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 ·
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.
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 etiologyPatients 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
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.
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