Abstract
Background
Various radiological markers have been proposed for diagnostics in idiopathic normal pressure hydrocephalus (iNPH). We examined the usefulness of radiological markers in the diagnostics and prediction of shunt response in iNPH.
Method
In this retrospective cohort study, we evaluated brain CT or MRI scans of 390 patients with suspected iNPH. Based on a 24-h intraventricular pressure monitoring session, patients were classified into a non-NPH (n = 161) or probable iNPH (n = 229) group. Volumes of cerebrospinal fluid compartments (lateral ventricles, sylvian and suprasylvian subarachnoid spaces and basal cisterns) were visually assessed. Disproportionally enlarged subarachnoid spaces, flow void, white matter changes, medial temporal lobe atrophy and focally dilated sulci were evaluated. Moreover, we measured quantitative markers: Evans’ index (EI), the modified cella media index, mean width of the temporal horns and callosal angle.
Results
iNPH was more likely in patients with severe volumetric disproportion between the suprasylvian and sylvian subarachnoid spaces than in those without disproportion (OR 7.5, CI 95 % 4.0–14.1, P < 0.0001). Mild disproportion (OR 2.6, CI 95 % 1.4–4.6, P = 0.001) and narrow temporal horns (OR per 1 mm 0.91, CI 95 % 0.84–0.98, P = 0.014) were also associated with an iNPH diagnosis. Other radiological markers had little association with the iNPH diagnosis in the final combined multivariate model. Interestingly, EI was higher in non-NPH than iNPH patients (0.40 vs. 0.38, P = 0.039). Preoperative radiological markers were not associated with shunt response.
Conclusions
Visually evaluated disproportion was the most useful radiological marker in iNPH diagnostics. Narrower temporal horns also supported an iNPH diagnosis, possibly since atrophy was more pronounced in the non-NPH than iNPH group.
Similar content being viewed by others
Abbreviations
- AD:
-
Alzheimer’s disease
- CA:
-
Callosal angle
- CSF:
-
Cerebrospinal fluid
- CT:
-
Computed tomography
- EI:
-
Evans’ index
- FDS:
-
Focally dilated sulci
- iNPH:
-
Idiopathic normal pressure hydrocephalus
- MRI:
-
Magnetic resonance imaging
- mCMI:
-
Modified cella media index
- NPH:
-
Normal pressure hydrocephalus
- SA:
-
Subarachnoid
- sNPH:
-
Secondary normal pressure hydrocephalus
- VD:
-
Vascular dementia
References
Adams RD, Fisher CM, Hakim S, Ojemann RG, Sweet WH (1965) Symptomatic occult hydrocephalus with “normal” cerebrospinal-fluid pressure. A treatable syndrome. N Engl J Med 273:117–126
Algin O, Hakyemez B, Taskapilioglu O, Ocakoglu G, Bekar A, Parlak M (2009) Morphologic features and flow void phenomenon in normal pressure hydrocephalus and other dementias: are they really significant? Acad Radiol 16:1373–1380
Bendel P, Koivisto T, Aikia M, Niskanen E, Kononen M, Hanninen T, Vanninen R (2010) Atrophic enlargement of CSF volume after subarachnoid hemorrhage: correlation with neuropsychological outcome. AJNR Am J Neuroradiol 31:370–376
Bradley WG Jr, Scalzo D, Queralt J, Nitz WN, Atkinson DJ, Wong P (1996) Normal-pressure hydrocephalus: evaluation with cerebrospinal fluid flow measurements at MR imaging. Radiology 198:523–529
Bradley WG Jr, Whittemore AR, Kortman KE, Watanabe AS, Homyak M, Teresi LM, Davis SJ (1991) Marked cerebrospinal fluid void: indicator of successful shunt in patients with suspected normal-pressure hydrocephalus. Radiology 178:459–466
DeCarli C, Murphy DG, McIntosh AR, Teichberg D, Schapiro MB, Horwitz B (1995) Discriminant analysis of MRI measures as a method to determine the presence of dementia of the Alzheimer type. Psychiatry Res 57:119–130
Dixon GR, Friedman JA, Luetmer PH, Quast LM, McClelland RL, Petersen RC, Maher CO, Ebersold MJ (2002) Use of cerebrospinal fluid flow rates measured by phase-contrast MR to predict outcome of ventriculoperitoneal shunting for idiopathic normal-pressure hydrocephalus. Mayo Clin Proc 77:509–514
Evans WA (1942) An encephalographic ratio for estimating ventricular enlargement and cerebral atrophy. Arch Neurol Psychiatr 47:931
Fazekas F, Chawluk JB, Alavi A, Hurtig HI, Zimmerman RA (1987) MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. AJR Am J Roentgenol 149:351–356
Fazekas F, Kleinert R, Offenbacher H, Schmidt R, Kleinert G, Payer F, Radner H, Lechner H (1993) Pathologic correlates of incidental MRI white matter signal hyperintensities. Neurology 43:1683–1689
Frisoni GB, Beltramello A, Weiss C, Geroldi C, Bianchetti A, Trabucchi M (1996) Linear measures of atrophy in mild Alzheimer disease. AJNR Am J Neuroradiol 17:913–923
Frisoni GB, Beltramello A, Weiss C, Geroldi C, Bianchetti A, Trabucchi M (1996) Usefulness of simple measures of temporal lobe atrophy in probable Alzheimer’s disease. Dementia 7:15–22
Frisoni GB, Geroldi C, Beltramello A, Bianchetti A, Binetti G, Bordiga G, DeCarli C, Laakso MP, Soininen H, Testa C, Zanetti O, Trabucchi M (2002) Radial width of the temporal horn: a sensitive measure in Alzheimer disease. AJNR Am J Neuroradiol 23:35–47
Graff-Radford NR (2007) Normal pressure hydrocephalus. Neurol Clin 25:809–832
Hashimoto M, Ishikawa M, Mori E, Kuwana N, Study of INPH on neurological improvement (SINPHONI) (2010) Diagnosis of idiopathic normal pressure hydrocephalus is supported by MRI-based scheme: a prospective cohort study. Cerebrospinal Fluid Res 7:18
Holodny AI, George AE, de Leon MJ, Golomb J, Kalnin AJ, Cooper PR (1998) Focal dilation and paradoxical collapse of cortical fissures and sulci in patients with normal-pressure hydrocephalus. J Neurosurg 89:742–747
Holodny AI, Waxman R, George AE, Rusinek H, Kalnin AJ, de Leon M (1998) MR differential diagnosis of normal-pressure hydrocephalus and Alzheimer disease: significance of perihippocampal fissures. AJNR Am J Neuroradiol 19:813–819
Ishii K, Kanda T, Harada A, Miyamoto N, Kawaguchi T, Shimada K, Ohkawa S, Uemura T, Yoshikawa T, Mori E (2008) Clinical impact of the callosal angle in the diagnosis of idiopathic normal pressure hydrocephalus. Eur Radiol 18:2678–2683
Ishii K, Kawaguchi T, Shimada K, Ohkawa S, Miyamoto N, Kanda T, Uemura T, Yoshikawa T, Mori E (2008) Voxel-based analysis of gray matter and CSF space in idiopathic normal pressure hydrocephalus. Dement Geriatr Cogn Disord 25:329–335
Killiany RJ, Moss MB, Albert MS, Sandor T, Tieman J, Jolesz F (1993) Temporal lobe regions on magnetic resonance imaging identify patients with early Alzheimer’s disease. Arch Neurol 50:949–954
Kitagaki H, Mori E, Ishii K, Yamaji S, Hirono N, Imamura T (1998) CSF spaces in idiopathic normal pressure hydrocephalus: morphology and volumetry. AJNR Am J Neuroradiol 19:1277–1284
Koivisto AM, Alafuzoff I, Savolainen S, Sutela A, Rummukainen J, Kurki M, Jaaskelainen JE, Soininen H, Rinne J, Leinonen V (2013) Poor cognitive outcome in shunt-responsive idiopathic normal pressure hydrocephalus. Neurosurgery 72:1–8. Kuopio NPH Registry (www.uef.fi/nph)
Krauss JK, Droste DW, Vach W, Regel JP, Orszagh M, Borremans JJ, Tietz A, Seeger W (1996) Cerebrospinal fluid shunting in idiopathic normal-pressure hydrocephalus of the elderly: effect of periventricular and deep white matter lesions. Neurosurgery 39:292–299
Krauss JK, Regel JP, Vach W, Jungling FD, Droste DW, Wakhloo AK (1997) Flow void of cerebrospinal fluid in idiopathic normal pressure hydrocephalus of the elderly: can it predict outcome after shunting? Neurosurgery 40:67–73
LeMay M, New PF (1970) Radiological diagnosis of occult normal-pressure hydrocephalus. Radiology 96:347–358
Malm J, Graff-Radford NR, Ishikawa M, Kristensen B, Leinonen V, Mori E, Owler BK, Tullberg M, Williams MA, Relkin NR (2013) 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 10:22
Meier U, Mutze S (2005) Does the ventricle size change after shunt operation of normal-pressure hydrocephalus? Acta Neurochir Suppl 95:257–259
Mori E, Ishikawa M, Kato T, Kazui H, Miyake H, Miyajima M, Nakajima M, Hashimoto M, Kuriyama N, Tokuda T, Ishii K, Kaijima M, Hirata Y, Saito M, Arai H, Japanese Society of Normal Pressure Hydrocephalus (2012) Guidelines for management of idiopathic normal pressure hydrocephalus: second edition. Neurol Med Chir (Tokyo) 52:775–809
Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM (2005) Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery 57:S4–S16
Scheltens P, Leys D, Barkhof F, Huglo D, Weinstein HC, Vermersch P, Kuiper M, Steinling M, Wolters EC, Valk J (1992) Atrophy of medial temporal lobes on MRI in “probable” Alzheimer’s disease and normal ageing: diagnostic value and neuropsychological correlates. J Neurol Neurosurg Psychiatry 55:967–972
Tisell M, Tullberg M, Hellstrom P, Edsbagge M, Hogfeldt M, Wikkelso C (2011) Shunt surgery in patients with hydrocephalus and white matter changes. J Neurosurg 114:1432–1438
Tullberg M, Jensen C, Ekholm S, Wikkelso C (2001) Normal pressure hydrocephalus: vascular white matter changes on MR images must not exclude patients from shunt surgery. AJNR Am J Neuroradiol 22:1665–1673
van Swieten JC, van den Hout JH, van Ketel BA, Hijdra A, Wokke JH, van Gijn J (1991) Periventricular lesions in the white matter on magnetic resonance imaging in the elderly. A morphometric correlation with arteriolosclerosis and dilated perivascular spaces. Brain 114(Pt 2):761–774
Virhammar J, Laurell K, Cesarini KG, Larsson EM (2014) The callosal angle measured on MRI as a predictor of outcome in idiopathic normal-pressure hydrocephalus. J Neurosurg 120:178–184
Virhammar J, Laurell K, Cesarini KG, Larsson EM (2014) Preoperative prognostic value of MRI findings in 108 patients with idiopathic normal pressure hydrocephalus. AJNR Am J Neuroradiol 35:2311–2318
Acknowledgments
The authors thank RN Marita Voutilainen for maintenance of the KUH NPH Register. We thank Gerald G. Netto for proofreading the article. We also thank biostatistician Tuomas Selander for statistical assistance.
Sources of funding
The Maire Taponen Foundation, KUH VTR Fund, The Finnish Medical Foundation.
Disclosure
All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.
Conflicts of interest
None.
Author information
Authors and Affiliations
Corresponding author
Additional information
Comments
Kojoukhova and co-workers present their register-based retrospective cohort study assessing the feasibility of radiological markers in idiopathic normal pressure hydrocephalus in 390 patients over a period of nearly 20 years. Even though this is a retrospective study with the well-known limitations of this study design, the number of patients included is comparatively large, and the study includes all important radiological markers of this entity. Moreover, the strengths and limitations of the present study appear to be adequately discussed by the authors themselves.
Marcus Reinges
Giessen,Germany
This rather large cohort study is still another attempt at sorting out radiological features/markers that can be used to foresee the likelihood of a person with enlarged ventricles is harboring idiopathic normal pressure hydrocephalus. The most important finding of the study is that only disproportion between the suprasylvian and sylvian subarachnoid spaces, as well as the temporal horn width, are significantly associated with the final iNPH diagnosis. In addition, the authors found that it was impossible to predict the shunt response by any preoperative radiological feature.
In my opinion the findings in this study add valuable information for future use in the diagnostic workup of probable iNPH patients.
K. Wester
Bergen, Norway
Anna Sutela and Ville Leinonen contributed equally to this work.
Rights and permissions
About this article
Cite this article
Kojoukhova, M., Koivisto, A.M., Korhonen, R. et al. Feasibility of radiological markers in idiopathic normal pressure hydrocephalus. Acta Neurochir 157, 1709–1719 (2015). https://doi.org/10.1007/s00701-015-2503-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00701-015-2503-8