Website Edition: April/May 2012

Understanding Gait in Aging: Finding the way forward: Part 1

Contributed by Richard Camicioli and Caterina Rosano

Related Articles

Introduction

Gait disorders are common both with aging and in the setting of specific neurological disorders and are a risk factor for dependence, cognitive decline, falls and death. After age 70 years, 35% of people have abnormal gait (1); after the age 85 years gait changes are found in the majority of people. Therefore, gait change is as common as cognitive syndromes including mild cognitive impairment and dementia. While gait changes, specifically slowing and decreased stride length are common occurrence in older people, the presence of gait abnormalities suggests overt or covert pathologies (2). Both nervous system and non-nervous system changes (e.g., cardiorespiratory and musculoskeletal changes) contribute to age-related changes in gait. New molecular and imaging research tools and the recognition of neural systems involved in cognitive and motor function are opening the door to better understand the mechanisms of gait change in vivo.

The New 'Classic' Approach to Gait Disorders

The classic neurological approach to localization allows for the identification of levels of involvement leading to gait impairment. Nutt and colleagues rekindled this Sherringtonian approach in a seminal paper published in Neurology (3). Importantly these authors highlighted evidence for gait disorders that are not explained by basic sensori-motor deficits, termed high-level gait disorders in contrast to lower level and middle level disorders. With aging, changes at each level occur conspiring to reduce mobility. Common spatio-temporal changes that can be attributed to changes from various neurological disorders include slowing, decreased stride-length, a slightly widened base and decreased ground clearance. (4). Some of these features can be accounted for by shortened stride length, but in pathological disorders changes include reduced cadence (5). A recent review summarized and operationalized the clinical approach to analysis of gait impairment (6).

"Lower level" changes, include loss of muscle function, which can be caused by muscle or neuromuscular junction dysfunction (7). The term saropenia refers to muscle mass loss with aging. Sarcopenia, associated with muscle wasting and weakness, is one of the components of one definition of frailty that additionally includes weakness, exhaustion, decreased activity, and slowed walking (8). Loss of muscle mass is also seen with motor neuron loss may occur with progressive pathological loss found in amyotrophic lateral sclerosis, wherein gait change include contributions from both weakness and pyramidal system involvement (9). In older people changes may be significant enough to justify a specific diagnosis but may occur at a sub-clinical level as well.

Basic visual, vestibular and peripheral nerve function all contribute to maintaining balance and are critical to effective mobility. At the level of the peripheral nerve, neuropathy is common in older people, most commonly associated with diabetes or glucose intolerance, which can itself be challenging to detect. Visual and vestibular changes also occur with aging and can be a component of age-related mobility decline (10).

At the "middle level" Parkinson and Huntington diseases are the paradigmatic basal ganglia disorders. Early in the course Parkinson disease, gait is characterized by bradykinesia, with short stride length and slowing, distinct from other middle level gait disorders (11). As PD evolves freezing of gait occurs, which might be considered a "higher level" disorder. Alternate diagnoses, such as progressive supranuclear palsy, multiple system atrophy, normal pressure hydrocephalus and vascular parkinsonism are considerations if there is early freezing. Primary progressive freezing of gait can be an isolated phenomenon, albeit with varied pathology (12). Gait in Huntington disease at the earlier diagnostic stage features chorea and dystonia superimposed on relatively normal gait, but quantitative studies show changes in spatiotemporal characteristics (such as slowing, decreased stride length, increased base-width and increased step to step variability) over time, that is evident even in pre-manifest gene carriers (13). Clinical and subclinical cerebrovascular disease can lead to hemiparesis and paraparesis which are associated with signs of upper motor neuron dysfunction. Spinal cord lesions typically lead to a more straight-forward spastic gait with added contributions from sensory impairment. These changes lead to decreased mobility. Cerebellar gait is characterized by variable stepping; however increased variability in timing or step length can occur at multiple levels (14). Interestingly the gait in people with essential tremor shows features that overlap with cerebellar disorders (15). Increased gait variability is a feature that can be also seen with sub-cortical white matter disease, whether due to a vascular or non-vascular etiology (i.e., multiple sclerosis). The basis and "localization" of variability in gait parameters remains to be fully understood.

"High level" gait disorders, alternatively termed frontal-subcortical gait disorder, or gait apraxia (a term which is not favored) are not completely understood. Features that indicate a higher order gait disorder include disequilibrium unexplained by basic sensori-motor deficits, problems initiation or maintaining stepping (freezing), and difficulty with appropriate foot placement when standing up or walking. These deficits can be brought out when adaptation is demanded (stopping and starting, turning, changing directions) and ultimately impede locomotion. These deficits can be amplified by performing a simultaneous cognitive task (dual-tasking).

Increased variability may represent a higher level problem since gait variability is related to cognitive decline (16). Further evidence for variability being at least partially mediated by cognition is the impact of dual-tasking (performing a simultaneous cognitive task while walking) on gait variability, which is particularly evident in people with mild cognitive impairment and dementia (17).

Fear of falling can sometimes lead to odd gaits. For example individuals might walk as if they are on ice. (18). Less extreme cautious gait patterns can also be observed. Some of the changes seen in typical aging may represent appropriate adaptations to sensori-motor changes of aging. At the extreme, psychogenic gait disorders may represent a higher level gait problem related to volitional or subconscious implementation of an abnormal walk. These don't generally fit with recognizable gait patterns (19).

Summary

The phenomenological approach to gait disorders is important from a clinical perspective. Disease models may provide some insight into age-related changes. A full understanding of the mechanisms of gait dysfunction will require an integrative approach that takes descriptive and quantitative aspects of gait and links to neural and non-neural processes. Current imaging tools (see companion piece) are providing novel insights. Without a doubt these will evolve. Although animal models cannot fully recapitulate human bipedal walking they too will be helpful in providing mechanistic insights.

Table: Pathological and age-related neurological changes that might contribute to gait impairment in older people.

Level Specific Anatomic Localization Pathology Age-related correlate Gait Characteristics/
Associated Findings
Lower Muscle Myopathy Sarcopenia Waddling, slow/ Weakness, difficutlty rising from a chair
  Neuromuscular Junction Myasthenia gravis Neuromuscular junction dysfunction with aging Slow, weak, fatiguable/
Oculomotor impairment, ptosis, fatiguable proximal weakness
  Peripheral Nerve Neuropathy Sensorimotor changes with aging Slow, wide-based, steppage/
Hyporeflexia, weakness, senory deficit
  Motor neuron Amyotrophic lateral sclerosis Motor neuron loss Slow, spastic/
Upper and lower motor neuron signs
Middle White Matter Stroke, White matter disease Neurovascular coupling Increased variability, shortened stride length, wide based/
Hyperreflexia, pyramidal sighs
  Basal Ganglia Parkinson disease (Lewy body disease) Parkinsonism Decreased stride length, narrow base/
Bradykinesia, rigidity, tremor
  Basal Ganglia Huntington Disease “Senile” chorea Variable base, flinging movements with chorea superimposed/
Cognitive impairment, chorea
  Cerebellar Alcoholism, Multiple System Atrophy, Spinocerebellar ataxias, Essential tremor Age-related cerebellar atrophy Wide-based variable gait/Neuropathy (Alcohol), Parkinsonism and autonomic features (MSA)
High Frontal-subcortical gait Vascular, Progressive Supranuclear Palsy (PSP), Late Parkinson Disease, Normal Pressure Hydrocephalus Most likely related to pathology Impaired foot placement and stepping, Wide or variable base, dysquilibrium/
Cognitive impairment, frontal release signs, Vertical gaze palsy (PSP), pyramidal findings
  Gait Ignition Failure Vascular, PSP, Late Parkinson’s Disease, Normal Pressure Hydrocephalus Patient with extreme cautious gait Inability to initiate walking, getting stuck on turns or after stopping. Festination/
Signs consistent with diagnosis, but can be seen in isolation
  Cautious Gait Fear of Falling Slowing with aging, to a lesser degree than seen with fear of falling Very slow walking, needing to hold onto items to walk/
Anxiety, Normal physical exam

Understanding Gait: References

  1. Verghese J, LeValley A, Hall CB, Katz MJ, Ambrose AF, Lipton RB. Epidemiology of gait disorders in community-residing older adults. J Am Geriatr Soc. 2006 Feb;54(2):255-61.
  2. Bloem BR, Haan J, Lagaay AM, van Beek W, Wintzen AR, Roos RA. Investigation of gait in elderly subjects over 88 years of age. J Geriatr Psychiatry Neurol. 1992 Apr-Jun;5(2):78-84.
  3. Nutt JG, Marsden CD, Thompson PD.Human walking and higher-level gait disorders, particularly in the elderly. Neurology. 1993 Feb;43(2):268-79.
  4. Elble RJ, Hughes L, Higgins C.The syndrome of senile gait. J Neurol. 1992 Feb;239(2):71-5.
  5. Elble RJ, Thomas SS, Higgins C, Colliver J. Stride-dependent changes in gait of older people. J Neurol. 1991 Feb;238(1):1-5.
  6. Snijders AH, van de Warrenburg BP, Giladi N, Bloem BR.Neurological gait disorders in elderly people: clinical approach and classification. Lancet Neurol. 2007 Jan;6(1):63-74.
  7. Clark DJ, Fielding RA. Neuromuscular contributions to age-related weakness. J Gerontol A Biol Sci Med Sci. 2012 Jan;67(1):41-7.
  8. Sternberg SA, Wershof Schwartz A, Karunananthan S, Bergman H, Mark Clarfield A. The identification of frailty: a systematic literature review. J Am Geriatr Soc. 2011 Nov;59(11):2129-38.
  9. Inam S, Vucic S, Brodaty NE, Zoing MC, Kiernan MC.The 10-metre gait speed as a functional biomarker in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2010 Dec;11(6):558-61.
  10. Callisaya ML, Blizzard L, Schmidt MD, McGinley JL, Lord SR, Srikanth VK.A population-based study of sensorimotor factors affecting gait in older people. Age Ageing. 2009 May;38(3):290-5.
  11. Ebersbach G, Sojer M, Valldeoriola F, Wissel J, Müller J, Tolosa E, Poewe W. Comparative analysis of gait in Parkinson's disease, cerebellar ataxia and subcortical arteriosclerotic encephalopathy. Brain. 1999 Jul;122 ( Pt 7):1349-55.
  12. Factor SA, Higgins DS, Qian J. Primary progressive freezing gait: a syndrome with many causes. Neurology. 2006 Feb 14;66(3):411-4.
  13. Rao AK, Mazzoni P, Wasserman P, Marder K. Longitudinal Change in Gait and Motor Function in Pre-manifest Huntington's Disease. PLoS Curr. 2011 Oct 4;3:RRN1268.
  14. Rao AK, Gillman A, Louis ED.Quantitative gait analysis in essential tremor reveals impairments that are maintained into advanced age. Gait Posture. 2011 May;34(1):65-70.
  15. Stolze H, Klebe S, Petersen G, Raethjen J, Wenzelburger R, Witt K, Deuschl G. Typical features of cerebellar ataxic gait. J Neurol Neurosurg Psychiatry. 2002 Sep;73(3):310-2.
  16. Beauchet O, Thiery S, Gautier J, Fantino B, Annweiler C, Allali G.Association between high variability of gait speed and mild cognitive impairment: a cross-sectional pilot study. J Am Geriatr Soc. 2011 Oct;59(10):1973-4.
  17. Muir SW, Speechley M, Wells J, Borrie M, Gopaul K, Montero-Odasso M. Gait assessment in mild cognitive impairment and Alzheimer's disease: the effect of dual-task challenges across the cognitive spectrum. Gait Posture. 2012 Jan;35(1):96-100.
  18. Balash Y, Hadar-Frumer M, Herman T, Peretz C, Giladi N, Hausdorff JM. The effects of reducing fear of falling on locomotion in older adults with a higher level gait disorder. J Neural Transm. 2007;114(10):1309-14.
  19. Baik JS, Lang AE. Gait abnormalities in psychogenic movement disorders. Mov Disord. 2007 Feb 15;22(3):395-9.

About Dr. Rosano, MD, MPH

Dr. Rosano, MD

Dr. Rosano has obtained her MD from the School of Medicine, Palermo, Italy, in 1995 and her Master in Epidemiology from the Graduate School of Public Health at the University of Pittsburgh in 2003. Dr. Rosano is the PI of the e-BRAIN research group (http://www.epidemiology.pitt.edu/rosano.asp).

The E-BRAIN group investigates the interactions and synergisms between brain structure and function in relationship with mobility impairment in aging. In the E-BRAIN projects, Dr. Rosano applies cutting-edge neuroimaging technology to precisely identify early subclinical markers of brain abnormalities in large population studies with comprehensive information on health-related factors and determinants of mobility impairment. Accordingly, Dr. Rosano’s work integrates three complementary approaches: a) quantify markers of brain abnormalities related to slowing in cognitive and physical domains; b) characterize the mechanisms underlying these relationships; c) identify the modifiable risk factors and causes of such brain changes.

“The results of these projects have the potential to augment our understanding of brain aging and l contribute to the discovery of new approaches to the promotion of survival free from disabilities.” – Dr. Rosano

About Dr. Richard Camicioli, MD

Richard CamicioliRichard Camicioli is a Geriatric Neurologist with an interest in both cognitive and movement disorders. He obtained his MDCM from McGill University in 1987 and completed his neurology residency at McGill in 1991. He then began a VA Fellowship in Geriatric Neurology at the Oregon Health and Sciences University and the Portland VA Medical Center. He then developed an interest in the relationship between motor function and cognition.

This led to work with the Oregon Brain Aging study. Since coming to the University of Alberta, he has focused on cognitive decline in people with Parkinson’s disease and has continued work with older “controls”. Recently he has rekindled studying people with mild cognitive impairment in order to define clinically distinct phenotypes.