Abstract
Objective
Idiopathic normal pressure hydrocephalus (iNPH), a classical triad of gait abnormality, cognitive disturbance, and urinary incontinence, increases in prevalence with aging. Sarcopenia is also characterized by low muscle strength and mass, contributing to gait difficulty. Gait abnormality and lower physical activity also lead to the development of sarcopenia. Therefore, this study aims to investigate the relationship between sarcopenia and iNPH.
Methods
A total of 327 participants were included in this retrospective cross-sectional study. Demographic and clinical characteristics, including age, sex, comorbidity index, number of medications, recurrent falls in the last year, laboratory findings and comprehensive geriatric assessment (CGA) parameters were recorded. Sarcopenia was defined according to the EGWSOP2 criteria. The relationship between sarcopenia and iNPH was assessed with regression analysis.
Results
There were 51 participants with iNPH, 49% female, mean age 78 years (SD 5.7) and 276 control participants, 74% female, mean age 72 years (SD 6.1). The sarcopenia rates in patients with iNPH and controls were 19.6% and 2.5%, respectively (p < 0.01). The odds of probable sarcopenia were 3.89 times, and the slow gait speed was 8.47 times higher in iNPH patients than in controls after adjusting for age, sex, and the other confounders. The Mini-Mental State Examination score (p = 0.042, OR = 0.869 with 95% CI:0.759–0.995) was associated with probable sarcopenia among patients with iNPH.
Conclusion
This study demonstrated that sarcopenia was common in older patients with iNPH, which seems to be closely associated with decreased muscle strength and slowed gait speed. Thus, considering the potential untoward effects of both diseases, it is important for physicians to evaluate sarcopenia routinely in the follow-up and treatment of older patients with iNPH.
Similar content being viewed by others
Data availability
The datasets used and analyzed during the present study are available from the corresponding author upon reasonable request.
References
Hakim S, Venegas JG, Burton JD (1976) The physics of the cranial cavity, hydrocephalus and normal pressure hydrocephalus: mechanical interpretation and mathematical model. Surg Neurol 5(3):187–210
Relkin N, Marmarou A, Klinge P, Bergsneider M, Black PM (2005) Diagnosing idiopathic normal-pressure hydrocephalus. Neurosurgery 57(3):S4-16
Martín-Láez R, Caballero-Arzapalo H, López-Menéndez LÁ, Arango-Lasprilla JC, Vázquez-Barquero A (2015) Epidemiology of idiopathic normal pressure hydrocephalus: a systematic review of the literature. World neurosurgery 84(6):2002–2009. https://doi.org/10.1016/j.wneu.2015.07.005
Andersson J, Rosell M, Kockum K, Lilja-Lund O, Söderström L, Laurell K (2019) Prevalence of idiopathic normal pressure hydrocephalus: a prospective, population-based study. PLoS ONE 14(5):e0217705. https://doi.org/10.1371/journal.pone.0217705
Nakajima M, Yamada S, Miyajima M, Ishii K, Kuriyama N, Kazui H, Kanemoto H, Suehiro T, Yoshiyama K, Kameda M, Kajimoto Y, Mase M, Murai H, Kita D, Kimura T, Samejima N, Tokuda T, Kaijima M, Akiba C, Kawamura K, Atsuchi M, Hirata Y, Matsumae M, Sasaki M, Yamashita F, Aoki S, Irie R, Miyake H, Kato T, Mori E, Ishikawa M, Date I, Arai H (2021) Guidelines for management of idiopathic normal pressure hydrocephalus (third edition): endorsed by the japanese society of normal pressure hydrocephalus. Neurol Med Chir (Tokyo) 61(2):63–97. https://doi.org/10.2176/nmc.st.2020-0292
Bonney PA, Briggs RG, Wu K, Choi W, Khahera A, Ojogho B, Shao X, Zhao Z, Borzage M, Wang DJJ, Liu C, Lee DJ (2022) Pathophysiological mechanisms underlying idiopathic normal pressure hydrocephalus: a review of recent insights. Frontiers aging neurosci 14:866313. https://doi.org/10.3389/fnagi.2022.866313
Halperin JJ, Kurlan R, Schwalb JM, Cusimano MD, Gronseth G, Gloss D (2015) Practice guideline: idiopathic normal pressure hydrocephalus: response to shunting and predictors of response: report of the guideline development, dissemination, and implementation subcommittee of the american academy of neurology. Neurology 85(23):2063–2071. https://doi.org/10.1212/wnl.0000000000002193
Williams MA, Malm J (2016) Diagnosis and treatment of idiopathic normal pressure hydrocephalus. Continuum (Minneap Minn). https://doi.org/10.1212/con.0000000000000305
Isik AT, Kaya D, Ates Bulut E, Dokuzlar O, Soysal P (2019) The outcomes of serial cerebrospinal fluid removal in elderly patients with idiopathic normal pressure hydrocephalus. Clin Interv Aging 14:2063–2069. https://doi.org/10.2147/cia.S228257
Kaya D, AT I, (2018) The significance of cerebral comorbidities in idiopathic normal pressure hydrocephalus. Biomed J Sci Tech Res. https://doi.org/10.26717/BJSTR.2018.06.001340
Nikaido Y, Urakami H, Akisue T, Okada Y, Katsuta N, Kawami Y, Ikeji T, Kuroda K, Hinoshita T, Ohno H, Kajimoto Y, Saura R (2019) Associations among falls, gait variability, and balance function in idiopathic normal pressure hydrocephalus. Clin Neurol Neurosurg 183:105385. https://doi.org/10.1016/j.clineuro.2019.105385
Kaya D, Erken N, Ontan MS, Altun ZS, Isik AT (2020) The applause sign in elderly patients with idiopathic normal pressure hydrocephalus. Appl Neuropsychol Adult. https://doi.org/10.1080/23279095.2020.1818563
Ates Bulut E, Soysal P, Isik AT (2018) Frequency and coincidence of geriatric syndromes according to age groups: single-center experience in Turkey between 2013 and 2017. Clin Interv Aging 13:1899–1905. https://doi.org/10.2147/cia.s180281
Cruz-Jentoft AJ, Bahat G, Bauer J (2019) Sarcopenia: revised European consensus on definition and diagnosis. Age ageing. https://doi.org/10.1093/ageing/afy169
Dost FS, Ates Bulut E, Dokuzlar O, Kaya D, Mutlay F, Yesil Gurel BH, Isik AT (2022) Sarcopenia is as common in older patients with dementia with lewy bodies as it is in those with Alzheimer’s disease. Geriatr Gerontol Int 22(5):418–424. https://doi.org/10.1111/ggi.14383
Dost FS, Erken N, Ontan MS, Ates Bulut E, Kaya D, Kocyigit SE, Dokuzlar O, Aydin AE, Isik AT (2022) Muscle strength seems to be related to the functional status and severity of dementia in older adults with Alzheimer’s disease. Curr Aging Sci. https://doi.org/10.2174/1573411018666220616114641
Tsekoura M, Kastrinis A, Katsoulaki M, Billis E, Gliatis J (2017) Sarcopenia and its impact on quality of life. Adv Exp Med Biol 987:213–218. https://doi.org/10.1007/978-3-319-57379-3_19
Xu J, Reijnierse EM, Pacifico J, Wan CS, Maier AB (2021) Sarcopenia is associated with 3-month and 1-year mortality in geriatric rehabilitation inpatients: RESORT. Age Ageing 50(6):2147–2156. https://doi.org/10.1093/ageing/afab134
Hsu YH, Liang CK, Chou MY, Liao MC, Lin YT, Chen LK, Lo YK (2014) Association of cognitive impairment, depressive symptoms and sarcopenia among healthy older men in the veterans retirement community in southern Taiwan: a cross-sectional study. Geriatr Gerontol Int 14(Suppl 1):102–108. https://doi.org/10.1111/ggi.12221
Schaap LA, van Schoor NM, Lips P, Visser M (2018) Associations of sarcopenia definitions, and their components, with the incidence of recurrent falling and fractures: the longitudinal aging study Amsterdam. J Gerontol A Biol Sci Med Sci 73(9):1199–1204. https://doi.org/10.1093/gerona/glx245
Ontan MS, Dokuzlar O, Ates Bulut E, Soysal P, Isik AT (2021) The relationship between osteoporosis and sarcopenia, according to EWGSOP-2 criteria, in outpatient elderly. J Bone Miner Metab 39(4):684–692. https://doi.org/10.1007/s00774-021-01213-6
Knutsson E, Lying-Tunell U (1985) Gait apraxia in normal-pressure hydrocephalus: patterns of movement and muscle activation. Neurology 35(2):155–160. https://doi.org/10.1212/wnl.35.2.155
Stolze H, Kuhtz-Buschbeck JP, Drücke H, Jöhnk K, Diercks C, Palmié S, Mehdorn HM, Illert M, Deuschl G (2000) Gait analysis in idiopathic normal pressure hydrocephalus–which parameters respond to the CSF tap test? Clin Neurophysiol 111(9):1678–1686. https://doi.org/10.1016/s1388-2457(00)00362-x
Matsuoka T, Iida JI, Kawahara M, Uchiyama Y (2016) Investigation and clinical applications of muscle strength change in cerebrospinal fluid tap test in cases of idiopathic normal pressure hydrocephalus: A retrospective study. J Neurol Sci 371:18–23. https://doi.org/10.1016/j.jns.2016.10.009
Canaslan K, Ates Bulut E, Kocyigit SE, Aydin AE, Isik AT (2022) Predictivity of the comorbidity indices for geriatric syndromes. BMC Geriatr 22(1):440. https://doi.org/10.1186/s12877-022-03066-8
Unutmaz GD, Soysal P, Tuven B, Isik AT (2018) Costs of medication in older patients: before and after comprehensive geriatric assessment. Clin Interv Aging 13:607–613. https://doi.org/10.2147/cia.s159966
Guigoz Y, Lauque S, Vellas BJ (2002) Identifying the elderly at risk for malnutrition. the mini nutritional assessment. Clin Geriatr Med 18(4):737–757. https://doi.org/10.1016/s0749-0690(02)00059-9
Ates Bulut E, Soysal P, Dokuzlar O, Kocyigit SE, Aydin AE, Yavuz I, Isik AT (2020) Validation of population-based cutoffs for low muscle mass and strength in a population of Turkish elderly adults. Aging Clin Exp Res. https://doi.org/10.1007/s40520-019-01448-4
Janssen I, Heymsfield SB, Baumgartner RN (1985) Ross R (2000) estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol (Bethesda, Md : 1985) 89(2):465–471
Owler BK, Momjian S, Czosnyka Z, Czosnyka M, Péna A, Harris NG, Smielewski P, Fryer T, Donovan T, Coles J, Carpenter A, Pickard JD (2004) Normal pressure hydrocephalus and cerebral blood flow: a PET study of baseline values. J Cereb Blood Flow Metab 24(1):17–23. https://doi.org/10.1097/01.Wcb.0000093326.88757.49
Wang Z, Zhang Y, Hu F, Ding J, Wang X (2020) Pathogenesis and pathophysiology of idiopathic normal pressure hydrocephalus. CNS Neurosci Ther 26(12):1230–1240. https://doi.org/10.1111/cns.13526
Manini TM, Hong SL, Clark BC (2013) Aging and muscle: a neuron’s perspective. Curr Opin Clin Nutr Metab Care 16(1):21–26. https://doi.org/10.1097/MCO.0b013e32835b5880
Tarkowski E, Tullberg M, Fredman P, Wikkelsö C (2003) Normal pressure hydrocephalus triggers intrathecal production of TNF-alpha. Neurobiol Aging 24(5):707–714. https://doi.org/10.1016/s0197-4580(02)00187-2
Khoo HM, Kishima H, Tani N, Oshino S, Maruo T, Hosomi K, Yanagisawa T, Kazui H, Watanabe Y, Shimokawa T, Aso T, Kawaguchi A, Yamashita F, Saitoh Y, Yoshimine T (2016) Default mode network connectivity in patients with idiopathic normal pressure hydrocephalus. J Neurosurg 124(2):350–358. https://doi.org/10.3171/2015.1.Jns141633
Chistyakov AV, Hafner H, Sinai A, Kaplan B, Zaaroor M (2012) Motor cortex disinhibition in normal-pressure hydrocephalus. J Neurosurg 116(2):453–459. https://doi.org/10.3171/2011.9.Jns11678
Morley JE (2021) Sarcopenia and the Brain. Arq Neuropsiquiatr 79(5):373–375. https://doi.org/10.1590/0004-282X-ANP-2021-e005
Wolfsegger T, Topakian R (2017) Cognitive impairment predicts worse short-term response to spinal tap test in normal pressure hydrocephalus. J Neurol Sci 379:222–225. https://doi.org/10.1016/j.jns.2017.06.028
Hamilton R, Patel S, Lee EB, Jackson EM, Lopinto J, Arnold SE, Clark CM, Basil A, Shaw LM, **e SX, Grady MS, Trojanowski JQ (2010) Lack of shunt response in suspected idiopathic normal pressure hydrocephalus with Alzheimer disease pathology. Ann Neurol 68(4):535–540. https://doi.org/10.1002/ana.22015
Carson RG (2018) Get a grip: individual variations in grip strength are a marker of brain health. Neurobiol Aging 71:189–222. https://doi.org/10.1016/j.neurobiolaging.2018.07.023
Black PM (1980) Idiopathic normal-pressure hydrocephalus. results of shunting in 62 patients. J Neurosurg 52(3):371–377. https://doi.org/10.3171/jns.1980.52.3.037
Stolze H, Kuhtz-Buschbeck JP, Drücke H, Jöhnk K, Illert M, Deuschl G (2001) Comparative analysis of the gait disorder of normal pressure hydrocephalus and Parkinson’s disease. J Neurol Neurosurg Psychiatry 70(3):289–297. https://doi.org/10.1136/jnnp.70.3.289
Said HM, Kaya D, Yavuz I, Dost FS, Altun ZS, Isik AT (2022) A Comparison of cerebrospinal fluid beta-amyloid and tau in idiopathic normal pressure hydrocephalus and neurodegenerative dementias. Clin Interv Aging 17:467–477. https://doi.org/10.2147/cia.S360736
Acknowledgements
The authors thank Idil Yavuz for the valuable statistical support.
Author information
Authors and Affiliations
Contributions
AEA: Conceptualization, Methodology, Data Curation, Writing—Original Draft; FSD: Data Curation, Formal analysis, Writing; DK: Conceptualization, Writing—Original Draft; EAB: Conceptualization, Methodology, Writing—Review & Editing; FM: Data Curation, Writing—Original Draft; ATI: Conceptualization, Writing—Review & Editing, Supervision.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Ethical approval
The study was approved by the ethics committee for Non-Interventional Studies. Informed consent was taken from all participants or parents/legal guardians. The study conformed to the ethical norms and standards in the Declaration of Helsinki.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Aydin, A.E., Dost, F.S., Kaya, D. et al. Sarcopenia in older patients with idiopathic normal pressure hydrocephalus: an observational study from a single geriatric clinic in Turkey. Acta Neurol Belg (2024). https://doi.org/10.1007/s13760-024-02583-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13760-024-02583-0