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Taiza E. G. Santos-Pontelli

Octávio M. Pontes-Neto

José Fernando Colafêmina

Dráulio B. de Araujo

Antônio Carlos Santos

João P. Leite

Contraversive pushing in non-stroke

patients

JON 1532

Introduction

Contraversive pushing behavior has been considered

one of the most intriguing disorders of postural control

in patients with brain lesions. The pusher syndrome was

first described by Davies who observed that some

hemi-plegic patients, rather than use the unaffected arm to

pull themselves up, extend this arm and actively push

away, toward the paretic side [2]. When sitting or

stand-ing, they lean toward the hemiparetic side and resist

at-tempts at passive correction toward the earth-vertical

upright position [2, 5, 9].

It was at first assumed that the contraversive pushing

was part of a syndrome also encompassing spatial

ne-glect and anosognosia, associated with right

hemi-sphere strokes [2, 5]. However, systematic investigation

in larger series have revealed that the pushing behavior

Received: 12 February 2004

Received in revised form: 3 May 2004 Accepted: 6 May 2004

T. E. G. Santos-Pontelli · O. M. Pontes-Neto, MD · Dr. João P. Leite (쾷)

Dept. of Neurology University of São Paulo

School of Medicine at Ribeirão Preto Ribeirão Preto

J. F. Colafêmina, MD, PhD Division of Otorhinolaringology University of São Paulo School of Medicine Ribeirão Preto, Brazil

A. C. Santos, MD, PhD Dept. of Internal Medicine University of São Paulo School of Medicine Ribeirão Preto, Brazil

D. B. de Araujo, PhD University of São Paulo School of Physics Ribeirão Preto, Brazil

Abstract

Background

Pusher

syndrome is a disorder of postural

control observed in patients with

right or left brain damage

associ-ated with hemiparesis. Those

pa-tients show a peculiar behavior of

actively pushing away from the

nonhemiparetic side and resisting

against passive correction, with a

tendency to fall toward the

para-lyzed side. Thus far this

phenome-non has been exclusively associated

with stroke patients.

Objective

We

investigate the occurrence, imaging

features and clinical evolution of

pusher behavior in patients with

acute encephalic lesions at a

ter-tiary emergency hospital.

Methods

Pusher patients were identified

from 530 inpatients during a 1 year

period. Patients were evaluated

us-ing a standardized Scale for

Con-traversive Pushing (SCP),

neuro-logical examination, assessment of

neuropsychological symptoms,

ac-tivities of daily living function and

neuroimaging studies.

Results We

found eight patients (1.5 %) with

severe contraversive pushing, three

female and five male. Age at

symp-toms onset ranged from 48 to 80

years (mean 65.4). All patients had

scores equal or above 1.5 in each

tested parameter of the SCP. Six

pa-tients (75 %) had right-hemisphere

brain damage. A stroke etiology

was found in four patients. The

other four patients had non-stroke

etiology (three traumatic, one

metastatic tumor). Stroke patients

showed complete recovery of

pusher behavior at a mean

dura-tion of 15.3 weeks. In patients with

brain trauma, pushing behavior

was completely resolved in a mean

time of 5 weeks.

Conclusions The

results demonstrate that

contraver-sive pushing may also occur in

pa-tients with non-stroke neurological

lesions and suggest that resolution

of symptoms may vary according

to the underlying etiology.

Key words

pusher syndrome ·

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can be dissociated from both spatial neglect and

anosognosia and may also occur in left hemisphere

stroke patients [4–6, 9, 10].

Recently, a possible explanation for the pushing

be-havior has been suggested. Pusher patients experience

their body as oriented upright when it is actually tilted

18° to the ipsilesional side, in spite of having normal

function of vestibular and visual systems [4].

Imaging studies from pusher patients with either

right or left sided lesions have shown that the ventral

posterior and lateral posterior nuclei of the

posterolat-eral thalamus are overlapping structures in all cases. A

central role of these nuclei on upright body posture has

been suggested, though additional substrates in the

cor-tex may also be critical [5].

Thus far, the pusher behavior has only been

de-scribed in stroke patients [2–7, 9, 10]. Moreover, the

res-olution of those symptoms has been reported as almost

complete within 6 months [7].

In the present study we investigated the occurrence,

imaging features and clinical evolution of pusher

be-havior in a group of patients with acute brain lesions in

a tertiary emergency hospital. Our investigations

indi-cate that the behavior can be found in association with

non-stroke neurological conditions and that the time

re-quired for the resolution of symptoms may vary

accord-ing to etiology.

Material and methods

Pusher patients were identified from 530 inpatients of a neurological emergency unit at a tertiary hospital of University of São Paulo School of Medicine at Ribeirão Preto, between 1 July 2002 and 30 June 2003. A physical therapist screened patients for any abnormal pos-tural behavior by awaking and putting them in a seated position. If any instability appeared, they were further assessed using a previ-ously standardized Scale for Contraversive Pushing (SCP) based on Davies’ criteria [4, 6]. This scale assesses three distinct aspects of pos-tural control: 1) symmetry of spontaneous posture while sitting and standing, 2) the use of the arm and/or the leg to extend the area of physical contact to the ground while sitting and standing, and 3) re-sistance to passive correction of posture while sitting and standing [4, 6]. Patients were scored as having contraversive pushing if all three criteria were met, reaching a total score of at least 1 in each criterion (sitting plus standing in the 3 situations). The duration of pusher be-havior was defined as the interval between injury onset and the com-plete resolution of symptoms. Evaluation included a full neurological examination, assessment of neuropsychological symptoms of hemi-neglect and anosognosia, activities of daily living (ADL) function and neuroimaging studies (CT and/or MRI). Patients were classified as having spatial neglect when there was clear evidence of a typical clin-ical behavior such as [1] a spontaneous deviation of the head and eyes toward the ipsilesional side, [2] orienting toward the ipsilesional side when addressed from the front or the contralesional side, and [3] ignoring of contralesional located people or objects [5]. Anosognosia was rated by questioning the patient about limb weakness and con-firmed only when no acknowledgement of motor weakness was ob-tained even after confrontation [1]. Activities of daily living (ADL) function was assessed between 5 to 12 months after lesion onset by the Barthel index (BI), which evaluates 10 different abilities and ranges a total score from 0 to 100 points [8].

Neuroimaging was performed to establish the etiology and topog-raphy of brain lesions. The side and extension of the lesion was de-termined by combining clinical and neuroimage data. CT or MRI was performed as early as possible according to the accessibility of the scanner and the patient’s clinical condition. CT was performed on a Somatom ARC equipment (Siemens, Erlangen, Germany), with 512×512 matrix, continuous 5 mm slice thickness on the posterior fossa and 10 mm slice thickness in the supratentorial region. MRI was performed on a 1.5-T superconductor system (Siemens, Vision Plus, Erlangen Germany), with 25 mT gradients, using a circular polarized head coil. The acquisition protocol included whole brain coverage with a T2-weighted axial turbo spin-echo sequence (SE), T1-weighted axial SE, T2 fluid attenuation inversion-recovered coronal sequence, and a 3D time-of-flight MR angiography, at minimum. All images were reported and reviewed by two neuroradiologists.

This study was approved by the ethics committee of our institu-tion.

Results

Among 530 inpatients we found eight (1.5 %) with

se-vere contraversive pushing, three female and five male.

Table 1 describes their demographic, clinical

character-istics and outcome. The age at symptom onset ranged

from 48 to 80 years (mean 65.4). Investigation for

push-ing behavior was performed within a mean of 31.7 days,

with a range of 13 to 60 days after hospital admission.

Patients stayed at the hospital for an average of 36.7 days

(range = 8 to 57 days). Two of them (patients 5 and 6)

were transferred to a secondary hospital after discharge.

Hypesthesia was observed in four patients, while six

of them showed spatial neglect. All patients had scores

equal or above 1.5 in each tested parameter of the SCP.

Six patients (75 %) had right-hemisphere brain damage,

two (25 %) had left-sided lesions.

A stroke etiology was found in four patients (three

is-chemic, one with intraparenchymal hemorrhage). In the

other four patients severe contraversive pushing was

as-sociated with non-stroke etiologies (described below).

Patient 5, a 62 year-old institutionalized male with a

previous history of epilepsy, systemic hypertension and

chronic alcohol intake was admitted after he had been

found in a confused state and with aphasia. Cranial CT

showed a left fronto-temporal subdural hematoma with

midline shift and areas of hemorrhage in the left basal

ganglia and frontal cortex (Fig. 1A and 1B). He was

transferred to a secondary hospital after 32 days, still

with severe contraversive pushing to the right side.

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Patient 7, a 50 year-old right-handed male, admitted

with a Glasgow Coma Scale (GCS) score of 9 and left

hemiparesis after having been hit by a car. Cranial CT

showed a right temporo-parietal contusion, laminar

subdural hemorrhage and mild cerebral edema. He

re-quired orotracheal intubation, ventilatory support and

intensive care treatment for about 8 days. He was then

transferred to the neurological unit. He was found to

have severe pushing behavior to the left side that lasted

about 27 days. He was discharged after 37 days with a

GCS score of 15, mild left hemiparesis and complete

res-olution of pusher behavior.

Patient 8, a 58 year-old left-handed-female, with a

previous history of a right gluteus rabdomyosarcoma

treated with surgery and chemotherapy and a

docu-mented lung metastasis, presented to the emergency

room with left hemiparesis and decreased level of

con-science. CT of the head showed multiple hemorrhagic

metastases with severe vasogenic edema around them,

which were distributed bilaterally within the deep white

matter (Figs. 1C and D). The lesions in the right

hemi-sphere were larger and were related to clinical motor

deficits. The first evaluation for pushing behavior was

performed 15 days after admission. Severe pushing

be-havior to the left side was observed. Three weeks later

she was transferred to another hospital still with severe

contraversive pushing. Her last evaluation was 23 days

after discharge and, by that time, it was impossible to

ac-cess pushing behavior because of her deteriorated

con-dition and decreased level of conscience. The patient

died a few weeks after her last evaluation.

Discussion

This study was carried out in an emergency unit of a

university hospital, which is the regional reference for

both traumatic and acute neurological patients. Over a

one year period, patients were systematically evaluated

for abnormal postural behavior and submitted to

reha-bilitation according to their needs. Within this

popula-tion, we found a relative frequency of 1.5 % for pushing

behavior, which is smaller than the 5.3 % found in a

pre-vious published series carried out in a specialized stroke

unit [9]. Our findings demonstrate, apparently for the

first time, that pushing behavior can occur in patients

with non-stroke neurological lesions, which represented

fifty percent of the present series.We believe that pusher

behavior may be underestimated in non-stroke

condi-tions because all previous studies have focused on

se-lected populations of stroke patients [2–5, 7, 9, 10].

We found right-sided lesions in six of our series of

eight. Although it was first assumed that pusher

syn-drome was associated with right hemisphere lesions, our

results are in agreement with more recent data which

in-dicate that pusher behavior can occur with either right

or left-sided lesions [3, 5, 9].

Regarding the evolution of pusher symptoms, stroke

patients in the present study showed complete recovery

of pusher behavior in a mean duration of 15.3 weeks

(8–28 weeks), which is in agreement with previous

stud-ies [7]. In contrast, we found the pushing behavior to be

completely resolved in a mean time of 5 weeks (3–7

weeks) in patients with brain trauma. The apparent

dif-ference in recovery time may be related to etiology,

ex-tension, or inherent resolution mechanisms of the

causative lesion. The small number of non-stroke

pa-Table 1 Demographic and clinical data, rehabilitation outcome and resolution of pushing behavior according to etiology

Patients Age Sex Interval (in Pain Sensibility Hemineglect SCP* Lesion Side of Clinical outcome Resolution Etiology

(years) days) between (Post/Ext/ side pushing (Barthel Index) of pushing

lesion onset and Resis) behavior behavior

first evaluation

1 74 M 55 Hypesthesia YES 2/2/2 R L Death Not evaluated Infarct

2 75 F 60 Hypesthesia YES 2/2/2 R L (50) 24–28 weeks Infarct

3 48 M 33 Normal NO 2/2/2 R L (85) 12 weeks Infarct

4 76 M 35 Normal NO 1.75/2/2 L R (25) 8 weeks Hem

5 62 M 16 Normal YES 2/2/2 L R (00) Not evaluatedb Traumatic

6 80 F 27 Hypesthesia YES 1.5/2/2 R L (80) 7 weeks Traumatic

7 50 M 13 Normal YES 1.5/1.5/2 R L (100) 3 weeks Traumatic

8 58 F 15 Hypesthesia YES 2/2/2 Ba L Death Not evaluated Tumor

* Scale for Contraversive Pushing (SCP) assesses 1) symmetry of spontaneous posture (Post) while sitting and standing (max, 2), 2) the use of the arm or the leg to extend (Ext) the area of physical contact to the ground while sitting and standing (max, 2), and 3) resistance (Resis) to passive correction of posture while sitting and standing (max,

2) . Hemintraparenchymatous hemorrhage; Rright; Lleft; BBilateral

aAlthough patient 8 had a small lesion over the left parieto-occipital transition, the lesions in the right hemisphere were larger, had a mass effect and were related to the

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tients in the present study prevent statistical analysis. It

is well known that stroke patients presenting pushing

behavior have their rehabilitation time needed for

re-covery increased twofold over that of patients without

pushing [9]. The impact of pusher symptoms associated

with other etiologies is still unclear. Further studies may

help to clarify the prognosis of pushing symptoms in

other neurological conditions.

The demonstration of contraversive pushing in

pa-tients with different brain lesions indicates that the

re-lated alteration of vertical postural control may be a

consequence of any lesion that produces dysfunction in

the neural network which processes the input for

verti-cal perception. The present data show that pusher

be-havior must be systematically evaluated in patients with

various encephalic disorders and this may help to

re-duce their stay in hospital, recovery time and improve

their quality of life. More efficient rehabilitation

strate-gies have to be developed in stroke and non-stroke

pa-tients and further research on pusher behavior is

needed to explore the nature of the symptom.

■Acknowledgements The authors thank the residents, physiothera-pists, medical staff and patients of the Emergency Unit of the Hospi-tal das Clínicas da Faculdade de Medicina de Ribeirão Preto/USP. J. P.Leite and O. M. Pontes-Neto, A. C. Santos and D. B. de Araujo are supported by Fundação de Apoio a Pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

Fig. 1 CT scans of patients showing different etiolo-gies for pushing behavior. Aand Bare from patient 5, with a traumatic brain injury. Note the left subdural haematoma and mass effect with midline shift and multiple areas of contusion over the left hemisphere.

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1. Bisiach E, Vallar G, Perani D, Papagno C, Berti A (1986) Unawareness of dis-ease following lesions of the right hemisphere: anosognosia for hemiple-gia and anosognosia for hemianopia. Neuropsychologia 24:471–482 2. Davies PM (1985) Steps to follow: a

guide to the treatment of adult hemi-plegia. New York: Springer

3. Karnath HO, Broetz D (2003) Under-standing and treating “Pusher Syn-drome”. Phys Ther 83:1119–1125 4. Karnath HO, Ferber S, Dichgans J

(2000) The origin of contraversive pushing: evidence for a second gravi-ceptive system in humans. Neurology 55:1298–1304

5. Karnath HO, Ferber S, Dichgans J (2000) The neural representation of postural control in humans. Proc Natl Acad Sci U S A 97:13931–13936 6. Karnath HO, Brotz D, Gotz A (2001)

[Clinical symptoms, origin, and ther-apy of the “pusher syndrome”]. Nervenarzt 72:86–92

7. Karnath HO, Johannsen L, Broetz D, Ferber S, Dichgans J (2002) Prognosis of contraversive pushing. J Neurol 249: 1250–1253

8. Mahoney F, Barthel D (1965) Func-tional evaluation: the Barthel Index. Md State Med J 2:61–65

9. Pedersen PM, Wandel A, Jorgensen HS, Nakayama H, Raaschou HO, Olsen TS (1996) Ipsilateral pushing in stroke: in-cidence, relation to neuropsychological symptoms, and impact on rehabilita-tion. The Copenhagen Stroke Study. Arch Phys Med Rehabil 77:25–28 10. Perennou DA, Amblard B, Laassel el M,

Benaim C, Herisson C, Pelissier J (2002) Understanding the pusher be-havior of some stroke patients with spatial deficits: a pilot study. Arch Phys Med Rehabil 83:570–575

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