Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-25T04:58:23.346Z Has data issue: false hasContentIssue false

Frontal Behavior Syndromes in Idiopathic Normal Pressure Hydrocephalus as a Function of Alzheimer’s Disease Biomarker Status

Published online by Cambridge University Press:  20 May 2020

Madison Niermeyer
Affiliation:
Division of Physical Medicine & Rehabilitation, University of Utah, Salt Lake City, UT
Chad Gaudet
Affiliation:
Department of Psychology, University of Rhode Island, Kingston, RI
Paul Malloy
Affiliation:
Department of Psychiatry and Human Behavior, Warren Alpert Medical School, Brown University, Providence, RI Memory and Aging Program, Butler Hospital, Providence, RI
Irene Piryatinsky
Affiliation:
Department of Psychiatry, Beth Israel Deaconess Medical Center, Boston, MA
Stephen Salloway
Affiliation:
Department of Psychiatry and Human Behavior, Warren Alpert Medical School, Brown University, Providence, RI Memory and Aging Program, Butler Hospital, Providence, RI Department of Neurology, Warren Alpert Medical School, Brown University, Providence, RI
Petra Klinge
Affiliation:
Department of Neurosurgery, Warren Alpert Medical School, Brown University, Providence, RI Lifespan Physician Group, Rhode Island Hospital, Providence, RI
Athene Lee*
Affiliation:
Department of Psychiatry and Human Behavior, Warren Alpert Medical School, Brown University, Providence, RI Memory and Aging Program, Butler Hospital, Providence, RI
*
*Correspondence and reprint requests to: Athene Lee, PhD, Department of Psychiatry and Human Behavior, Warren Alpert Medical School, Brown University, 345 Blackstone Boulevard, Providence, RI02906. E-mail: [email protected]

Abstract

Objectives:

Cognitive impairment and apathy are well-documented features of idiopathic normal pressure hydrocephalus (iNPH). However, research examining other neuropsychiatric manifestations of iNPH is scant, and it is unknown whether the neuropsychiatric presentation differs for iNPH patients with comorbid Alzheimer’s disease (AD) versus iNPH without AD. This study aims to advance our understanding of neuropsychiatric syndromes associated with iNPH.

Methods:

Fifty patients from Butler Hospital’s Normal Pressure Hydrocephalus Clinic met inclusion criteria. Caregiver ratings on the Frontal Systems Behavior Scale (FrSBe) were examined to appraise changes in apathy, executive dysfunction, and disinhibition. Patients also completed cognitive tests of global cognition, psychomotor speed, and executive functioning. AD biomarker status was determined by either amyloid-beta (Aβ) positron emission tomography (PET) imaging or cerebrospinal fluid (CSF) total tau to Aβ-42 ratio.

Results:

Results revealed clinically significant elevations on the FrSBe’s apathy and executive dysfunction scales and modest correlations among these scales and cognitive measures. Of the 44 patients with available neuroimaging or CSF draw data, 14 presented with comorbid AD. Relative to the iNPH-only group, the iNPH + AD group showed a larger increase from pre-illness to current informant ratings on the executive dysfunction scale, but not the apathy or disinhibition scales.

Conclusions:

These results replicate and extend prior research by identifying apathy and executive dysfunction as prominent neuropsychiatric symptoms of iNPH and suggest comorbid AD exacerbates dysexecutive behaviors. Future research is warranted to examine the effects of comorbid AD pathology in response to shunt surgery for iNPH, neuropsychiatric symptom changes, and resultant caregiver burden.

Type
Regular Research
Copyright
Copyright © INS. Published by Cambridge University Press, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adams, R.D., Fisher, C.M., Hakim, S., Ojemann, R.G., & Sweet, W.H. (1965). Symptomatic occult hydrocephalus with normal cerebrospinal-fluid pressure: A treatable syndrome. The New England Journal of Medicine, 273(3), 117126. https://doi.org/20026348CrossRefGoogle ScholarPubMed
Allain, P., Etcharry-Bouyx, F., & Verny, C. (2013). Executive functions in clinical and preclinical Alzheimer’s disease. Revue Neurologique, 169, 695708.10.1016/j.neurol.2013.07.020CrossRefGoogle ScholarPubMed
Allali, G., Laidet, M., Armand, S., Saj, A., Krack, P., & Assal, F. (2017). Apathy and higher level of gait control in normal pressure hydrocephalus. International Journal of Psychophysiology, 119, 127131. doi: 10.1016/j.ijpsycho.2016.12.002CrossRefGoogle ScholarPubMed
Allali, G., Laidet, M., Armand, S., Saj, A., Krack, P., & Assal, F. (2018). Apathy in idiopathic normal pressure hydrocephalus: A marker of reversible gait disorders. International Journal of Geriatric Psychiatry, 33(5), 735742. doi: 10.1002/gps.4847CrossRefGoogle ScholarPubMed
Andreasen, N., Minthon, L., Pia, D., Vanmechelen, E., Vanderstichele, H., Winblad, B., & Blennow, K. (2001). Evaluation of CSF-tau and CSF-Aβ 42 as diagnostic markers for Alzheimer disease in clinical practice. Archives of Neurology, 58, 29.CrossRefGoogle Scholar
Bech-Azeddine, R., Høgh, P., Juhler, M., Gjerris, F., & Waldemar, G. (2007). Idiopathic normal-pressure hydrocephalus: Clinical comorbidity correlated with cerebral biopsy findings and outcome of cerebrospinal fluid shunting. Journal of Neurology, Neurosurgery and Psychiatry, 78(2), 157161. doi: 10.1136/jnnp.2006.095117CrossRefGoogle ScholarPubMed
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57(1), 289300.CrossRefGoogle Scholar
Boyle, P.A., Malloy, P.F., Salloway, S., Cahn-Weiner, D.A., Cohen, R., & Cummings, J.L. (2003). Executive dysfunction and apathy predict functional impairment in Alzheimer disease. American Journal of Geriatric Psychiatry, 11(2), 214221.CrossRefGoogle ScholarPubMed
Chiaravalloti, N.D., & Deluca, J. (2003). Assessing the behavioral consequences of multiple sclerosis: An application of the Frontal Systems Behavior Scale (FrSBe). Cognitive and Behavioral Neurology, 16(1), 5467.CrossRefGoogle Scholar
Clark, C.M., Schneider, J.A., Bedell, B.J., Beach, T.G., Bilker, W.B., Minimi, M., … Skovronsky, D.M. (2011). Use of Florbetapir-PET for imaging P-amyloid pathology. JAMA: The Journal of the American Medical Association, 305(3), 275283.CrossRefGoogle Scholar
Cummings, J.L., Ketchel, P., Ed, M., Shelley, T., Lopez, O.L., & Dekosky, S.T. (2000). Validation of the NPI-Q, a brief clinical form of the Neuropsychiatric Inventory. The Journal of Neuropsychiatry and Clinical Neurosciences, 12(2), 233239.Google Scholar
DeVito, E.E., Salmond, C.H., Owler, B.K., Sahakian, B.J., & Pickard, J.D. (2007). Caudate structural abnormalities in idiopathic normal pressure hydrocephalus. Acta Neurologica Scandinavica, 116(5), 328332. doi: 10.1111/j.1600-0404.2007.00906.xCrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189.CrossRefGoogle ScholarPubMed
Golomb, J., Wisoff, J., Miller, D.C., Boksay, I., Kluger, A., Weiner, H., & Salton, J. (2000). Alzheimer’s disease comorbidity in normal pressure hydrocephalus: Prevalence and shunt response. Journal of Neurology Neurosurgery and Psychiatry, 68(6), 778781. doi: 10.1136/jnnp.68.6.778CrossRefGoogle ScholarPubMed
Gomez-Gallego, M., Gomez-Garcia, J., & Ato-Lozano, E. (2015). Addressing the bias problem in the assessment of the quality of life of patients with dementia: Determinants of the accuracy and precision of the proxy ratings. Journal of Nutrition, Health & Aging, 19(3), 366372.CrossRefGoogle ScholarPubMed
Graff-Radford, N.R. (2014). Alzheimer CSF biomarkers may be misleading in normal-pressure hydrocephalus. Neurology, 83(17), 15731575. doi: 10.1212/WNL.0000000000000916CrossRefGoogle ScholarPubMed
Hong, Y.J., Kim, M.-J., Jeong, E., Kim, J.-E., Hwang, J., Lee, J.-I., … Na, D.L. (2018). Preoperative biomarkers in patients with idiopathic normal pressure hydrocephalus showing a favorable shunt surgery outcome. Journal of the Neurological Sciences, 387(August 2017), 2126. doi: 10.1016/j.jns.2018.01.017CrossRefGoogle ScholarPubMed
Israelsson, H., Allard, P., Eklund, A., & Malm, J. (2016). Symptoms of depression are common in patients with Idiopathic Normal Pressure Hydrocephalus: The INPH-CRasH study. Neurosurgery, 78(2), 161168. doi: 10.1227/NEU.0000000000001093CrossRefGoogle ScholarPubMed
Jang, H., Beom, S., Yeshin, P., Kim, K.W., Lee, J.Il, Tae, S., … Duk, W.Y. (2018). Prognostic value of amyloid PET scan in normal pressure hydrocephalus. Journal of Neurology, 265(1), 6373. doi: 10.1007/s00415-017-8650-5CrossRefGoogle ScholarPubMed
Kanemoto, H., Kazui, H., Suzuki, Y., Sato, S., Kishima, H., Yoshimine, T., & Yoshiyama, K. (2016). Effect of lumbo-peritoneal shunt surgery on neuropsychiatric symptoms in patients with idiopathic normal pressure hydrocephalus. Journal of the Neurological Sciences, 361, 206212. doi: 10.1016/j.jns.2016.01.001CrossRefGoogle ScholarPubMed
Katzen, H., Ravdin, L.D., Assuras, S., Heros, R., Kaplitt, M., Schwartz, T.H., … Relkin, N.R. (2011). Postshunt cognitive and functional improvement in idiopathic normal pressure hydrocephalus. Neurosurgery, 68(2), 416419. doi: 10.1227/NEU.0b013e3181ff9d01CrossRefGoogle ScholarPubMed
Kazui, H., Kanemoto, H., Yoshiyama, K., Kishima, H., Suzuki, Y., Sato, S., … Tanaka, T. (2016). Association between high biomarker probability of Alzheimer’s disease and improvement of clinical outcomes after shunt surgery in patients with idiopathic normal pressure hydrocephalus. Journal of the Neurological Sciences, 369, 236241. doi: 10.1016/j.jns.2016.08.040CrossRefGoogle ScholarPubMed
Keong, N.C., Pena, A., Price, S.J., Czosnyka, M., Czosnyka, Z., Devito, E.E., … Pickard, J.D. (2017). Diffusion tensor imaging profiles reveal specific neural tract distortion in normal pressure hydrocephalus. PLoS ONE, 12(8), 125. doi: 10.1371/journal.pone.0181624CrossRefGoogle ScholarPubMed
Kiel, C. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175191.Google Scholar
Kito, Y., Kazui, H., Kubo, Y., Yoshida, T., Takaya, M., Wada, T., … Takeda, M. (2009). Neuropsychiatric symptoms in patients with idiopathic normal pressure hydrocephalus. Behavioural Neurology, 21(3–4), 165174. doi: 10.3233/BEN-2009-0233CrossRefGoogle ScholarPubMed
Klinge, P.M., Brooks, D.J., Samii, A., Weckesser, E., van den Hoff, J., Fricke, H., … Berding, G. (2008). Correlates of local cerebral blood flow (CBF) in normal pressure hydrocephalus patients before and after shunting—A retrospective analysis of [15O] H2O PET-CBF studies in 65 patients. Clinical Neurology and Neurosurgery, 110(4), 369375. doi: 10.1016/j.clineuro.2007.12.019CrossRefGoogle Scholar
Malloy, P.F., & Grace, J. (2001). Frontal Systems Behavior Scale (FrSBe): Professional Manual. Lutz, FL: Psychological Assessment Resources.Google Scholar
Malloy, P.F., Tremont, G., Grace, J., & Frakey, L. (2007). The Frontal Systems Behavior Scale discriminates frontotemporal dementia from Alzheimer’s disease. Alzheimer’s and Dementia, 3(3), 200203. doi: 10.1016/j.jalz.2007.04.374CrossRefGoogle ScholarPubMed
Marin, R.S. (1990). Differential diagnosis and classification of apathy. American Journal of Psychiatry, 147(1), 2230. doi: 10.1176/ajp.147.1.22Google ScholarPubMed
Mitrushina, M., Boone, K.B., Razani, J., & D’Elia, L.F. (2005). Handbook of Normative Data for Neuropsychological Assessment (2nd ed.). New York, NY: Oxford University Press.Google Scholar
Molinuevo, J.L., Blennow, K., Dubois, B., Engelborghs, S., Lewczuk, P., Perret-Liaudet, A., … Parnetti, L. (2014). The clinical use of cerebrospinal fluid biomarker testing for Alzheimer’s disease diagnosis: A consensus paper from the Alzheimer’s biomarkers standardization initiative. Alzheimer’s & Dementia, 10, 808817.10.1016/j.jalz.2014.03.003CrossRefGoogle ScholarPubMed
Nassar, B.R., & Lippa, C.F. (2016). Idiopathic normal pressure hydrocephalus. Gerontology and Geriatric Medicine, 2, 233372141664370. https://doi.org/10.1177/2333721416643702CrossRefGoogle ScholarPubMed
Norton, L.E., Malloy, P.F., & Salloway, S. (2001). The impact of behavioral symptoms on activities of daily living in patients with dementia. American Journal of Geriatric Psychiatry, 9, 4148.CrossRefGoogle ScholarPubMed
Ogino, A., Kazui, H., Miyoshi, N., Hashimoto, M., Ohkawa, S., Tokunaga, H., … Takeda, M. (2006). Cognitive impairment in patients with idiopathic normal pressure hydrocephalus. Dementia and Geriatric Cognitive Disorders, 21(2), 113119. doi: 10.1159/000090510CrossRefGoogle ScholarPubMed
Ouchi, Y., Nakayama, T., Kanno, T., Yoshikawa, E., Shinke, T., & Torizuka, T. (2007). In vivo presynaptic and postsynaptic striatal dopamine functions in idiopathic normal pressure hydrocephalus. Journal of Cerebral Blood Flow and Metabolism, 27(4), 803810. doi: 10.1038/sj.jcbfm.9600389CrossRefGoogle ScholarPubMed
Owler, B.K., & Pickard, J.D. (2001). Normal pressure hydrocephalus and cerebral blood flow: A review. Acta Neurologica Scandinavica, 104(6), 325342. doi: 10.1034/j.1600-0404.2001.00092.xCrossRefGoogle ScholarPubMed
Paulsen, J.S., Stout, J.C., DeLaPena, R. R., Zeena, T.-R., Swenson, M., & Malloy, P.F. (1996). Frontal behavioral syndromes in cortical and subcortical dementia. Assessment, 3(3), 327357.CrossRefGoogle Scholar
Peterson, K.A., Housden, C.R., Killikelly, C., Devito, E.E., Keong, N.C., Savulich, G., … Sahakian, B.J. (2016). Apathy, ventriculomegaly and neurocognitive improvement following shunt surgery in normal pressure hydrocephalus. British Journal of Neurosurgery, 30(1), 3842. doi: 10.3109/02688697.2015.1029429Google ScholarPubMed
Pfeifer, L., Drobetz, R., Fankhauser, S., Mortby, M.E., Maercker, A., & Forstmeier, S. (2015). Caregiver rating bias in mild cognitive impairment and mild Alzheimer’s disease: Impact of caregiver burden and depression on dyadic rating discrepancy across domains. International Psychogeriatrics, 25(8), 13451355. doi: 10.1017/S1041610213000562CrossRefGoogle Scholar
Puente, A.N., Cohen, M.L., Aita, S., & Brandt, J. (2016). Behavioral ratings of executive functioning explain instrumental activities of daily living beyond test scores in Parkinson’s disease. The Clinical Neuropsychologist, 30, 95106. doi: 10.1080/13854046.2015.1133847CrossRefGoogle ScholarPubMed
Picascia, M., Minafra, B., Zangaglia, R., Gracardi, L., Pozzi, N.G., Sinforiani, E., & Pacchetti, C. (2016). Spectrum of cognitive disorders in idiopathic normal pressure hydrocephalus. Functional Neurology, 31(3), 143148. doi: 10.11138/FNeur/2016.31.3.143Google ScholarPubMed
Ready, R.E., Ott, B.R., Grace, J., & Cahn-Weiner, D.A. (2003). Apathy and executive dysfunction in mild cognitive impairment and Alzheimer disease. American Journal of Geriatric Psychiatry, 11(2), 222228. doi: 10.1097/00019442-200303000-00013CrossRefGoogle ScholarPubMed
Rigamonti, D. (2014). Adult Hydrocephalus. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Rymer, S., Salloway, S., Norton, L., Malloy, P., Correia, S., & Monast, D. (2002). Impaired awareness, behavior disturbance, and caregiver burden in Alzheimer disease. Alzheimer Disease and Associated Disorders, 16(4), 248253. doi: 10.1097/00002093-200210000-00006CrossRefGoogle ScholarPubMed
Schulz, R., Cook, T.B., Beach, S.R., & Lingler, J.H. (2013). Magnitude and causes of bias among family caregivers rating Alzheimer disease patients. The American Journal of Geriatric Psychiatry, 21, 1425. doi: 10.1016/j.jagp.2012.10.002CrossRefGoogle ScholarPubMed
Stout, J.C., Wyman, M.F., Johnson, S.A., Peavy, G.M., & Salmon, D.P. (2003). Frontal behavioral syndromes and functional status in probable Alzheimer disease. American Journal of Geriatric Psychiatry, 11(6), 683686.10.1097/00019442-200311000-00014CrossRefGoogle ScholarPubMed
Stuss, D.T. (2011). Functions of the frontal lobes: Relation to executive functions. Journal of the International Neuropsychological Society, 17(5), 759. doi: 10.1017/S1355617711000695CrossRefGoogle ScholarPubMed
Suchy, Y. (2016). Executive functioning: A comprehensive guide for clinical practice. New York: Oxford Press.Google Scholar
Tekin, S. & Cummings, J.L. (2002). Frontal-subcortical neuronal circuits and clinical neuropsychiatry: An update. Journal of Psychosomatic Research, 53(2), 647654. doi: 10.1016/S0022-3999(02)00428-2CrossRefGoogle ScholarPubMed
Williams, M.A. & Malm, J. (2016). Diagnosis and treatment of idiopathic normal pressure hydrocephalus. Continuum, 57(3), 416. doi: 10.1097/01376517-200704000-00007Google Scholar
Zarit, S., Orr, N.K., & Zarit, J.M. (1985). The hidden victims of Alzheimer's disease: Families under stress. New York, NY: NYU Press.Google Scholar
Zawacki, T.M., Grace, J., Paul, R., Moser, D.J., Ott, B.R., Gordon, N., & Cohen, R.A. (2002). Behavioral problems as predictors of functional abilities of vascular dementia patients. The Journal of Neuropsychiatry and Clinical Neurosciences, 14(3), 296302. doi: 10.1176/jnp.14.3.296CrossRefGoogle ScholarPubMed