Skip to main content
Log in

Feasibility of radiological markers in idiopathic normal pressure hydrocephalus

  • Clinical Article - Neurosurgical Anatomy
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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

  1. 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

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  PubMed  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. 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

    Article  CAS  PubMed  Google Scholar 

  7. 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

    Article  PubMed  Google Scholar 

  8. Evans WA (1942) An encephalographic ratio for estimating ventricular enlargement and cerebral atrophy. Arch Neurol Psychiatr 47:931

    Article  Google Scholar 

  9. 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

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. 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

    CAS  PubMed  Google Scholar 

  12. 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

    CAS  PubMed  Google Scholar 

  13. 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

    PubMed  Google Scholar 

  14. Graff-Radford NR (2007) Normal pressure hydrocephalus. Neurol Clin 25:809–832

    Article  PubMed  Google Scholar 

  15. 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

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. 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

    CAS  PubMed  Google Scholar 

  18. 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

    Article  PubMed  Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. 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

    Article  CAS  PubMed  Google Scholar 

  21. 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

    CAS  PubMed  Google Scholar 

  22. 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)

  23. 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

    Article  CAS  PubMed  Google Scholar 

  24. 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

    CAS  PubMed  Google Scholar 

  25. LeMay M, New PF (1970) Radiological diagnosis of occult normal-pressure hydrocephalus. Radiology 96:347–358

    Article  CAS  PubMed  Google Scholar 

  26. 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

  27. Meier U, Mutze S (2005) Does the ventricle size change after shunt operation of normal-pressure hydrocephalus? Acta Neurochir Suppl 95:257–259

    Article  CAS  PubMed  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM (2005) Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery 57:S4–S16

    PubMed  Google Scholar 

  30. 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. 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

    PubMed  Google Scholar 

  32. 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

    CAS  PubMed  Google Scholar 

  33. 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

    Article  PubMed  Google Scholar 

  34. 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

    Article  PubMed  Google Scholar 

  35. 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

    Article  CAS  PubMed  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Maria Kojoukhova.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-015-2503-8

Keywords

Navigation