J Clin Neurol.  2016 Oct;12(4):452-459. 10.3988/jcn.2016.12.4.452.

Asymmetric and Upper Body Parkinsonism in Patients with Idiopathic Normal-Pressure Hydrocephalus

• Kang K
• Jeon JS
• Kim T
• Choi D
• Ko PW
• Hwang SK
• Lee HW

• KMID: 2385110
• DOI: http://doi.org/10.3988/jcn.2016.12.4.452

Abstract

BACKGROUND AND PURPOSE
Our aims were to analyze the characteristics of parkinsonian features and to characterize changes in parkinsonian motor symptoms before and after the cerebrospinal fluid tap test (CSFTT) in idiopathic normal-pressure hydrocephalus (INPH) patients.
METHODS
INPH subjects were selected in consecutive order from a prospectively enrolled INPH registry. Fifty-five INPH patients (37 males) having a positive response to the CSFTT constituted the final sample for analysis. The mean age was 73.7±4.7 years. The pre-tap mean Unified Parkinson's Disease Rating Scale motor (UPDRS-III) score was 24.5±10.2.
RESULTS
There was no significant difference between the upper and lower body UPDRS-III scores (p=0.174). The parkinsonian signs were asymmetrical in 32 of 55 patients (58.2%). At baseline, the Timed Up and Go Test and 10-meter walking test scores were positively correlated with the total motor score, global bradykinesia score, global rigidity score, upper body score, lower body score, and postural instability/gait difficulties score of UPDRS-III. After the CSFTT, the total motor score, global bradykinesia score, upper body score, and lower body score of UPDRS-III significantly improved (p<0.01). There was a significant decrease in the number of patients with asymmetric parkinsonism (p<0.05).
CONCLUSIONS
In the differential diagnosis of elderly patients presenting with asymmetric and upper body parkinsonism, we need to consider a diagnosis of INPH. The association between gait function and parkinsonism severity suggests the involvement of similar circuits producing gait and parkinsonian symptoms in INPH.

Keyword

normal pressure hydrocephalus; parkinsonism; Parkinson's disease

MeSH Terms

Aged
Cerebrospinal Fluid
Diagnosis
Diagnosis, Differential
Gait
Humans
Hydrocephalus*
Hydrocephalus, Normal Pressure
Hypokinesia
Parkinson Disease
Parkinsonian Disorders*
Prospective Studies
Walking

Reference

1. Cabral D, Beach TG, Vedders L, Sue LI, Jacobson S, Myers K, et al. Frequency of Alzheimer's disease pathology at autopsy in patients with clinical normal pressure hydrocephalus. Alzheimers Dement. 2011; 7:509–513.

2. Kim MJ, Seo SW, Lee KM, Kim ST, Lee JI, Nam DH, et al. Differential diagnosis of idiopathic normal pressure hydrocephalus from other dementias using diffusion tensor imaging. AJNR Am J Neuroradiol. 2011; 32:1496–1503.

3. Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH. Symptomatic occult hydrocephalus with "normal" cerebrospinal-fluid pressure: a treatable syndrome. N Engl J Med. 1965; 273:117–126.

4. Owler BK, Momjian S, Czosnyka Z, Czosnyka M, Péna A, Harris NG, et al. Normal pressure hydrocephalus and cerebral blood flow: a PET study of baseline values. J Cereb Blood Flow Metab. 2004; 24:17–23.

5. Ishikawa M, Hashimoto M, Kuwana N, Mori E, Miyake H, Wachi A, et al. Guidelines for management of idiopathic normal pressure hydrocephalus. Neurol Med Chir (Tokyo). 2008; 48:48 Suppl. S1–S23.

6. Barbosa MT, Caramelli P, Maia DP, Cunningham MC, Guerra HL, Lima-Costa MF, et al. Parkinsonism and Parkinson's disease in the elderly: a community-based survey in Brazil (the Bambuí study). Mov Disord. 2006; 21:800–808.

7. Eckert T, Barnes A, Dhawan V, Frucht S, Gordon MF, Feigin AS, et al. FDG PET in the differential diagnosis of parkinsonian disorders. Neuroimage. 2005; 26:912–921.

8. Akiguchi I, Ishii M, Watanabe Y, Watanabe T, Kawasaki T, Yagi H, et al. Shunt-responsive parkinsonism and reversible white matter lesions in patients with idiopathic NPH. J Neurol. 2008; 255:1392–1399.

9. Gnanalingham KK, Byrne EJ, Thornton A, Sambrook MA, Bannister P. Motor and cognitive function in Lewy body dementia: comparison with Alzheimer's and Parkinson's diseases. J Neurol Neurosurg Psychiatry. 1997; 62:243–252.

10. Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM. Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery. 2005; 57:3 Suppl. S4–S16. discussion ii-v.

11. Kang K, Hwang SK, Lee HW. Shunt-responsive idiopathic normal pressure hydrocephalus patient with delayed improvement after tap test. J Korean Neurosurg Soc. 2013; 54:437–440.

12. Bugalho P, Alves L, Miguel R. Gait dysfunction in Parkinson's disease and normal pressure hydrocephalus: a comparative study. J Neural Transm (Vienna). 2013; 120:1201–1207.

13. Ishikawa M, Hashimoto M, Mori E, Kuwana N, Kazui H. The value of the cerebrospinal fluid tap test for predicting shunt effectiveness in idiopathic normal pressure hydrocephalus. Fluids Barriers CNS. 2012; 9:1.

14. Kang K, Yoon U, Lee JM, Lee HW. Idiopathic normal-pressure hydrocephalus, cortical thinning, and the cerebrospinal fluid tap test. J Neurol Sci. 2013; 334:55–62.

15. Choi SH, Na DL, Lee BH, Hahm DS, Jeong JH, Yoon SJ, et al. Estimating the validity of the Korean version of Expanded Clinical Dementia Rating (CDR) scale. J Korean Neurol Assoc. 2001; 19:585–591.

16. Kang Y, Na DL, Hahn S. A validity study on the Korean Mini-Mental State Examination (K-MMSE) in dementia patients. J Korean Neurol Assoc. 1997; 15:300–308.

17. Mataró M, Matarín M, Poca MA, Pueyo R, Sahuquillo J, Barrios M, et al. Functional and magnetic resonance imaging correlates of corpus callosum in normal pressure hydrocephalus before and after shunting. J Neurol Neurosurg Psychiatry. 2007; 78:395–398.

18. Kubo Y, Kazui H, Yoshida T, Kito Y, Kimura N, Tokunaga H, et al. Validation of grading scale for evaluating symptoms of idiopathic normal-pressure hydrocephalus. Dement Geriatr Cogn Disord. 2008; 25:37–45.

19. Hassin-Baer S, Sirota P, Korczyn AD, Treves TA, Epstein B, Shabtai H, et al. Clinical characteristics of neuroleptic-induced parkinsonism. J Neural Transm (Vienna). 2001; 108:1299–1308.

20. Oosterveld LP, Allen JC Jr, Reinoso G, Seah SH, Tay KY, Au WL, et al. Prognostic factors for early mortality in Parkinson's disease. Parkinsonism Relat Disord. 2015; 21:226–230.

21. Nocera J, Hass C. Should gait speed be included in the clinical evaluation of Parkinson's disease? Adv Parkinsons Dis. 2012; 1:1–4.

22. Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA. MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am J Roentgenol. 1987; 149:351–356.

23. Potter GM, Doubal FN, Jackson CA, Sudlow CL, Dennis MS, Wardlaw JM. Lack of association of white matter lesions with ipsilateral carotid artery stenosis. Cerebrovasc Dis. 2012; 33:378–384.

24. Kiroğlu Y, Karabulut N, Oncel C, Yagci B, Sabir N, Ozdemir B. Cerebral lateral ventricular asymmetry on CT: how much asymmetry is representing pathology? Surg Radiol Anat. 2008; 30:249–255.

25. Espay AJ, Narayan RK, Duker AP, Barrett ET Jr, de Courten-Myers G. Lower-body parkinsonism: reconsidering the threshold for external lumbar drainage. Nat Clin Pract Neurol. 2008; 4:50–55.

26. Gallia GL, Rigamonti D, Williams MA. The diagnosis and treatment of idiopathic normal pressure hydrocephalus. Nat Clin Pract Neurol. 2006; 2:375–381.

27. Nowak DA, Topka HR. Broadening a classic clinical triad: the hypokinetic motor disorder of normal pressure hydrocephalus also affects the hand. Exp Neurol. 2006; 198:81–87.

28. Krauss JK, Regel JP, Droste DW, Orszagh M, Borremans JJ, Vach W. Movement disorders in adult hydrocephalus. Mov Disord. 1997; 12:53–60.

29. Blandini F, Nappi G, Tassorelli C, Martignoni E. Functional changes of the basal ganglia circuitry in Parkinson's disease. Prog Neurobiol. 2000; 62:63–88.

30. Obeso JA, Marin C, Rodriguez-Oroz C, Blesa J, Benitez-Temiño B, Mena-Segovia J, et al. The basal ganglia in Parkinson's disease: current concepts and unexplained observations. Ann Neurol. 2008; 64:Suppl 2. S30–S46.

31. Wu T, Wang J, Wang C, Hallett M, Zang Y, Wu X, et al. Basal ganglia circuits changes in Parkinson's disease patients. Neurosci Lett. 2012; 524:55–59.

32. Tohgi H, Yonezawa H, Takahashi S, Sato N, Kato E, Kudo M, et al. Cerebral blood flow and oxygen metabolism in senile dementia of Alzheimer's type and vascular dementia with deep white matter changes. Neuroradiology. 1998; 40:131–137.

33. van der Hoorn A, Burger H, Leenders KL, de Jong BM. Handedness correlates with the dominant Parkinson side: a systematic review and meta-analysis. Mov Disord. 2012; 27:206–210.

34. Malm J, Graff-Radford NR, Ishikawa M, Kristensen B, Leinonen V, Mori E, et al. Influence of comorbidities in idiopathic normal pressure hydrocephalus - research and clinical care. A report of the ISHCSF task force on comorbidities in INPH. Fluids Barriers CNS. 2013; 10:22.

35. Yamanouchi H, Nagura H. Neurological signs and frontal white matter lesions in vascular parkinsonism. A clinicopathologic study. Stroke. 1997; 28:965–969.

36. Elbaz A, Bower JH, Peterson BJ, Maraganore DM, McDonnell SK, Ahlskog JE, et al. Survival study of Parkinson disease in Olmsted County, Minnesota. Arch Neurol. 2003; 60:91–96.

37. Derflinger S, Sorg C, Gaser C, Myers N, Arsic M, Kurz A, et al. Grey-matter atrophy in Alzheimer's disease is asymmetric but not lateralized. J Alzheimers Dis. 2011; 25:347–357.

38. Hamilton R, Patel S, Lee EB, Jackson EM, Lopinto J, Arnold SE, et al. Lack of shunt response in suspected idiopathic normal pressure hydrocephalus with Alzheimer disease pathology. Ann Neurol. 2010; 68:535–540.

39. Herman T, Rosenberg-Katz K, Jacob Y, Auriel E, Gurevich T, Giladi N, et al. White matter hyperintensities in Parkinson's disease: do they explain the disparity between the postural instability gait difficulty and tremor dominant subtypes? PLoS One. 2013; 8:e55193.

40. Palm WM, Walchenbach R, Bruinsma B, Admiraal-Behloul F, Middelkoop HA, Launer LJ, et al. Intracranial compartment volumes in normal pressure hydrocephalus: volumetric assessment versus outcome. AJNR Am J Neuroradiol. 2006; 27:76–79.

41. Helmich RC, Hallett M, Deuschl G, Toni I, Bloem BR. Cerebral causes and consequences of parkinsonian resting tremor: a tale of two circuits? Brain. 2012; 135(Pt 11):3206–3226.

42. Hallett M. Parkinson's disease tremor: pathophysiology. Parkinsonism Relat Disord. 2012; 18:Suppl 1. S85–S86.

43. Bugalho P, Guimarães J. Gait disturbance in normal pressure hydrocephalus: a clinical study. Parkinsonism Relat Disord. 2007; 13:434–437.

44. Ouchi Y, Nakayama T, Kanno T, Yoshikawa E, Shinke T, Torizuka T. In vivo presynaptic and postsynaptic striatal dopamine functions in idiopathic normal pressure hydrocephalus. J Cereb Blood Flow Metab. 2007; 27:803–810.

45. Stolze H, Kuhtz-Buschbeck JP, Drücke H, Jöhnk K, Diercks C, Palmié S, et al. Gait analysis in idiopathic normal pressure hydrocephalus--which parameters respond to the CSF tap test? Clin Neurophysiol. 2000; 111:1678–1686.

46. Lenfeldt N, Larsson A, Nyberg L, Andersson M, Birgander R, Eklund A, et al. Idiopathic normal pressure hydrocephalus: increased supplementary motor activity accounts for improvement after CSF drainage. Brain. 2008; 131(Pt 11):2904–2912.

47. Haber S, McFarland NR. The place of the thalamus in frontal cortical-basal ganglia circuits. Neuroscientist. 2001; 7:315–324.

48. Rosin B, Nevet A, Elias S, Rivlin-Etzion M, Israel Z, Bergman H. Physiology and pathophysiology of the basal ganglia-thalamo-cortical networks. Parkinsonism Relat Disord. 2007; 13:Suppl 3. S437–S439.

49. Prodoehl J, Planetta PJ, Kurani AS, Comella CL, Corcos DM, Vaillan-court DE. Differences in brain activation between tremor- and non-tremor-dominant Parkinson disease. JAMA Neurol. 2013; 70:100–106.

50. Várkuti B, Cavusoglu M, Kullik A, Schiffler B, Veit R, Yilmaz Ö, et al. Quantifying the link between anatomical connectivity, gray matter volume and regional cerebral blood flow: an integrative MRI study. PLoS One. 2011; 6:e14801.

51. Obeso JA, Rodriguez-Oroz MC, Rodriguez M, DeLong MR, Olanow CW. Pathophysiology of levodopa-induced dyskinesias in Parkinson's disease: problems with the current model. Ann Neurol. 2000; 47:4 Suppl 1. S22–S32. discussion S32-S34.

52. Fasano A, Aquino CC, Krauss JK, Honey CR, Bloem BR. Axial disability and deep brain stimulation in patients with Parkinson disease. Nat Rev Neurol. 2015; 11:98–110.

53. Kang K, Ko PW, Jin M, Suk K, Lee HW. Idiopathic normal-pressure hydrocephalus, cerebrospinal fluid biomarkers, and the cerebrospinal fluid tap test. J Clin Neurosci. 2014; 21:1398–1403.