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Neuropsychology Review

, Volume 28, Issue 2, pp 176–187 | Cite as

A Systematic Review of Cognition in Chiari I Malformation

  • Jeffrey M. RogersEmail author
  • Greg Savage
  • Marcus A. Stoodley
Review

Abstract

Displacement of the cerebellar tonsils in Chiari type I malformation (CMI) can affect functions controlled by the cerebellum and brainstem. While playing an integral role in the control of movement, the cerebellum also has widespread cortical connections, influencing a range of cognitive process. A systematic literature review was conducted to examine the relationship between cognition and CMI, assessing evidence for general or domain-specific cognitive change. The search protocol examined the AMED, CINAHL, Cochrane Library, EMBASE, MEDLINE, PsycINFO, and Scopus databases. Articles meeting the following criteria were included in this review (i) examined children or adults with a clinically defined diagnosis of CMI, (ii) assessed cognitive function with a prospective examination, (iii) included at least one standardized instrument designed to measure general or specific domains of cognitive function, and (iv) were published in English in a peer-reviewed journal. Twelve articles were identified, including 783 cases aged 3 months to 64 years. General cognition, processing speed, and learning and memory appeared less affected, while language deficits appeared to diminish with age. Executive dysfunction was the most commonly reported cognitive impairment, while attention and working memory, and visuospatial and perceptual skills also appeared vulnerable. Numerous methodological limitations were identified that should be considered in interpreting the impact of CMI and planning future investigations. Overall, there is currently insufficient evidence to describe a valid and reliable profile of cognitive impairment in CMI. Further research is required to confirm these preliminary psychometric results and integrate them with pathophysiological models

Keywords

Arnold Chiari malformation Cognition Neuropsychological test Systematic review 

Abbreviations

CCAS

cerebellar cognitive affective syndrome

CMI

Chiari type I malformation

CSF

cerebrospinal fluid

Notes

Funding

This work was supported by a grant from the Column of Hope.

Compliance with Ethical Standards

Conflict of Interest

The authors have no conflicts of interest to report.

References

  1. Abbott, D., Brockmeyer, D., Neklason, D. W., Teerlink, C., & Cannon-Albright, L. A. (2017). Population-based description of familial clustering of Chiari malformation type I. Journal of Neurosurgery, 128, 460–465.  https://doi.org/10.3171/2016.9.jns161274.CrossRefPubMedGoogle Scholar
  2. Abd-Elfattah, H. M., Abdelazeim, F. H., & Elshennawy, S. (2015). Physical and cognitive consequences of fatigue: a review. Journal of Advanced Research, 6(3), 351–358.  https://doi.org/10.1016/j.jare.2015.01.011.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Allen, P. A., Houston, J. R., Pollock, J. W., Buzzelli, C., Li, X., Harrington, A. K., et al. (2014). Task-specific and general cognitive effects in Chiari malformation type I. PLoS One, 9(4), e94844.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Allen, P. A., Delahanty, D., Kaut, K. P., Li, X., Garcia, M., Houston, J. R., et al. (2017). Chiari 1000 registry project: assessment of surgical outcome on self-focused attention, pain, and delayed recall. Psychological Medicine, 1–11.  https://doi.org/10.1017/s0033291717003117.
  5. Arnautovic, A., Splavski, B., Boop, F. A., & Arnautovic, K. I. (2015). Pediatric and adult Chiari malformation type I surgical series 1965-2013: a review of demographics, operative treatment, and outcomes. Journal of Neurosurgery: Pediatrics, 15(2), 161–177.  https://doi.org/10.3171/2014.10.peds14295.PubMedCrossRefGoogle Scholar
  6. Arnett, B. (2003). Arnold-Chiari malformation. Archives of Neurology, 60(6), 898–900.  https://doi.org/10.1001/archneur.60.6.898.CrossRefPubMedGoogle Scholar
  7. Aydin, S., Hanimoglu, H., Tanriverdi, T., Yentur, E., & Kaynar, M. Y. (2005). Chiari type I malformations in adults: a morphometric analysis of the posterior cranial fossa. Surgical Neurology, 64(3), 237–241.  https://doi.org/10.1016/j.surneu.2005.02.021.CrossRefPubMedGoogle Scholar
  8. Bawor, M., Dennis, B. B., Anglin, R., Steiner, M., Thabane, L., & Samaan, Z. (2014). Sex differences in outcomes of methadone maintenance treatment for opioid addiction: a systematic review protocol. Systematic Reviews, 3, 45.  https://doi.org/10.1186/2046-4053-3-45.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Belio, C., Prouteau, A., Koleck, M., Saada, Y., Merceron, K., Dayre, E., et al. (2014). Participation restrictions in patients with psychiatric and/or cognitive disabilities: preliminary results for an ICF-derived assessment tool. Annals of Physical and Rehabilitation Medicine, 57(2), 114–137.  https://doi.org/10.1016/j.rehab.2013.11.005.CrossRefPubMedGoogle Scholar
  10. Bernard, J. A., Leopold, D. R., Calhoun, V. D., & Mittal, V. A. (2015). Regional cerebellar volume and cognitive function from adolescence to late middle age. Human Brain Mapping, 36(3), 1102–1120.  https://doi.org/10.1002/hbm.22690.CrossRefPubMedGoogle Scholar
  11. Bernard, J. A., Orr, J. M., & Mittal, V. A. (2016). Differential motor and prefrontal cerebello-cortical network development: evidence from multimodal neuroimaging. Neuro Image, 124(Pt A), 591–601.  https://doi.org/10.1016/j.neuroimage.2015.09.022.PubMedCrossRefGoogle Scholar
  12. Buoni, S., Zannolli, R., di Bartolo, R. M., Donati, P. A., Mussa, F., Giordano, F., & Genitori, L. (2006). Surgery removes EEG abnormalities in patients with Chiari type I malformation and poor CSF flow. Clinical Neurophysiology, 117(5), 959–963.  https://doi.org/10.1016/j.clinph.2006.01.019.CrossRefPubMedGoogle Scholar
  13. Caykoylu, A., Ekinci, O., Albayrak, Y., Kuloglu, M., & Deniz, O. (2008). Arnold-Chiari I malformation association with generalized anxiety disorder: a case report. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 32(6), 1613–1614.  https://doi.org/10.1016/j.pnpbp.2008.05.018.CrossRefGoogle Scholar
  14. Chamberlain, S. R., & Sahakian, B. J. (2006). The neuropsychology of mood disorders. Current Psychiatry Reports, 8(6), 458–463.CrossRefPubMedGoogle Scholar
  15. Chisholm, B. T., Velamoor, R., Chandarana, P. C., & Cochrane, D. K. (1993). Anxiety disorder in a case of Arnold-Chiari malformation. Journal of Psychiatry & Neuroscience, 18(2), 67–68.Google Scholar
  16. Cormack, F. K., Taptiklis, N., Abbott, R. A., Anatürk, M., Cartland, I., Coppieters, L., et al. (2016). Changes to validity of online cognitive assessment in young and older adults: a comparison to supervised testing using the Cantab battery. Alzheimer's & Dementia, 12(7), P286–P287.  https://doi.org/10.1016/j.jalz.2016.06.520.CrossRefGoogle Scholar
  17. Cowan, N. (2008). What are the differences between long-term, short-term, and working memory? Progress in Brain Research, 169, 323–338.  https://doi.org/10.1016/s0079-6123(07)00020-9.CrossRefPubMedPubMedCentralGoogle Scholar
  18. Del Casale, A., Serata, D., Rapinesi, C., Simonetti, A., Tamorri, S. M., Comparelli, A., et al. (2012). Psychosis risk syndrome comorbid with panic attack disorder in a cannabis-abusing patient affected by Arnold-Chiari malformation type I. General Hospital Psychiatry, 34(6), e5–e7.Google Scholar
  19. deSouza, R. M., Zador, Z., & Frim, D. M. (2011). Chiari malformation type I: related conditions. Neurological Research, 33(3), 278–284.  https://doi.org/10.1179/016164111x12962202723922.CrossRefPubMedGoogle Scholar
  20. Diamond, A. (2000). Close interrelation of motor development and cognitive development and of the cerebellum and prefrontal cortex. Child Development, 71(1), 44–56.CrossRefPubMedGoogle Scholar
  21. Dupont, W. D. (1988). Power calculations for matched case-control studies. Biometrics, 44(4), 1157–1168.CrossRefPubMedGoogle Scholar
  22. Elster, A. D., & Chen, M. Y. (1992). Chiari I malformations: clinical and radiologic reappraisal. Radiology, 183(2), 347–353.  https://doi.org/10.1148/radiology.183.2.1561334.CrossRefPubMedGoogle Scholar
  23. Fischbein, R., Saling, J. R., Marty, P., Kropp, D., Meeker, J., Amerine, J., & Chyatte, M. R. (2015). Patient-reported Chiari malformation type I symptoms and diagnostic experiences: a report from the national Conquer Chiari patient registry database. Neurological Sciences, 36(9), 1617–1624.  https://doi.org/10.1007/s10072-015-2219-9.CrossRefPubMedGoogle Scholar
  24. Frisoni, G. B., Fratiglioni, L., Fastbom, J., Guo, Z., Viitanen, M., & Winblad, B. (2000). Mild cognitive impairment in the population and physical health: data on 1,435 individuals aged 75 to 95. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 55(6), M322–M328.CrossRefPubMedGoogle Scholar
  25. Gabrielli, O., Coppa, G. V., Manzoni, M., Carloni, I., Kantar, A., Maricotti, M., & Salvolini, U. (1998). Minor cerebral alterations observed by magnetic resonance imaging in syndromic children with mental retardation. European Journal of Radiology, 27(2), 139–144.CrossRefPubMedGoogle Scholar
  26. Godil, S. S., Parker, S. L., Zuckerman, S. L., Mendenhall, S. K., & McGirt, M. J. (2013). Accurately measuring outcomes after surgery for adult Chiari I malformation: determining the most valid and responsive instruments. Neurosurgery, 72(5), 820–827.  https://doi.org/10.1227/NEU.0b013e3182897341.CrossRefPubMedGoogle Scholar
  27. Grosso, S., Scattolini, R., Paolo, G., Di Bartolo, R. M., Morgese, G., & Balestri, P. (2001). Association of Chiari I malformation, mental retardation, speech delay, and epilepsy: a specific disorder? Neurosurgery, 49(5), 1099–1103.PubMedGoogle Scholar
  28. Guell, X., Gabrieli, J. D. E., & Schmahmann, J. D. (2017). Embodied cognition and the cerebellum: Perspectives from the Dysmetria of Thought and the Universal Cerebellar Transform theories. Cortex.  https://doi.org/10.1016/j.cortex.2017.07.005.
  29. Haapanen, M. L. (2007). CHERI: time to identify the syndrome? The Journal of Craniofacial Surgery, 18(2), 369–373.  https://doi.org/10.1097/scs.0b013e3180336075.CrossRefPubMedGoogle Scholar
  30. Iwabuchi, K., Miyauchi, T., Kyuuma, Y., Hosaka, H., Kunimi, Y., & Yagishita, S. (1985). A sudden-death in a case of Arnold-Chiari malformation (type I) with sleep apnea. Nō to Shinkei, 37(6), 575–581.PubMedGoogle Scholar
  31. Klein, R., Hopewell, C. A., & Oien, M. (2014). Chiari malformation type I: a neuropsychological case study. Military Medicine, 179(6), e712–e718.  https://doi.org/10.7205/milmed-d-13-00227.CrossRefPubMedGoogle Scholar
  32. Koziol, L. F., Budding, D. E., & Chidekel, D. (2012). From movement to thought: executive function, embodied cognition, and the cerebellum. Cerebellum, 11(2), 505–525.  https://doi.org/10.1007/s12311-011-0321-y.CrossRefPubMedGoogle Scholar
  33. Krishna, V., Sammartino, F., Yee, P., Mikulis, D., Walker, M., Elias, G., & Hodaie, M. (2016). Diffusion tensor imaging assessment of microstructural brainstem integrity in Chiari malformation Type I. Journal of Neurosurgery, 125(5), 1112–1119.  https://doi.org/10.3171/2015.9.jns151196.CrossRefPubMedGoogle Scholar
  34. Kumar, M., Rathore, R. K. S., Srivastava, A., Yadav, S. K., Behari, S., & Gupta, R. K. (2011). Correlation of diffusion tensor imaging metrics with neurocognitive function in Chiari I malformation. World Neurosurgery, 76(1–2), 189–194.  https://doi.org/10.1016/j.wneu.2011.02.022.CrossRefPubMedGoogle Scholar
  35. Kurtcan, S., Alkan, A., Yetis, H., Tuzun, U., Aralasmak, A., Toprak, H., & Ozdemir, H. (2017). Diffusion tensor imaging findings of the brainstem in subjects with tonsillar ectopia. Acta Neurologica Belgica.  https://doi.org/10.1007/s13760-017-0792-9.
  36. Lacy, M., Ellefson, S. E., DeDios-Stern, S., & Frim, D. M. (2016). Parent-reported executive dysfunction in children and adolescents with Chiari malformation Type 1. Pediatric Neurosurgery, 51(5), 236–243.  https://doi.org/10.1159/000445899.CrossRefPubMedGoogle Scholar
  37. Ladner, T. R., Westrick, A. C., Wellons 3rd, J. C., & Shannon, C. N. (2016). Health-related quality of life in pediatric Chiari Type I malformation: the Chiari Health Index for Pediatrics. Journal of Neurosurgery: Pediatrics, 17(1), 76–85.  https://doi.org/10.3171/2015.5.peds1513.PubMedCrossRefGoogle Scholar
  38. Leung, V., Magnussen, J. S., Stoodley, M. A., & Bilston, L. E. (2016). Cerebellar and hindbrain motion in Chiari malformation with and without syringomyelia. Journal of Neurosurgery: Spine, 24(4), 546–555.  https://doi.org/10.3171/2015.8.spine15325.PubMedCrossRefGoogle Scholar
  39. Lezak, M. D., Howieson, D. B., Bigler, E. D., & Tranel, D. (2012). Neuropsychological assessment (5th ed.). New York: Oxford University Press.Google Scholar
  40. Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gotzsche, P. C., Ioannidis, J. P., et al. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. Journal of Clinical Epidemiology, 62(10), e1–34.  https://doi.org/10.1016/j.jclinepi.2009.06.006.CrossRefPubMedGoogle Scholar
  41. Mackenzie, I. S., Morant, S. V., Bloomfield, G. A., MacDonald, T. M., & O'Riordan, J. (2014). Incidence and prevalence of multiple sclerosis in the UK 1990-2010: a descriptive study in the general practice research database. Journal of Neurology, Neurosurgery, and Psychiatry, 85(1), 76–84.  https://doi.org/10.1136/jnnp-2013-305450.CrossRefPubMedGoogle Scholar
  42. Mahgoub, N., Avari, J., & Francois, D. (2012). A case of Arnold-Chiari malformation associated with dementia. Journal of Neuropsychiatry and Clinical Neurosciences, 24(2), E44–E45.CrossRefPubMedGoogle Scholar
  43. Meadows, J., Kraut, M., Guarnieri, M., Haroun, R. I., & Carson, B. S. (2000). Asymptomatic Chiari Type I malformations identified on magnetic resonance imaging. Journal of Neurosurgery, 92(6), 920–926.  https://doi.org/10.3171/jns.2000.92.6.0920.CrossRefPubMedGoogle Scholar
  44. Meeker, J., Amerine, J., Kropp, D., Chyatte, M., & Fischbein, R. (2015). The impact of Chiari malformation on daily activities: a report from the national Conquer Chiari Patient Registry database. Disability and Health Journal, 8(4), 521–526.  https://doi.org/10.1016/j.dhjo.2015.01.003.CrossRefPubMedGoogle Scholar
  45. Mestres, O., Poca, M. A., Solana, E., Radoi, A., Quintana, M., Force, E., & Sahuquillo, J. (2012). Evaluation of the quality of life of patients with a Chiari type I malformation. A pilot study in a cohort of 67 patients. Revista de Neurologia, 55(3), 148–156.PubMedGoogle Scholar
  46. Mirza, S. S., Ikram, M. A., Bos, D., Mihaescu, R., Hofman, A., & Tiemeier, H. (2017). Mild cognitive impairment and risk of depression and anxiety: a population-based study. Alzheimer's & Dementia, 13(2), 130–139.  https://doi.org/10.1016/j.jalz.2016.06.2361.CrossRefGoogle Scholar
  47. Mlinac, M. E., & Feng, M. C. (2016). Assessment of activities of daily living, self-care, and independence. Archives of Clinical Neuropsychology, 31(6), 506–516.  https://doi.org/10.1093/arclin/acw049.CrossRefPubMedGoogle Scholar
  48. Moriarty, O., McGuire, B. E., & Finn, D. P. (2011). The effect of pain on cognitive function: a review of clinical and preclinical research. Progress in Neurobiology, 93(3), 385–404.  https://doi.org/10.1016/j.pneurobio.2011.01.002.CrossRefPubMedGoogle Scholar
  49. Morris, Z., Whiteley, W. N., Longstreth Jr., W. T., Weber, F., Lee, Y. C., Tsushima, Y., et al. (2009). Incidental findings on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ, 339, b3016.  https://doi.org/10.1136/bmj.b3016.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Mueller, D., & Oro, J. J. (2005). Prospective analysis of self-perceived quality of life before and after posterior fossa decompression in 112 patients with Chiari malformation with or without syringomyelia. Neurosurgical Focus, 18(2), ECP2.CrossRefPubMedGoogle Scholar
  51. Novegno, F., Caldarelli, M., Massa, A., Chieffo, D., Massimi, L., Pettorini, B., et al. (2008). The natural history of the Chiari type I anomaly. Journal of Neurosurgery. Pediatrics, 2(3), 179–187.PubMedGoogle Scholar
  52. O'Halloran, C. J., Kinsella, G. J., & Storey, E. (2012). The cerebellum and neuropsychological functioning: a critical review. Journal of Clinical and Experimental Neuropsychology, 34(1), 35–56.  https://doi.org/10.1080/13803395.2011.614599.CrossRefPubMedGoogle Scholar
  53. Öktem, H., Dilli, A., Kürkçüoğlu, A., Soysal, H., Yazici, C., & Pelin, C. (2016). Prevalence of Chiari type I malformation on cervical magnetic resonance imaging: a retrospective study. Anatomy, 10(1), 40–45.CrossRefGoogle Scholar
  54. Payot, A., & Barrington, K. J. (2011). The quality of life of young children and infants with chronic medical problems: review of the literature. Current Problems in Pediatric and Adolescent Health Care, 41(4), 91–101.  https://doi.org/10.1016/j.cppeds.2010.10.008.CrossRefPubMedGoogle Scholar
  55. Riva, D., Usilla, A., Saletti, V., Esposito, S., & Bulgheroni, S. (2011). Can Chiari malformation negatively affect higher mental functioning in developmental age? Neurological Sciences, 32(Suppl 3), S307–S309.  https://doi.org/10.1007/s10072-011-0779-x.CrossRefPubMedGoogle Scholar
  56. Schijman, E. (2004). History, anatomic forms, and pathogenesis of Chiari I malformations. Child's Nervous System, 20(5), 323–328.  https://doi.org/10.1007/s00381-003-0878-y.CrossRefPubMedGoogle Scholar
  57. Schmahmann, J. D. (1991). An emerging concept. The cerebellar contribution to higher function. Archives of Neurology, 48(11), 1178–1187.CrossRefPubMedGoogle Scholar
  58. Schmahmann, J. D. (2004). Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. Journal of Neuropsychiatry and Clinical Neurosciences, 16(3), 367–378.  https://doi.org/10.1176/jnp.16.3.367.CrossRefPubMedGoogle Scholar
  59. Schmahmann, J. D. (2010). The role of the cerebellum in cognition and emotion: Personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychology Review, 20(3), 236–260.  https://doi.org/10.1007/s11065-010-9142-x.CrossRefPubMedGoogle Scholar
  60. Schmahmann, J. D., & Sherman, J. C. (1998). The cerebellar cognitive affective syndrome. Brain, 121(4), 561–579.CrossRefPubMedGoogle Scholar
  61. Shrank, W. H., Patrick, A. R., & Brookhart, M. A. (2011). Healthy user and related biases in observational studies of preventive interventions: a primer for physicians. Journal of General Internal Medicine, 26(5), 546–550.  https://doi.org/10.1007/s11606-010-1609-1.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Smith, B. W., Strahle, J., Bapuraj, J. R., Muraszko, K. M., Garton, H. J., & Maher, C. O. (2013). Distribution of cerebellar tonsil position: implications for understanding Chiari malformation. Journal of Neurosurgery, 119(3), 812–819.  https://doi.org/10.3171/2013.5.jns121825.CrossRefPubMedGoogle Scholar
  63. Speer, M. C., Enterline, D. S., Mehltretter, L., Hammock, P., Joseph, J., Dickerson, M., et al. (2003). Chiari type I malformation with or without syringomyelia: prevalence and genetics. Journal of Genetic Counseling, 12(4), 297–311.CrossRefPubMedGoogle Scholar
  64. Stoodley, C. J., MacMore, J. P., Makris, N., Sherman, J. C., & Schmahmann, J. D. (2016). Location of lesion determines motor vs. cognitive consequences in patients with cerebellar stroke. Neuroimage Clinical, 12, 765–775.  https://doi.org/10.1016/j.nicl.2016.10.013.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Stoverud, K. H., Langtangen, H. P., Ringstad, G. A., Eide, P. K., & Mardal, K. A. (2016). Computational investigation of cerebrospinal fluid dynamics in the posterior cranial fossa and cervical subarachnoid space in patients with Chiari I Malformation. PLoS One, 11(10), e0162938.  https://doi.org/10.1371/journal.pone.0162938.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Strahle, J., Muraszko, K. M., Kapurch, J., Bapuraj, J. R., Garton, H. J., & Maher, C. O. (2011). Chiari malformation Type I and syrinx in children undergoing magnetic resonance imaging. Journal of Neurosurgery: Pediatrics, 8(2), 205–213.  https://doi.org/10.3171/2011.5.peds1121.PubMedCrossRefGoogle Scholar
  67. Strauss, E., Sherman, E. M., & Spreen, O. (2006). A compendium of neuropsychological tests: Administration, norms, and commentary (3rd ed.). New York: Oxford University Press.Google Scholar
  68. Strayer, A. (2001). Chiari I malformation: Clinical presentation and management. Journal of Neuroscience Nursing, 33(2), 90–96.CrossRefPubMedGoogle Scholar
  69. Torkamani, M., Ernst, L., Cheung, L. S., Lambru, G., Matharu, M., & Jahanshahi, M. (2015). The neuropsychology of cluster headache: cognition, mood, disability, and quality of life of patients with chronic and episodic cluster headache. Headache, 55(2), 287–300.  https://doi.org/10.1111/head.12486.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Vernooij, M. W., Ikram, M. A., Tanghe, H. L., Vincent, A. J., Hofman, A., Krestin, G. P., et al. (2007). Incidental findings on brain MRI in the general population. The New England Journal of Medicine, 357(18), 1821–1828.  https://doi.org/10.1056/NEJMoa070972.CrossRefPubMedGoogle Scholar
  71. Waters, F., & Bucks, R. S. (2011). Neuropsychological effects of sleep loss: implication for neuropsychologists. Journal of the International Neuropsychological Society, 17(4), 571–586.  https://doi.org/10.1017/s1355617711000610.CrossRefPubMedGoogle Scholar
  72. Wilkinson, D. A., Johnson, K., Garton, H. J., Muraszko, K. M., & Maher, C. O. (2017). Trends in surgical treatment of Chiari malformation type I in the United States. Journal of Neurosurgery: Pediatrics, 19(2), 208–216.  https://doi.org/10.3171/2016.8.peds16273.PubMedCrossRefGoogle Scholar
  73. Wolf, M. S., Curtis, L. M., Wilson, E. A., Revelle, W., Waite, K. R., Smith, S. G., et al. (2012). Literacy, cognitive function, and health: results of the LitCog study. Journal of General Internal Medicine, 27(10), 1300–1307.  https://doi.org/10.1007/s11606-012-2079-4.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Woodford, H. J., & George, J. (2007). Cognitive assessment in the elderly: a review of clinical methods. QJM, 100(8), 469–484.  https://doi.org/10.1093/qjmed/hcm051.CrossRefPubMedGoogle Scholar
  75. Wu, Y. W., Chin, C. T., Chan, K. M., Barkovich, A. J., & Ferriero, D. M. (1999). Pediatric Chiari I malformations: do clinical and radiologic features correlate? Neurology, 53(6), 1271–1276.CrossRefPubMedGoogle Scholar
  76. Yost, K. J., DeWalt, D. A., Lindquist, L. A., & Hahn, E. A. (2013). The association between health literacy and indicators of cognitive impairment in a diverse sample of primary care patients. Patient Education and Counseling, 93(2), 319–326.  https://doi.org/10.1016/j.pec.2013.07.006.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Jeffrey M. Rogers
    • 1
    Email author
  • Greg Savage
    • 2
  • Marcus A. Stoodley
    • 1
  1. 1.Department of Clinical Medicine, Faculty of Medicine and Health SciencesMacquarie UniversityNew South WalesAustralia
  2. 2.ARC Centre of Excellence in Cognition and its Disorders, Department of PsychologyMacquarie UniversityNew South WalesAustralia

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