of the cerebral sulci over the parasagittal convexity was found in all but 4 patients. Marked clinical improvement of the gait disorder as assessed by two independent observers after lumbar or ventricular removal of CSF was assumed to be confirmatory for the diagnosis of NPH. Hydrodynamic studies were considered to be indicative for NPH in patients with a pressure-volume index of 13 mL or less and a resistance to outflow greater than 12 mm Hg/mL per minute.19 25 CSF pressure monitoring was thought to be compatible with the diagnosis of NPH in patients with a baseline CSF pressure in the upper normal range (12 to 20 cm H2O), an occurrence of B waves during at least 70% of the recording time, and the presence of ramp-type and/or other high-amplitude B waves. White matter lesions were not considered to be a contraindication for shunting. Patients with a history of events known to cause secondary NPH were excluded.
Functional disability was graded according to a modification of the scale of Stein and Langfitt26 : 0, no deficits; I, minimal deficits, no functional disability; II, some help or supervision required; III, considerable help or supervision required; and IV, no independent functional capacity.
Routine examination on admission included complete physical examination, routine laboratory tests, chest x-ray, and a standard electrocardiogram. Blood pressure was measured at least three times daily. Vascular risk factors and cardiac and arteriosclerotic diseases were assessed according to the patients' histories, information provided by the family and referring doctors, previous clinical reports, and additional investigations on admission. For statistical analysis items were assigned to be either present or absent.
Risk factors and cardiac and arteriosclerotic diseases were assessed by nine binary variables. The variables were defined as follows: (1) arterial hypertension: documented history and treatment for hypertension, or blood pressure measures more than 160 mm Hg systolic and/or 90 diastolic on at least two different measurements. Subcategories included (a) medication with antihypertensive drugs and (b) blood pressure exceeding limits as defined above during observation; (2) diabetes mellitus: documented history and treatment for diabetes, or fasting serum glucose levels above 6.7 mmol/L. Subcategories included (a) treatment with oral antidiabetic drugs, (b) treatment with insulin, and (c) fasting glucose exceeding limit as indicated above; (3) hypercholesterolemia: fasting total cholesterol levels exceeding 5.2 mmol/L; (4) hyperlipidemia: fasting triglyceride level above 1.6 mmol/L; (5) smoking: previous or present habits of cigarette smoking; (6) obesity: body mass index (weight/height2) exceeding 27 kg/m2; (7) cardiac diseases: documented history and treatment, or present on admission with the subcategories (a) cardiac insufficiency, (b) valvular disease, (c) symptomatic arrhythmia, (d) myocardial infarction, and (e) symptomatic or asymptomatic electrocardiogram-documented ischemic heart disease; (8) cerebrovascular arteriosclerotic diseases: documented history of (a) transient ischemic attacks, (b) ischemic stroke, and (c) stenosis of extracranial cerebral arteries; and (9) other arteriosclerotic diseases (excluding categories 7 and 8): documented history of retinal, renal, aortic, iliac, or peripheral arteriosclerosis.
The control group consisted of 70 preoperative neurosurgical patients older than 60 years who were operated on in the Department of Neurosurgery between 1991 and 1993 selected at random from three groups: those with small cerebellopontine angle tumors (8 patients), pituitary adenomas (22), and lumbar and cervical spinal disc disease (40).
ORs obtained by univariate and multivariate analyses were used to describe the differences of the prevalences between patients with NPH and the control group. Furthermore, ORs were calculated for associations between other binary variables. The corresponding probability values refer to the Cochran-Mantel-Haenszel test. Calculations were done with SAS statistical software. To also include subjects with incomplete covariate information in the logistic regression analysis, a procedure described recently by Vach and Blettner27 was used. Statistical significance was declared at the P<.05 level.
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Results |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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The mean age of the 65 patients with idiopathic NPH was 70.8±7.4 (SD) years, with a range from 50 to 87 years. Thirty patients were men (46%) and 35 were women (54%). The mean age of patients from the control group was 69.3±5.9 (SD) years, with a range from 60 to 83 years. Twenty-eight patients were men (40%), and 42 were women (60%).
Fifty-two patients with idiopathic NPH underwent ventriculoatrial or ventriculoperitoneal CSF diversion. Fifty patients were followed for a mean of 19.4 months; in 2 patients no long-term follow-up was available.
A gait disturbance was present in all NPH patients, mental impairment in 64 of 65 (98%), and urgency or urinary incontinence in 54 of 65 (83%); 53 of 65 patients presented with all three symptoms (82%). When these symptoms were assessed and assigned to two categories according to the degree of the impairment (mild/normal versus severe/marked), the following distributions were found. The gait disturbance was mild (cautious gait or impaired tandem gait) in 12 of 65 patients (18%) and severe/marked (unaided gait not possible or considerable unstable gait) in 53 of 65 (82%). Mental impairment was mild/normal (well oriented, some memory or attention deficits) in 26 of 65 patients (40%) and severe/marked (disoriented or considerable memory/attention deficits) in 39 of 65 (60%). Urinary incontinence was graded as mild/absent (sporadic or no incontinence) in 29 of 65 patients (45%) and as severe/marked (permanent or frequent) in 36 of 65 (55%). Functional disability was graded as 0 in 0 of 65 patients (0%), I in 8 of 65 (12%), II in 17 of 65 (26%), III in 19 of 65 (29%), and IV in 21 of 65 (32%).
The diagnosis of idiopathic NPH was designated as "definite" in all patients who showed prolonged clinical improvement after probatory CSF removal or who improved after shunting (54 of 65 patients [83%]) and as "probable" in the remaining 11 patients (11 of 65 [17%]). All patients of the latter group fulfilled the criteria for idiopathic NPH as indicated above; however, a shunt operation was refused by 3 patients or their relatives (3 of 65 [5%]), 3 other patients who were scheduled for a shunt operation died from other diseases (3 of 65 [5%]), and 5 did not benefit from shunting (5 of 65 [8%]).
The variables arterial hypertension and cardiac,
cerebral arteriosclerotic, and other
arteriosclerotic diseases could be evaluated in all
patients (Table 1
). Laboratory investigations for
cholesterol and triglycerides, however, were
available in subpopulations of 38 of 65 (58%) and 32 of 65 patients
(49%), respectively. Reliable information on smoking habits could be
obtained from 49 of 65 patients (75%) and on diabetes from 63 of 65
(97%). The distribution of vascular risk factors and cardiac and
arteriosclerotic diseases in patients with
idiopathic NPH was comparable between the subgroups of definite (54 of
65) and probable (11 of 65) NPH.
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The relative frequencies of vascular risk factors and cardiac and
arteriosclerotic diseases as defined by
variables and subcategories are summarized in Table 1
.
Arterial hypertension was found in 83% of patients with
idiopathic NPH. Among the 54 patients with arterial
hypertension, 39 (72%) were treated with antihypertensive drugs,
whereas 15 patients (28%) did not receive specific treatment when they
were admitted. Arterial hypertension was controlled in only
15 of 54 patients (28%). There was a high prevalence of diabetes
mellitus (31 of 63 patients [49%]). Cardiac diseases were detected
in 46 of 65 patients (71%). The prevalence of ischemic heart
disease was 57% (37 of 65), that of cerebral
arteriosclerotic disease 32% (21 of 65), and that
of other arteriosclerotic diseases 35% (23 of
65).
Data on the variables hypercholesterolemia
and hyperlipidemia were available for subpopulations of
the control group that were similar in size to the subpopulations with
NPH: 39 of 70 (56%) and 38 of 70 control subjects (54%), respectively
(Table 2).
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The prevalence of vascular risk factors and cardiac and
arteriosclerotic diseases in the control group was
as follows: arterial hypertension in 25 of 70 patients
(36%) and diabetes in 20 of 70 patients (29%). The frequency of
cardiac diseases was 39%, of cerebral
arteriosclerotic diseases 13%, and of other
arteriosclerotic diseases 11% (Table 2).
To compare the relative frequencies of vascular risk factors between
patients with idiopathic NPH and the control group, a
univariate analysis was performed to calculate ORs
and to determine statistically significant differences (Table
3). This analysis revealed a highly significant
association of arterial hypertension (P<.001)
and a weaker although significant association of diabetes mellitus
(P=.015) with idiopathic NPH (Table 3). No
significant
differences were found for the other vascular risk factors.
Furthermore, there was a highly significant association between the
prevalence of cardiac (P<.001), cerebrovascular
(P=.007), and other arteriosclerotic
diseases (P=.001) with idiopathic NPH.
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To assess potential relationships between the various vascular risk factors we determined ORs for combinations of the variables arterial hypertension, diabetes mellitus, hypercholesterolemia, hyperlipidemia, smoking, and obesity for both groups. A strong association for diabetes mellitus and arterial hypertension was found, with an OR of 3.2 (95% CI, 1.3 to 7.5).
A multivariate analysis in which a logistic
regression was used was applied to clarify whether the differences in
the prevalences of single vascular risk factors were independent of
each other or whether they could be explained by possible associations
between the different risk factors. The results of this
analysis are presented in Table 3. The adjusted values
revealed that the association of hypertension with NPH remained highly
significant (P<.0001). Because of the strong association
between diabetes mellitus and hypertension, however, it was not
possible to show a significant effect of diabetes mellitus
(P=.12), although the adjusted OR (2.1) is only slightly
smaller than the unadjusted one (2.4). The multivariate
analysis also suggests a possible association between
hypercholesterolemia and NPH
(P=.06).
We also investigated and compared the subgroups from both collectives with cardiac, cerebrovascular arteriosclerotic, and/or other arteriosclerotic diseases. Among those 90 patients (54 NPH patients, 36 control subjects), an association between hypertension and NPH was also established by an OR of 5.8 (95% CI, 2.2 to 15.0; P<.001) and an adjusted OR of 8.1 (95% CI, 2.5 to 26.5; P<.001). For diabetes the adjusted OR was 2.5 (95% CI, 0.8 to 7.2; P=.17).
Possible relationships between the clinical presentation
and arterial hypertension and diabetes were
analyzed in the group of patients with NPH. A positive
association is recognized between a severe/marked degree of impairment
in relation to all three cardinal symptoms and arterial
hypertension (Table 4). The strongest association is
demonstrated between marked/severe gait disturbance and
arterial hypertension. Similarly, a positive yet somehow
weaker association exists between arterial hypertension and
a functional disability score of III or more (Table 4). The
association
of the severity of the cardinal symptoms with diabetes mellitus was
much weaker (Table 4). No consistent associations were found
when the other vascular risk factors were examined.
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Patients with NPH were assigned to three groups according to the
duration of the disease after onset of the first symptoms to
investigate whether duration of the disease had an impact on the
presence of hypertension or diabetes (Table 5). As
demonstrated, neither the frequency of hypertension nor that of
diabetes increased with the duration of the symptoms of NPH.
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Discussion |
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TopAbstractIntroductionSubjects and Methods Results Discussion References |
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Our study demonstrates a highly significant association between idiopathic NPH and systemic arterial hypertension. There are also potential associations between idiopathic NPH and diabetes mellitus and between idiopathic NPH and hypercholesterolemia. Furthermore, the data suggest that patients with idiopathic NPH suffer more frequently from cardiac and arteriosclerotic diseases than control subjects with comparable age distribution.
It is essential to note that diagnostic criteria for idiopathic NPH are not consistent in different studies.2 9 16 28 29 30 Confirmation of a suspected diagnosis of idiopathic NPH that has been set forth according to the clinical presentation of the patient should be mandatory. The diagnosis is proven only in those patients who show unequivocal improvement after shunting; however, conversely it is not possible to state that patients who do not improve do not suffer from NPH. Considering these aspects, we started our analysis by comparing the two subgroups of our collective with definite and probable NPH. This did not reveal a different distribution of the variables that were evaluated.
According to the criteria used for the diagnosis of NPH, we believe that our series of 65 patients is a representative sample of idiopathic NPH of the elderly.
Arterial hypertension was a consistent feature in the majority of elderly patients suffering from idiopathic NPH. Eighty-three percent of our patients with idiopathic NPH presented with a history of arterial hypertension or had high blood pressure on admission, which markedly contrasted with the prevalence of 36% in the control group. The significance of this difference is also evident when the ORs for possible relationships between different factors are adjusted with the logistic regression model. Furthermore, this association can be established in those patients with cardiac, cerebrovascular, and/or other arteriosclerotic diseases. This finding lends further support to the possibility that hypertension might be an independent risk factor for NPH. A history of arterial hypertension or the presence of hypertensive vascular encephalopathy had been previously described in several patients with idiopathic NPH.1 11 12 13 14 18 31 Graff-Radford and Godersky15 were the first to assess the prevalence of arterial hypertension in a small series of 19 patients with idiopathic NPH. Although their criteria for assigning patients to the hypertensive group differed from ours, 74% of their patients with idiopathic NPH had arterial hypertension, which is similar to the 83% in our series. A highly significant association between NPH and arterial hypertension was also reported by Casmiro et al.16 Among the several possibilities that might explain the association of idiopathic NPH and hypertension, Graff-Radford and Godersky15 hypothesized that it was most likely that hypertension actually might contribute to the pathogenesis of NPH; however, their data did not allow them to rule out the possibility that NPH could cause hypertension. If NPH could cause hypertension, more patients should be expected to develop hypertension with progression of hydrocephalus. The fact that arterial hypertension was not related to the duration of idiopathic NPH in our study does not support this possibility. The association between arterial hypertension and marked/severe symptoms and a higher disability score is remarkable. These findings allow several interpretations. It is conceivable that these patients have a more severe form of coexistent vascular encephalopathy. On the other hand, it is also possible that hypertension might speed up the progression of the disease.
The association of idiopathic NPH with diabetes mellitus has received less attention.16 17 The prevalence of 49% in the NPH group is significantly different from the prevalence of 29% in the control group. These figures are similar to those of Jacobs,17 who investigated the association of NPH and diabetes in 1977. Jacobs found a significantly higher prevalence of 51.5% (17 of 33 patients) in idiopathic NPH compared with 12.1% in age-matched control subjects. However, he did not report on the prevalence of arterial hypertension in his study group. We found a strong association between arterial hypertension and diabetes since most patients who presented with diabetes also suffered from arterial hypertension. Hence, the multivariate analyses do not allow us to establish diabetes as a risk factor independent of hypertension. Nevertheless, diabetes may be involved in the development of vascular encephalopathy in patients with NPH.
The comparative analysis for the relative frequency of hyperlipidemia and hypercholesterolemia between patients with idiopathic NPH and control subjects should be interpreted with caution. Although the size of subpopulations in both cohorts was similar, the results may be biased by the incomplete sample volumes. The results of the multivariate analysis suggest a potential association between hypercholesterolemia and idiopathic NPH. We did not investigate for subfractions of cholesterol. It is of interest that Casmiro et al16 previously described an association between low high-density lipoprotein cholesterol levels and NPH. Our study does not suggest relevant associations between hyperlipidemia, obesity, or smoking and idiopathic NPH.
Only few data are available on the prevalence of arteriosclerotic disease in patients with idiopathic NPH. Casmiro et al16 described a strong association between idiopathic NPH and ischemic heart disease, and Graff-Radford and Godersky15 reported on electrocardiographic abnormalities in 16 of 19 patients. The significant association of cardiac, cerebrovascular, and other arteriosclerotic diseases with idiopathic NPH in our series may have various implications. Whether these accompanying diseases are only secondary to the high prevalence of vascular risk factors or whether cardiac and cerebrovascular diseases might additionally contribute to the development of idiopathic NPH in some cases awaits further clarification. Nevertheless, our analysis of subgroups with vascular diseases allows us to exclude the possibility that the association of arterial hypertension and NPH is explained merely by the dependence between hypertension and vascular diseases on the one hand and the dependence between vascular diseases and NPH on the other.
Arterial hypertension may promote the development of idiopathic NPH in various ways. The association between arterial hypertension and white matter lesions is well known.10 32 There is some evidence that vascular lesions of the periventricular and the deep white matter might be involved in the pathophysiology of idiopathic NPH.5 11 33 O'Connell34 was the first to suggest that white matter lesions could predispose subjects to the development of hydrocephalus. Earnest et al11 hypothesized that hypertensive vascular disease might be the initial pathological event in some patients with NPH. Bradley et al5 described a significant association of deep white matter lesions with NPH according to MR studies. White matter lesions could reduce periventricular tissue strength and alter the elastic properties, thus predisposing the ventricles to dilate under the CSF pulse pressure.35 36 Thus, defective CSF absorption would rather be a consequence in these patients.11 Ongoing clinical deterioration most probably results from decreased periventricular blood flow.9 37 In accordance with this hypothesis, it has been shown that periventricular cerebral blood flow is increased in some patients who improved after shunting.38
The hypothesis that idiopathic NPH might be secondary to vascular encephalopathy, however, is still unproved and not uniformly accepted.6 7 In particular, the criteria for the diagnosis of idiopathic NPH in the study of Bradley et al5 have been questioned.6 7 Concerning periventricular lesions in NPH, it remains unclear whether these are a cause or a result of hydrocephalus.6 The possibility should also be considered that vascular encephalopathy might be only an additional factor contributing to the symptoms of NPH.
It is also conceivable that arterial hypertension might be linked to increased CSF pulsatility in some patients. Hyperdynamic CSF flow has been shown in patients with idiopathic NPH by MR investigations, and it has been hypothesized that this mechanism might contribute to the progression of NPH.5 39 Since it has been demonstrated that autoregulation can be impaired in patients with idiopathic NPH,40 it is conceivable that high blood pressure might reinforce vascular pulsations. This could result in increased CSF pulsatility acting on the walls of the dilated ventricles, especially in patients with impaired cerebral compliance.
It is probable that idiopathic NPH of the elderly has several underlying causes. Although arterial hypertension is found in the majority of patients and idiopathic NPH is frequently associated with other vascular diseases, some patients have none of these associations. NPH in these patients might actually be some kind of secondary NPH due to events that in a given case did not elicit clinically relevant symptoms initially.
In view of our findings, it is conceivable that early treatment of vascular risk factors, especially of arterial hypertension, might slow the progression of NPH in some older patients with idiopathic NPH.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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We wish to thank H. Förster and V. Sonntag-O'Brien for their expert help in preparation of the manuscript.
Received April 10, 1995; revision received September 19, 1995; accepted September 25, 1995.
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