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Parkinsonian Symptoms in Normal Pressure Hydrocephalus: a Population-Based Study

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Parkinsonian Symptoms in Normal Pressure Hydrocephalus: a Population-Based Study http://www.diva-portal.org This is the published version of a paper published in Journal of Neurology. Citation for the original published paper (version of record): Molde, K., Söderström, L., Laurell, K. (2017) Parkinsonian symptoms in normal pressure hydrocephalus: a population-based study. Journal of Neurology, 264(10): 2141-2148 https://doi.org/10.1007/s00415-017-8598-5 Access to the published version may require subscription. N.B. When citing this work, cite the original published paper. Permanent link to this version: http://urn.kb.se/resolve?urn=urn:nbn:se:umu:diva-142915 J Neurol (2017) 264:2141–2148 DOI 10.1007/s00415-017-8598-5 ORIGINAL COMMUNICATION Parkinsonian symptoms in normal pressure hydrocephalus: a population‑based study Karin Molde1 · Lars Söderström1 · Katarina Laurell1 Received: 3 June 2017 / Revised: 17 August 2017 / Accepted: 18 August 2017 / Published online: 6 September 2017 © The Author(s) 2017. This article is an open access publication Abstract It may be challenging to diferentiate normal liberal use of neuroradiological imaging when investigating pressure hydrocephalus (NPH) from neurodegenerative a patient with parkinsonian features. disorders such as Parkinson’s disease. In this population- based study, we wanted to describe the frequency of par- Keywords Normal pressure hydrocephalus · kinsonian symptoms among individuals with and without Hydrocephalus · Parkinsonism · Parkinson’s disease · NPH, and whether the motor examination part of the Unifed UPDRS Parkinson’s Disease Rating Scale (UPDRS-m) score difers between these groups. Furthermore, we wanted to fnd out whether there was a relationship between UPDRS-m score, Introduction NPH symptoms, and radiological signs of NPH. A sam- ple of 168 individuals over the age of 65 with and without Parkinsonian symptomatology exists in addition to the clas- self-reported symptoms of NPH underwent a computerized sical triad of gait, cognitive, and urinary symptoms in nor- tomography of the brain and clinical examination, including mal pressure hydrocephalus (NPH) [1–4], and may compli- UPDRS-m to grade parkinsonian symptoms. According to cate the diagnostic considerations [5, 6]. Radiology of the diagnostic guidelines, 38 fulflled criteria for NPH, whereas brain is essential to diagnose NPH [7], with typical fnd- 130 had unlikely NPH. Bradykinesia was signifcantly more ings of dilated ventricles without any macroscopic obstruc- common among those with NPH (79%) compared to those tion to cerebral spinal fuid (CSF) fow, often with signs of with unlikely NPH (32%) (p < 0.001). The corresponding compressed cortical sulci combined with focally enlarged fgures for rigidity were 43 vs. 15% (p < 0.001), for postural sulci [8]. NPH is a treatable condition; in about 80% of the instability 71 vs. 22% (p < 0.001), and for tremor at rest 5 vs. patients, the symptoms improve after surgical treatment with 6% (not signifcant). The total UPDRS-m score was signif- CSF shunt [9]. cantly higher among individuals with NPH (median = 12) The Unifed Parkinson’s Disease Rating Scale (UPDRS) than without (median = 1) and correlated signifcantly with [10] is a widely used rating scale for Parkinson’s disease the degree of NPH symptoms (r = −0.72) and ventriculo- (PD) [11] and the motor examination part (UPDRS-m) has megaly (r = 0.31). In this study, parkinsonian symptoms, also been used to rate parkinsonian motor symptoms in except resting tremor, were frequent in individuals with NPH patients [12–15]. In the previous hospital-based stud- NPH and correlated with the severity of NPH symptoms. ies, upper body bradykinesia has been described in 62% Asymmetric symptoms were uncommon. We recommend a and parkinsonism in up to 71% of NPH patients [2, 12]. Signifcant improvements in the total UPDRS-m score have been described after shunt surgery and after CSF removal by lumbar puncture (CSF tap test) [12–15]. Mild parkinsonian * Karin Molde signs [16] in the four categories bradykinesia, tremor at rest, [email protected] rigidity, and postural/gait changes are found in 20–40% of 1 Department of Pharmacology and Clinical Neuroscience, the older population [17, 18]. Except from neurodegenera- Umeå University, Umeå, Sweden tive diseases, factors associated with normal aging as well as Vol.:(0123456789)1 3 2142 J Neurol (2017) 264:2141–2148 comorbidities such as cerebrovascular disease and essential 200 mmH2O, or less. However, when CSF pressure measure- tremor may contribute to fndings of isolated parkinsonian ments are not performed, as in the present study, the diagno- signs [16, 19]. sis “possible NPH with neuroradiological support” can be As parkinsonian features are important in the diferential used instead. It requires an NPH-specifc radiological picture diagnosis of neurological disorders, we wanted to describe of the brain with narrowing of the sulci and subarachnoid the frequency of such symptoms and compare the UPDRS-m spaces over the high convexity/midline surface [21]. Finally, score between individuals from the general population with the diagnosis “defnitive NPH” is used when the symptoms and without signs of NPH. Furthermore, we wanted to fnd improve after shunt surgery. To simplify, we denominated out whether there was a relationship between UPDRS-m the groups as “unlikely”, “possible”, and “probable” NPH score, NPH symptoms, and radiological signs of NPH. where the latter was equivalent to “possible NPH with neu- roradiological support”. The only two individuals with the diagnosis of “defnite NPH”, i.e., confrmed with shunt sur- Methods gery were included in the “probable NPH” group. Radiological evaluation was made with a CT scan of Material the brain. Previously described radiological markers were analyzed, i.e., Evans’ index, callosal angle, signs of narrow This study is part of an ongoing epidemiological study on medial sulci, focally enlarged sulci, dilated fssure Sylvii, the prevalence of NPH. Out of the total population of 28,000 and size of temporal horns [8] (Fig. 2). individuals aged 65 years or older living in Jämtland County, To investigate the degree of parkinsonian motor symp- 1000 were randomly selected from the Swedish population toms, UPDRS-m [10] was used, grading the patients motor register and received a questionnaire on NPH symptoms. function from 0 to 4, where 0 represents normal and 4 repre- The questionnaire is based on an on-line screening tool for sents severe impairment. Tremor, rigidity, and bradykinesia NPH [20], and consists of seven yes or no questions regard- in extremities are measured and scored bilaterally. A senior ing balance and gait disturbance, cognitive impairment, and consultant in neurology with assistance of a trained medical urinary symptoms. Individuals who reported two symptoms student made all the examinations. Tremor at rest, bradyki- (including gait or balance disturbance) or more were invited nesia in extremities, rigidity, and postural instability were to undergo further investigations. In total, 673 returned a described as present when scored 1 or more. Parkinsonism correct flled in questionnaire giving a response rate of was defned according to the UK brain bank criteria, as the 67.3%, of which 168 individuals with and without symp- presence of bradykinesia together with at least one of the toms of NPH underwent computerized tomography (CT) symptoms tremor at rest, rigidity, and postural instability of the brain and neurological examinations. The fow chart [22]. describes the selection of the fnal study population (Fig. 1). We used a scale developed by Hellström et al. [23] to Exclusion criteria were severe medical conditions sufcient measure the severity of NPH symptoms. The scale is com- to explain the symptoms, for example known brain tumor or posed of four diferent domain scores (gait, balance, neu- severe multiple sclerosis diagnosed by a neurologist. Among ropsychology, and continence) which are assessed by 10 m those who returned the questionnaire and accepted further walking test, ordinal ratings of gait and balance, Grooved studies, one reported that he was under treatment for idi- pegboard test, Ray Auditory Verbal Learning Test (RAVLT), opathic PD at the Neurology Department. He had no signs of Stroop test, and an ordinal continence scale based on self- NPH on a previous CT scan and was excluded from further reports [23]. A total NPH score is calculated as the mean of studies. Among the investigated 168 individuals, two had the four domain scores with the gait domain counted twice. tested dopaminergic treatment but discontinued because of A score of 100 means the absence of symptoms, and 0 is the lack of efect. One of them had an ischemic lesion in basal most severe state. ganglia on CT brain, whereas the other had radiological The neurologist was blinded to radiological data and, signs of NPH and received a shunt in June 2016 with a clear accordingly, the radiologist was blinded to clinical data. improvement. To diagnose NPH, we used the guidelines by Mori et al. [7], which are suitable for population-based studies, because Statistical analysis they can be used without CSF pressure measurement. The criteria for “possible NPH” require at least two symptoms Descriptive statistics were used to present the frequency of from the clinical triad; gait disturbance, cognitive impair- diferent parkinsonian symptoms among individuals with ment, and urinary symptoms. Ventricular dilation (Evans’ and without signs of NPH. index> 0.3) is mandatory. “Probable NPH” requires in addi- Differences in the level of
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