REVIEW Neurology Series Editor, Wil[iam J. Mu[[atly, MD

Gait Disorders 6i)c'o.,tt"'t Jessica M. Baker, MD Deparlnrcnt of Neurologt, Brighatn and Women's Hospital, Boston, Mass.

ABSTRACI

Walking is an extraordinarily complex task requiring integration of the entire nervous system, making gait susceptible to a variety of underlying neurologic abnormalities. Gait disorders are particularly prevalent in the elderly and increase fall risk. In this review we discuss an approach to the examination ofgait and high- light key features of common gait disorders and their underlying causes. We review gaits due to lesions of motor systems (spasticity and neuromuscular weakness), the cerebellum and sensory systems (), par- kinsonism, and frontal lobes and discuss the remarkably diverse phenomenology of functional (psychogenic) gait disorders. We offer a pragmatic approach to the diagnosis and management of neurologic gait disor- ders, because prompt recognition and intervention may improve quality of life in affected individuals.

A 2U 8 Elsevier Inc. All rights reserved. . The American Jountal of Medicine (201 8) 1 31 , 602407

KEYW0RDS: Ataxia; Foot drop; Frontal gait; Functional ; Gait disorders; Parkinsonism; Spasticiry

Gait disorders are common. contribute significantly to mor- PHYSIOLOGY AND THE GAIT CYCLE bidity through falls,r and may yield clues to diseases occurring Normal gait requires precise control of limb movements, at all locations of the nervous system, making the examina- posture, and muscle tone, an extraordinarily complex process tion of gait one of the most complex and high-yield that involves the entire nervous system. Specialized groups components of the neurologic examination. In this review we of neurons in the spinal cord and brainstem generate rhyth- offer a pragmatic approach to examining gait and discuss clin- mic activity and provide output to motor neurons, which in ical features of common gait disorders and their underlying turn activate muscles in the limbs. The cerebral cortex inte- etiologies. Abnormal gait is particularly prevalent in the elderly, grates input from visual, vestibular, and proprioceptive systems; affecting approximately I in 3 community-dwelling indi- additional input is received from the brainstem, , viduals older than 60 years. Gait disorders in this population cerebellum, and afferent neurons carrying proprioceptive are associated with diminished quality of life2 and nursing signals from muscle stretch receptors (as may be damaged home placementr and may be an indicator of progression to in peripheral neuropathy). Together, these systems allow in- dementia in individuals with mild cognitive impairment.a A dividuals to walk not only in a straight, unencumbered line history that includes weakness of the legs, imbalance, un- but to adapt their gait to avoid obstacles and adjust posture steadiness on one's feet, or multiple falls may hint at an to maintain balance.5 Abnormalities of any portion of the underlying gait disorder. Prompt recognition, examination, nervous system can therefore give rise to a gait disorder. and classification of gait disolders is therefore of para- The gait cycle (Figure 1) begins when one heel (illus- mount importance. trated here as right) strikes the ground. Supported by the stance of the right leg, body weight shifts forward as the left leg flexes at the hip and knees and swings forwards, eventually strik- ing the left heel on the ground. Weight then shifts forwards Funding: None. Conflict of Interestl None. on the left leg, while the right leg swings forward and again Authorship: The author is solely responsiblc for the content of the manu- strikes the ground. Thus, while one leg is in srarce phase, script. JMB's current affiliaiion is: Department of Medicine, University of the opposite is in swing phase. Periods of double support, Wisconsin Hospital and Clinics. Madison. during which both legs make contact with the ground, nor- Requests for reprints should be addresscd to Jessica M. Baker, MD, Uni- mally comprise approximately lOVo of the gait cycle6 but versity of Wisconsin Hospital and Clinics, Department of Medicine, I 111 Highland Avenue, WIMR 3rd floor, Madison, WI 53705. increase as compensation for unsteadiness in many abnor- E-mail address: [email protected] mal gaits.

0002-9343/5 - see liont matter O 2018 Elsevier Inc. All rights reserved. https://doi.org/ 10. l0 I 6/j.am_imed.20l 7. I 1.0-5 1 Baker Gait Disorders 603

EXAMINATION OF GAIT CLINICAL FEATURES AND ETIOLOGY OF The examination of gait begins with observing a patient as GAIT DISORDERS he or she walks from the waiting a.rea to an examination room. Gait disorders may be neurologic or nonneurologic in origin. The ideal setting for a formal gait examination is a long, un- Common nonneurologic causes of abnomal gait include os- cluttered hallway, providing enough distance to reach a teoarthritis of the hip and knee, orthopedic deformities, and comfortable speed with good arm swing. Hands visual lossr; individuals may reduce should be free except for neces- the stance time of the aff'ected lirnb sary assistive devices. Observe to reduce pain, resulting in an asym- individuals as they walk in a straight metric cttttolgic gnil. Common Iine, but also note any difficulty Gait disorders increase fa[L risk and often neurologic causes of abnr-rrmal gaits rising from a chair. initiating gait. resuLt from an undertying neurotogic are listed in the Tairle and are de- or turning. The gait examination condition. scribed here irr fufther detail. Mildly provides significant insight into an shortened step length, decreased ve- gaits resutt individual's functional status, and Specific features of abnormaI locity, slightly widened base, and much will be missed if the assess- from a combination of a deficit and at- increased double support time are ment is limited to the examination tempts at compensation. features ofnonnal agingT but are also (dis- in- room! Make note of velctcity Many gait disorders are readity treat- seen as a response to perceived tance covered in a given time) and stability, either intrinsic (eg, able with specific therapies, such as cadence (steps per miwte). Stride disequilibrium) or extrinsic (eg, dopaminergic therapy for Parkinson's length meastres distance covered by walking on ice). Individuals may disease, or cerebrospjnaI ftuid shunt- the gait cycle; step length mea- walk with hands outstretched in an pressure hydrocephaLus. sures the distance covered during ing for normal attempt to steady themselves. This the swing phase of a single leg. Srep and assistive devices coutictus gait is nonspecific but may width or ba.se is the distance may improve mobility and decrease fa[[ herald an underlying neurologic gait between the left and right feet while risk. disorder. walking (F'igure 2). Also make note of posture, arm swing, the height of each step, leg stiffness, or side-to- side lurching. Muscle strength and tone in the legs, sensation, Spastic gaits are caused by lesions in the corticospinal tract and reflexes rnay provide further clues as to the etiology of at any level and may be unilateral or bilateral. When unilat- an underlying gait disorder. The Romberg sign is tested by eral, the affected Ieg is held in extension and plantar flexion; asking patients to stand still with feet together and eyes closed the ipsilateral arm is often flexed. There is circumduction of and is considered positive (abnormal) if eye closure pro- the affected leg during the swing phase of each step. Common vokes a fall. Test tandem gait by asking a patient to take at causes include or other unilateral lesions of the cere- Ieast 10 steps touching heel-to-, as if walking on a tight- bral cortex. If bilateral, thc spastic gait may appear stifl-- rope. Heel or toe walking can unmask subtle distal weakness legged or scissoring owing to increased tone in the adductor that might be missed by direct confrontational testing. muscles, such that the legs nearly touch with each step

Right LeftToe Left Leg Left Heel RightToe RightIA Leg Right l-teel AIIAIHeel Strike Off Swing Strike Off Swing Strike

Figure 1 The gait cycle. Right leg is shaded grey. The gait cycle is divided into stance and swing phases. During stance, body weight shifts forward on the supporting leg, while the opposite leg swings forward, eventually making contact with the ground via the heel. Shaded blxes indicate periods of double support, during which both the left and right legs make contact with the ground. 604 The American Journa[ of Medicine, VoL 131, No 6, June 2018

Gait cycle

Stepf 6S, widthJ . (\-,'?-=----.-':s SteP length Q

Stride length

Figure 2 Terminology describing the gait cycle. Reproduced with permission from Pirker and Katzenschlager.6

(Figure 3B). Common causes of bilateral spastic gait (spastic often have difficulty rising from a chair without using their paraparesis) include , cervical spondylotic my- arTns. elopathy, and , among many others, and are The steppage gair is caused by weakness of ankle dorsi- often accompanied by signs of myelopathy, such as bowel flexion, also known as afoot drop. Individuals with a steppage and bladder dysfunction, increased reflexes, and Babinski sigrs. gait lift the swinging leg higher to compensate for the ' Antispasticity agents such as baclofen or tizanidine are vari- inability to clear the ground with each step; the foot landing ably effective in improving gait but may reduce painful . often has a slapping quality. Weakness of ankle dorsiflexion Botulinum toxin injections may be useful in cases of focal may be appreciated by direct testing on physical examina- spasticity. tion, though more subtle weakness may be elicited when an individual is asked to walk on his or her heels. Foot drop may be bilateral, as can be seen in peripheral polyneuropathy, or Neuromuscular Gaits unilateral. Common causes include an L5 radiculopathy or Weakness of muscles of the lower extremities may manifest peroneal neuropathy, which can be differentiated from the as a gait disorder. The waddling gait can be seen in cases of former by preservation of ankle inversion on physical exam- proximal muscle weakness, such as myopathy. In normal gait ination. Electromyography with nerve conduction studies may the gluteal muscles serve to stabilize the pelvis, elevating the aid in diagnosis. Individuals with foot drop may benefit from non-weight-bearing side with each step. With weakness of ankle foot orthoses, which stabilize the ankle in a neutral these muscles, and particularly the gluteus medius, instabil- position. ity of the weight-bearing hip instead causes the non-weight- bearing side to drop (Trendelenburg's sign). This leads to excessive side-to-side trunk motion, giving the gait a wad- The parkinsonian gait is among the most common gait dis- dling appearance.E Individuals with proximal muscle weakness orders in the elderly. The classic "shuffling" appearance is

Table Prevatence of Neurotogic Gait Disorders in L17 Community-Dwetting Adutts Neurotogic Gait Disorder (GD) Number (Percentage)* TotaI Numberl Causes (Number)

Sing[e neurotogic GD 81 (6e.2) 5ensory ataxic 22 (18) 46 PeripheraI sensory neuropathy (46) Parki nsonian te (76.2) 34 Parkinson's disease (18), drug-induced parkinsonism (8), other (4) FrontaI e (7.7) 31 Vascutar disease (20), normaL pressure hydrocephdtus (1), dementia (7), other (3) Cerebeltar ataxic 7 (6,0) 10 Stroke (3), multipLe scterosis (1), essentiaI (3), chronic atcohoI abuse (1), other (2) Cautious 7 (6.0) 7 Idiopathic (7) Pa retic/hypoto ni c 6 (5.1) 1,4 Lumbar spinal stenosis (7), peripherat nerve injury (5). other (3) Spastic 6 (5.1) 7 Ischemic stroke (3), intracerebraI hemorrhage (3), congenitat (1) 0ther 5 (4.3) 10 Vestibutar disease (6), dyskinetic (4) Muttipte neurotogic GD 36 (30.8) TotaI 1,77

Modified and used with permission from Mahtknecht P., Kiecht S., Btoem 8.R., Wittei J., Scherfter C., Gasperi A., Rungger G., Poewe W., Seppi K. Prev- alence a nd burden of gait disorders in etderly men and women aged 90-97 yea rs: a population-based study. PLoS 0NE. 2o13;82e69627 . *Percentage represents individuats with a singte gait disorder as a proportion of the entire study population. tTotal number of individuats with each gait disorder, includes individuats with muttiple causes of gait disorders, For examp[e, 22 of 777 individuats had an isolated sensory ataxic gait disorder, 24 individuals had and an addjtional neurologic gait disorder. Baker Gait Disorders 605

(_,.--\la-J.\L 4- ,4 freezing but also occurs independently and further contrib- a\-!--- -rS q# utes to fall risk.t6 A. Normal Cerebeltar Ataxic Gait lrsions of the cerebellum cause irregular, uncoordinated move- B. Spastic ments called ataxia. Ataxia of the limbs (appendicular ataxia, -4 *4€ .* 4u as might be assessed with finger-nose-finger testing) is typ- d*- c=-&.^lE *6_# ically caused by lesions of the cerebellar hemispheres, whereas qf\G*<# ataxia ofgait (truncal ataxia) is caused by midline lesions of \

Sensory Ataxic Gait caused by a decrease in both step length and height; posture (limb joint po- is stooped, arm swing is reduced, and the base is narrow to Individuals with deflcits of proprioception and nornal (Figure 3D). Parkinsonian turns are characterizedby sition sense) are unable to sense the position of their feet relative ground, gait. simultaneous rotation of the head, trunk, and pelvis, the so- to the resulting in an unsteady The stance called en bloc turn: in normal individuals. the head rotates is wide-based, with a shortened step length and stomping quality first, followed by the trunk then pelvis.e Parkinson's disease as the foot hits the ground. Visual cues may partial- is typically asymmetric at onset, so arrn swing and step length ly compensate for proprioceptive deficits, so affected are diminished more on the affected side. Asymmetric shuf- individuals often look down at their feet while walking. Gait fling can often be heard as scuffing of one foot more than therefore worsens dramatically in the dark or with eyes closed, the other. A parkinsonian (resting) tremor may activate during a feature useful for differentiating sensory from cerebellar present. gaits walking. Step length, velocity, arm swing, and turning speed ataxia. Romberg's sign is Sensory ataxic are t0 peripheral improve with dopaminergic treatment. commonly caused by lesions of nerves or the dorsal columns of the spinal cord, such as with syphilis or vitamin Freezing of gait and festinatior are features of more ad- position and sense are vanced Parkinson's disease. Freezing is defined as "an episodic B12 deficiency. Joint vibratory dimin- ished in loss suggests inability (lasting seconds) to generate effective stepping" the lower extremities; of reflexes the presence of a peripheral neuropathy. Many patients improve despite the intention to walk.rr Affected individuals feel as physical if their feet are stuck to the floor. often associated with al- with therapy.ls ternating trembling of the legs. Freezing is commonly seen while initiating gait, tuming, or approaching a destination but FrontaI Gait can also be provoked by features ofone's environment, such Higher-level gait disorders encompass a class of gaits not tz as narrow hallways, doorways, or even large crowds. Freez- caused by lesions ofthe corticospinal tract, basal ganglia, cer- ing is a major contributor to fall risk.13 Freezing may improve ebellum, or neuromuscular systems.'' Among the most with optimization of dopaminergic medications. If freezing corrmon of higher-level gait disorders is the frontal gait, typ- persists despite medication adjustment, symptoms may improve ically caused by Iesions of the frontal lobes (Figure 3E). with visual or auditory cueing. For example, individuals may Impaired balance is a core feature, and like cerebellar and avoid or overcome freezing by consciously stepping over a sensory ataxia, step width is also widened. Step length is de- line on the floor, or marching to the beat of a metronome. A creased and variable, and step height is diminished. Failure laser line produced by an attachment to a cane or walker may to initiate gait is a prominent feature, feet may appear glued be a particularly effective intervention.ra't5 Festination de- to the floor when an individual attempts to begin walking, a scribes a phenomenon in which steps become increasingly feature that may also occur in isolation.re Freezing with turns rapid and short, so that gait takes on the appearance ofrunning. is common. These features lead to the classic description of The center of gravity moves forward. Festination may precede this gait as "magnetic." Common causes include microvas- 606 The American Journal of Medicine, Vot 131, No 6, June 2018

cular white matter disease, vascular or neurodegenerative ACKNOWLEDGMENTS dementias, and normal pressure hydrocephalus (NPH), the I thank Dr. Lewis Sudarsky for insightful comments on an latter of which may be accompanied by cognitive decline and early draft of this review. urinary incontinence and should be excluded by imaging. Only a small proportion of individuals with NPH present with the complete triad, so suspicion should be high in the setting of References enlarged ventricles and a compatible gait disorder. Gait ab- l. Guideline for the prevention of falls in older persons. American Geri- normalities are an early feature of NPH and are also the most atrics Society. British Geriatrics Society, and American Academy of Onhopaedic Surgeons Panel on Falls Prevention. J Am Geriatr Soc. likely to respond to cerebrospinal fluid shunting.20 For indi- 2001 :49(5):664-672. doi: I 0. 10461j.1532-5415.2001.49 I 15.x. gaits other than NPH, viduals with frontal from disorders 2. Mahlknecht P, Kiechl S, Bloem BR, et al. Prevalence and burden of physical therapy and assistive devices may improve ambulation gait disorders in elderly men and women aged 60-97 years: a population- and decrease fall risk. based study. P Lo S O N E. 2013 :8(7 ):e69627. doi: I 0. I 37 l/journal.pone .0069627. 3. Verghese J, LeValley A, Hall CB, Katz MJ, Ambrose AF, Lipton RB. Functiona[ (Psychogenic) Gait Disorder Epidemiology of gait disorders in community-residing older adults. J

e i r I I j.l I Functional gait disorders, formerly referred to as "psycho- A m G r a r S o c, 2006;54(2) :255-261. doi : 0. I I I I 532- 54 5.2005 .00580.x. genic," frequently co-occur with other functional neurologic 4. Montero-Odasso MM, Sarquis-Adamson Y, Speechley M, et al. Asso- disorders and are common in clinical practice. Though their ciation of dual-task gait with incident dementia in mild cognitive presentation is heterogeneous, functional gait disorders are impairment: results from the gait and brain study. JAMA Neurol. typically abrupt in onset, fluctuate over time, and are both 2017',7 4(7 ):857 -865. doi : I 0. I 00 I /jamaneurol.20 I 7.0643. of gait: from the spinal cord to the suggestible and easily distractible. Common patterns include 5. Takakusaki K. Neurophysiology frontal lobe. Mov Disord. 2013:.28(ll):1483-1491. doi:10.1002/ excessive slowing of gait or buckling of the knees, usually mds.25669. without falls.2r Abnormal twisting or muscle contractions may 6. Pirker W, Katzenschlager R. Gait disorders in adults and the elderly: a superficially resemble dystonia. Astasia-abasia describes an clinical guide. Wien KI in Wochenschr. 2016:129:8|-95. doi: I 0. I007/ inability to stand or walk without support, despite ability to s00508-016-1096-4. otherwise use the legs normally. Bizarre, inefflcient pos- 7. Aboutorabi A. Arazpour M, Balramizadeh M, Hutchins SW, FadayevaLm R. The effect of aging on gait parameters in able-bodied older sub- tures that appear unsteady yet do not result in falls are another jects: a literature review. Aging Clin Exp Res.2016:28(3):393-405. are feature of functional gait disorders.22 Mood disorders doi: I 0. I 007/s40520-01 5-0420-6. present in a substantial number of patients but are not re- 8. RopperAH, Samuels MA, Klein JP. Chapter7. Disorders of stance and quired for diagnosis.2l gait. In: Ropper AH, Samuels MA, Klein JP, erJs. Principles of Neu- I}tb ed. New York, NY: McGaw-Hill; 2011:ll5-126. The diagnosis of a functional gait disorder should be made robg.'-. 9. Hong M. Perlmutter JS, Earhart GM. A kinematic and electromyo- not purely by exclusion of organic disease but by positive iden- graphic analysis of turning in people with Parkinson disease. Neurorehabil tification of internal inconsistencies or distractibility. For Neural Repair. 2009;23(2):166- I 76. doi: 10. I 177 /1545968308320639. example, functional gait disorders or postural instability may 10. Smulders K, Dale ML, Carlson-Kuhta P, Nutt JG, Horak FB. normalize when an individual is asked to walk while talking Pharmacological treatment in Parkitrson's disease: eft'ects on gait. Pur- on the phone. Sharing these inconsistent features with the kinsonism Re lat D isord. 20 t 613 I :3- I 3. doi: I 0. I 0 I 6/j.parkreldis.20 16 .07.006. patient highlights their potential reversibility and may be ther- I l. Giladi N, Nieuwboer A. Understanding and treating freezing of gait in apeutic. Communicating the diagnosis should focus more on parkinsonism, proposed working definition, and setting the stage. Mov positive features than diseases that have been excluded and Di so t d. 2O08 :23(suppl 2):5423-5425. doi: I 0. I 002 I mds.2 I 927 . emphasize mechanism over etiology. The metaphor of "a 12. Nutt JG, Bloem BR, Giladi N, Hallett M, Horak FB, Nieuwboer A. problem with the software, not the hardware" may be par- Freezing of gait: moving tbrward on a mysterious clinical phenome- non. L.tncet Neurol. 2011;10(8):734-744. doi:10.1016/51474 involves a ticularly effective.2r Treatment often -4422(11)7Ot43-0. multidisciplinary team of neurologists and psychiatrists; 13. Kerr GK, Worringham CJ, Cole MH, Lacherez PF, Wood JM, Silburn consensus-based guidelines for physical therapy have been PA. Predictors of future falls in Parkinson disease. Neurology. published.2a 2010;7 5(2): I I 6-124. doi:10.1212/!VNL.0b0 I 3e3 I 8 I e7b688. 14. McCandless PJ. Evans BJ. Janssen J. Selfe J, Churchill A, Richards J. Effect of three cueing devices for people with Parkinson's disease with

gait initiation difficulties. G o i t Post ure. 20 I 6:44:7 - | I . doi: I 0. 10 t 6/ CONCLUSIONS j.gaitpost.20 I 5. I 1.006. 15. Donovan S, Lim C, Diaz N, et al. Laserlight cues for gait freezing in Gait disorders are a major source of disability, morbidity, and Parkinson's disease: an open-label sludy. Purkinsortism Relat Disotd. or mortality in the elderly and may be neurologic 20ll',17 (4):240-245. doi: 10.101 6/j.parkreldis.20l 0.08.01 0. nonneurologic in origin. When neurologic in origin, gait dis- 16. Ebersbach G, Moreau C, Gandor F, Defebvre L, Devos D. Clinical syn- orders may arise from lesions in any part of the nervous dromes: Parkinsonian gait. Mov Disord. 2O13;28(l 1):1552-1559. system. This review has provided an overview of the clini- doi : I 0. 1002/mds.25675. 17. Timmann D, Brandauer B, Hermsdijrfer J, et al. l-esion-symptom mapping cal features of various gait disorders, emphasizing clinical of the h urnan cerebel lu m. C e re b e I I u m. 2tJ08l'7 (4) :602-606. doi : I 0. I 007/ features allowing for prompt recognition, offering an oPpor- sl23ll-008-0066-4. tunity fbr effective intervention and improvement in quality I 8. Baker JM, Sudarsky L. Gait disorders, balance and falls. In: Jameson of life. JL, Fauci AS. Kasper DL, Hauser SL, Longo DL, Loscalzo J, eds. Baker Gait Disorders 607

Harrisons Principks of Internal Medicine.20th ed. New York NY: 22. l-nmpert T, Brandt T, Dieterich M, Huppert D. How to identify psy- McGraw-Hill; 2017:l-20,2018. [Chapter 23]. In press. chogenic disorders of stance and gait. A video study in 37 patients. .I 19. Nuft JG, Marsden CD, Thompson PD. Human walking and higherJevel N eurol. l99l ;238(3): 140- 146. gait disoders, particularly in the elderly. Neurulogy. 1993;43Q):268-279. 23. Stone J. Functional neurological disorders: the neurological assess- 20. Klassen BT, Ahlskog JE. Normal pressure hydrocephalus: how often ment as treatment. Neurophysiol Clin. 2016;16(l):7 -17. doi:.10.11361 does the diagnosis hold water? Ne urolo gy. 2011 ;77 (12):1119- 1125. practneurol-20 I 5 -00l24l .

doi : I 0. 1 2 I 2AIINL .Ofi 13 e3 I 822tu2f5. 24. Nielsen G, Stone J, Matthews A, et al. Physiotherapy for functional 21. Baik JS, Lang AE. Gait abnormalities in psychogenic movement dis- motor disorders: a consensus recommendation. J Neurol Neurosurg orders. Mov Disord. 200'l :22(3):395-399. doi: 10.1002:/mds.21283. Psychiatry. 2015;86(10):1113-ll 19. doi:10.1136/jnnp-2014-309255.