The influence of lumbar spinal drainage on diffusion parameters in patients with suspected normal pressure hydrocephalus using 3T MRI

Abstract

Background

Normal pressure hydrocephalus (NPH) has been an ongoing and challenging field of research for the past decades because two main issues are still not fully understood: the pathophysiologic mechanisms underlying ventricular enlargement and prediction of outcome after surgery.

Purpose

To evaluate changes in diffusion tensor imaging (DTI) derived parameters in patients with suspected normal pressure hydrocephalus before and after withdrawal of cerebrospinal fluid (CSF).

Material and Methods

Twenty-four consecutive patients with clinical and radiological suspicion of NPH and 14 age-matched control subjects were examined with DTI on a clinical 3T scanner. Patients were examined before and 6–36 h after CSF drainage (interval between scans, 5 days). Fifteen patients were finally included in data analysis. Fractional anisotropy (FA) and mean, parallel, and radial diffusivity (MD, PD, RD) were evaluated using a combination of a ROI-based approach and a whole-brain voxel-by-voxel analysis.

Results

Alteration of DTI parameters in patients with suspected NPH is regionally different. Compared to the control group, we found an elevation of FA in the subcortical white matter (SCWM) and corpus callosum, whereas the other diffusion parameters showed an increase throughout the brain in variable extent. We also found a slight normalization of RD in the SCWM in patients after lumbar drainage.

Conclusion

Our results show that DWI parameters are regionally dependent and reflect multifactorial (patho-) physiological mechanisms, which need to be interpreted carefully. It seems that improvement of gait is caused by a decrease of interstitial water deposition in the SCWM.

Keywords

Normal pressure hydrocephalus magnetic resonance imaging (MRI)diffusion tensor imaging cerebrospinal fluid (CSF)spinal drainage tap test voxel-based analysis

Get full access to this article

View all access options for this article.

References

Hakim

Adams

. The special clinical problem of symptomatic hydrocephalus with normal cerebrospinal fluid pressure. Observations on cerebrospinal fluid hydrodynamics. J Neurol Sci 1965; 2: 307–327.

Tarnaris

Kitchen

Watkins

. Noninvasive biomarkers in normal pressure hydrocephalus: evidence for the role of neuroimaging. J Neurosurg 2009; 110: 837–851.

Marmarou

Bergsneider

Klinge

. The value of supplemental prognostic tests for the preoperative assessment of idiopathic normal-pressure hydrocephalus. Neurosurgery 2005; 57: S17–S28. discussion ii–v.

Stephensen

Andersson

Eklund

. Objective B wave analysis in 55 patients with non-communicating and communicating hydrocephalus. J Neurol Neurosurg Psychiatry 2005; 76: 965–970.

Hattingen

Jurcoane

Melber

. Diffusion tensor imaging in patients with adult chronic idiopathic hydrocephalus. Neurosurgery 2010; 66: 917–924.

Eide

Sorteberg

. Diagnostic intracranial pressure monitoring and surgical management in idiopathic normal pressure hydrocephalus: a 6-year review of 214 patients. Neurosurgery 2010; 66: 80–91.

Braun

Gooskens

Vandertop

. 1H magnetic resonance spectroscopy in human hydrocephalus. J Magn Reson Imaging 2003; 17: 291–299.

Shiino

Nishida

Yasuda

. Magnetic resonance spectroscopic determination of a neuronal and axonal marker in white matter predicts reversibility of deficits in secondary normal pressure hydrocephalus. J Neurol Neurosurg Psychiatry 2004; 75: 1141–1148.

Basser

Pierpaoli

. A simplified method to measure the diffusion tensor from seven MR images. Magn Reson Med 1998; 39: 928–934.

10.

Anik

Demirci

Anik

. Apparent diffusion coefficient and cerebrospinal fluid flow measurements in patients with hydrocephalus. J Comput Assist Tomogr 2008; 32: 392–396.

11.

Assaf

Ben-Sira

Constantini

. Diffusion tensor imaging in hydrocephalus: initial experience. Am J Neuroradiol 2006; 27: 1717–1724.

12.

Scheel

Diekhoff

Sprung

. Diffusion tensor imaging in hydrocephalus-findings before and after shunt surgery. Acta Neurochir (Wien) 2012; 154: 1699–1706.

13.

Marmarou

Bergsneider

Relkin

. Development of guidelines for idiopathic normal-pressure hydrocephalus: introduction. Neurosurgery 2005; 57: S1–S3. discussion ii–v.

14.

Rorden

Karnath

Bonilha

. Improving lesion-symptom mapping. J Cogn Neurosci 2007; 19: 1081–1088.

15.

Smith

Jenkinson

Woolrich

. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004; 23(Suppl. 1): S208–S219.

16.

Smith

. Fast robust automated brain extraction. Hum Brain Mapp 2002; 17: 143–155.

17.

Behrens

Johansen-Berg

Woolrich

. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 2003; 6: 750–757.

18.

Smith

Jenkinson

Johansen-Berg

. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 2006; 31: 1487–1505.

19.

Lenfeldt

Larsson

Nyberg

. Diffusion tensor imaging reveals supplementary lesions to frontal white matter in idiopathic normal pressure hydrocephalus. Neurosurgery 2011; 68: 1586–1593. discussion 93.

20.

Osuka

Matsushita

Yamamoto

. Evaluation of ventriculomegaly using diffusion tensor imaging: correlations with chronic hydrocephalus and atrophy. J Neurosurg 2010; 112: 832–839.

21.

Smith

Johansen-Berg

Jenkinson

. Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nat Protoc 2007; 2: 499–503.

22.

Nichols

Holmes

. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 2002; 15: 1–25.

23.

Graff-Radford

Godersky

. Normal-pressure hydrocephalus. Onset of gait abnormality before dementia predicts good surgical outcome. Arch Neurol 1986; 43: 940–942.

24.

Roricht

Meyer

Woiciechowsky

. Callosal and corticospinal tract function in patients with hydrocephalus: a morphometric and transcranial magnetic stimulation study. J Neurol 1998; 245: 280–288.

25.

Nowak

Topka

. Broadening a classic clinical triad: The hypokinetic motor disorder of normal pressure hydrocephalus also affects the hand. Exp Neurol 2006; 198: 81–87.

26.

Stolze

Kuhtz-Buschbeck

Drücke

. Comparative analysis of the gait disorder of normal pressure hydrocephalus and Parkinson's disease. J Neurol Neurosurg Psychiatry 2001; 70: 289–297.

27.

Lenfeldt

Larsson

Nyberg

. Idiopathic normal pressure hydrocephalus: increased supplementary motor activity accounts for improvement after CSF drainage. Brain 2008; 131: 2904–2912.

28.

Klinge

Brooks

Samii

. Correlates of local cerebral blood flow (CBF) in normal pressure hydrocephalus patients before and after shunting–A retrospective analysis of [(15)O]H(2)O PET-CBF studies in 65 patients. Clin Neurol Neurosurg 2008; 110: 369–375.

29.

Mataro

Matarin

Poca

. 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.

30.

Hattori

Yuasa

Aoki

. Altered microstructure in corticospinal tract in idiopathic normal pressure hydrocephalus: comparison with Alzheimer disease and Parkinson disease with dementia. Am J Neuroradiol 2011; 32: 1681–1687.

31.

Osuka

Matsumura

Ishikawa

. Diffusion tensor imaging in patients with adult chronic idiopathic hydrocephalus. Neurosurgery 2010; 67: E1474–E1474.

32.

Demura

Mase

Miyati

. Changes of fractional anisotropy and apparent diffusion coefficient in patients with idiopathic normal pressure hydrocephalus. Acta Neurochir Suppl 2012; 113: 29–32.

33.

Singer

Melber

Hattingen

. MR volumetric changes after diagnostic CSF removal in normal pressure hydrocephalus. J Neurol 2012; 259: 2440–2446.