Correlation of Midbrain Diameter and Gait Disturbance in Patients With
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0958_0963_Lee_JON_1791 08.08.2005 07:34 Uhr Seite 958 J Neurol (2005) 252:958–963 DOI 10.1007/s00415-005-0791-2 ORIGINAL COMMUNICATION Phil Hyu Lee Correlation of midbrain diameter and gait Suk Woo Yong Yo ung Hwan Ahn disturbance in patients with idiopathic Kyoon Huh normal pressure hydrocephalus ■ Received: 13 July 2004 Abstract Background and pur- significantly smaller in the NPH Received in revised form: pose Although gait disturbance is group than in the controls 19 November 2004 an important feature of idiopathic (14.8 ± 0.9 vs. 17.1 ± 0.7 mm, Accepted: 13 December 2004 normal pressure hydrocephalus p < 0.001). There were inverse cor- Published online: 19 April 2005 (NPH), only tentative theories have relations between the midbrain di- been offered to explain its patho- ameter and the widths of the two physiology. It has been suggested ventricles (r = –0.562, p = 0.008 for that the mesencephalic locomotor the third ventricle, and r = –0.510, region is the anatomical substrate p = 0.018 for the lateral ventricle). for the development of the hypoki- The severity of gait disturbance netic NPH gait. To investigate this was negatively correlated with the possibility, we evaluated the corre- midbrain diameter (r = –0.598, lation between gait disturbance p = 0.004), but the degree of cogni- and midbrain diameter. Methods tive dysfunction and incontinence We enrolled 21 patients with NPH showed no significant correlation P. H . Le e, M.D., Ph.D. (౧) · S. W.Yong, M.D. · and 20 age-matched control sub- with midbrain diameter or ventric- K. Huh, M.D. jects for the study. The maximal di- ular width. Conclusions This study Dept. of Neurology, College of Medicine Ajou University ameter of the midbrain and pons, suggests that midbrain atrophy is Woncheon-dong San 5, Paldal-ku and the width of the lateral and significantly associated with gait Suwon, Kyungki-do, 442–749, South Korea third ventricles were measured us- disturbance in NPH. Tel.: +82-31/219-5174 ing midsagittal T1-weighted MRI Fax: +82-31/219-5178 ■ E-Mail: [email protected] and axial T2-weighted MRI, respec- Key words normal pressure tively. Gait disturbance, cognitive hydrocephalus · midbrain · gait Y. H. Ahn, M.D., Ph.D. Dept. of Neurosurgery dysfunction, and incontinence disturbance · mesencephalic Ajou University School of Medicine were semiquantified. Results The locomotor region Suwon, Korea maximal midbrain diameter was The clinical elements of the NPH gait can be summa- Introduction rized as a hypokinetic gait which is characterized by di- minished gait velocity, reduced stride length, reduced Idiopathic normal pressure hydrocephalus (NPH) is step height, and dynamic disequilibrium [17, 28, 31, 34]. characterized by the clinical triad of gait disturbance, Patients with many other neurodegenerative diseases, progressive cognitive dysfunction, and urinary inconti- such as Parkinson’s disease, subcortical arteriosclerotic nence. Radiological investigations typically reveal en- encephalopathy, progressive supranuclear palsy (PSP), largement of the ventricles without cortical atrophy [2, and corticobasal degeneration, may develop hypoki- 10].Gait disturbance is the first clinical manifestation in netic gait during the disease progression [4, 35, 37]. The most cases of NPH and is one of the most important question of how gait disturbances develop in NPH pa- JON 1791 symptoms [5, 9, 24]. tients remains unresolved. Some researchers have pos- 0958_0963_Lee_JON_1791 08.08.2005 07:34 Uhr Seite 959 959 tulated that frontal lobe dysfunction plays a major role, tio of the greatest distance between the lateral walls in the frontal horns of the first and second ventricles, and the diameter of the inner while others have suggested that hydrocephalus con- table of the skull, both in the transverse plane) was calculated on T1- tributes to the interruption of the subcortical circuit weighted imaging. The maximal diameter of the midbrain and pons connecting the frontal lobe and basal ganglia [3, 19, 28]. was measured on T1-weighted imaging of the midsagittal plane with Based on recent animal studies, the mesencephalic the scanners’internal measurement device [39],using the PiView sys- locomotor region, which plays a major role in locomo- tem program (Fig. 1A). Since maximal ventricular width is known to be well correlated with ventricular volume [38], we measured the tion, has been suggested as the anatomical substrate for width of the lateral ventricle (horizontal distance at the midpoint of the development of gait freezing in idiopathic Parkin- the anteroposterior ventricular scan at the level of the septum pellu- son’s disease and other parkinsonisms [7, 23, 30]. In hu- cidum) on T2-weighted axial images (Fig. 1B). The diameter of the mans, the mesencephalic locomotor region is located in third ventricle was determined by the maximum transverse diameter on axial scans (Fig. 1C). Two neurologists (L. P.H and Y.S.U) mea- the dorsolateral portion of the midbrain [8]. sured the widths of each image in a blinded fashion, and the average In the present study, we assessed the midbrain diam- value was obtained. eter in patients with NPH and analyzed the relationship between the midbrain diameter and gait disturbance to ■ evaluate the contribution of midbrain to NPH gait. Rating scales of NPH symptoms The degree of gait disturbance was semiquantified according to the scale developed by Larsson et al. [22]: 1, normal; 2, insecure; 3, inse- Patients and methods cure with cane; 4, bimanual support; 5, aided; 6, wheelchair. The de- gree of urinary incontinence was recorded semiquantitatively, based ■ Patient population and controls on the scale developed by Krauss et al. [18]: 0, none; 1, sporadic in- continence or urge phenomena; 2,frequent incontinence; 3,only min- Twenty-one NPH patients who were inpatients in the Department of imal control.The degree of cognitive impairment was also semiquan- Neurology and Neurosurgery at Ajou University Hospital from Janu- tified according to the scale of Krauss et al.[20,22]: 0,none; 1,minimal ary, 2001, to April, 2004, were enrolled in the study. The diagnosis of attention or memory deficits; 2, considerable deficits, but oriented to NPH was based on the presence of the following symptoms and signs: situational context; 3, not or only marginally oriented. (1) gait disturbance, (2) cognitive dysfunction, urinary disturbance, or both, (3) ventricular enlargement (Evans ratio > 0.31) without cor- ■ tical atrophy on brain magnetic resonance imaging (MRI) [31],(4) in- Statistical Analysis tracranial pressure below 20 CmH20, as measured by lumbar punc- ture, (5) ventricular filling and block of convexity flow on Statistical analyses were performed with the use of a commercially radionuclide cisternography, (6) absence of other neurological dis- available software package (SPSS, version 10.0). The diameters of the eases that could explain the symptoms, such as progressive supranu- pons and midbrain of patients with NPH and controls were compared clear palsy (PSP) or corticobasal degeneration, or ventricular en- using the Mann-Whitney U test. The Spearman’s correlation test was largement described above [10, 21]. The control group consisted of used to test for associations between the midbrain size and the degree age- and sex-matched healthy volunteers who were free of neurolog- of clinical symptoms of NPH. To determine the interobserver relia- ical disease and whose neurological examinations were normal. bility of the rating, a Cronbach’s alpha coefficient was calculated. P values less than 0.05 were considered statistically significant. ■ Brain MRI and measurements Routine MRI images of the brain were obtained for all subjects on a 1.5-T Signa Scanner (GE, Signa, Advantage). The Evans ratio (the ra- ABC Fig. 1 (A) Measurement of the midsagittal maximal anteroposterior diameter of the midbrain (solid line) and pons (dotted line) on sagittal T1-weighted MR images using the internal measurement device. (B) Maximum lateral ventricle width (solid line) determined where the septum pellucidum remains thin. (C) The maximal third ventricle width (solid line) 0958_0963_Lee_JON_1791 08.08.2005 07:34 Uhr Seite 960 960 Results the diameter of the third ventricle and the diameter of the midbrain (r = –0.562, p = 0.008; Fig. 3A). In addition, The mean age of the patients with NPH was 70.5 years the diameter of the lateral ventricle was inversely corre- (SD 5.6),and 9 (42.8%) were female.The mean age of the lated with the diameter of the midbrain (r = –0.510, healthy control subjects (73.5 years, SD 4.9) was not sta- p = 0.018; Fig. 3B). tistically different from that of patients with NPH, and 9 Among the major symptoms of NPH, only the sever- (45%) were female. All patients with NPH had under- ity of gait disturbance showed an inverse correlation gone radionuclide cisternography that had confirmed with the midbrain diameter (r = –0.598,p = 0.004; Fig. 4); communicating hydrocephalus. All patients with NPH no association was found between urinary incontinence performed the CSF drainage, which subjectively im- or cognitive dysfunction and the midbrain diameter. No proved gait in all patients. The mean of the Evans ratio significant correlation was found between gait disturb- in patients with NPH was 0.39 (SD 0.03). The reliability ance, urinary incontinence, or cognitive dysfunction coefficients for the width of ventricle and maximal mid- with the diameters of the lateral or third ventricle. sagittal diameter of midbrain and pons were as follows: the lateral ventricle, 0.98; the third ventricle, 0.982; the midbrain, 0.975; the pons, 0.979. A The degree of gait disturbance was rated at level 1 in four patients, level 2 in nine patients, level 3 in three pa- tients, level 4 in two patients, level 5 in one patient, and level 6 in two patients.Urinary incontinence was present at level 0 in eight patients, level 1 in six patients, level 2 in five patients,and level 3 in two patients.The degree of cognitive impairment was level 0 in ten patients, level 1 in four patients, level 2 in seven patients, and level 3 in no patients.