**1. Introduction**

238 Neuroimaging for Clinicians – Combining Research and Practice

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Disorders of postural balance are common in patients with encephalic lesions. According Tyson et al. (Tyson et al., 2006), around 80% of patients experiencing their first cerebrovascular event have static or dynamic postural imbalance. Historically, the first description of postural balance dysfunction in stroke patients dates back to more than one hundred years ago. In 1909, Beevor described the occasional lack of lateral balance in stroke patients that cause them to fall towards their contralesional side due to their paresis (Beevor, 1909). Later, Brunnstrom reported the 'listing phenomenon' as a list toward the affected side that patients cope by climbing onto something with their nonparetic hand to prevent listing (Brunnstrom, 1970).

In 1968, a tendency to fall towards the lesion side and lateropulsion were described by Bjerver and coworkers in patients with Wallenberg's syndrome due to dorsolateral medullary infarction (Bjerver &Silfverskiold, 1968). These patients also presented with transient ocular tilt reaction and ipsiversive deviations of the subjective vertical, which indicate a pathological shift in the internal representation of the gravitational vector (Dieterich &Brandt, 1992; Brandt &Dieterich, 2000; Dieterich, 2007).

Another postural imbalance observed in patients with encephalic lesions is thalamic astasia. According to Masdeu and Gorelick, this disorder is characterized by the inability to maintain an unsupported upright posture even without paresis or sensory or cerebellar deficits.8 When asked to sit up, patients with this disorder use the unaffected arm to pull themselves up (Masdeu & Gorelick, 1988). This behavior could be explained in part by a vestibular tone imbalance in the roll plane, especially since skew deviation was included as a feature of the syndrome (Brandt & Dieterich, 2000; Dieterich, 2007).

As opposed to all other syndromes and phenomena described above, the pusher behavior (PB) is characterized by actively pushing away from the nonparetic side (Davies, 1985). Moreover, patients with PB lean to the side opposite the lesion and strongly resist any attempt at passive correction of their tilted body while sitting or standing. In the most severe cases, this resistance occurs even in a supine position (Pedersen et al., 1996; Lafosse et al., 2005). Such patients report a fear of falling towards their ipsilesional side (Davies, 1985; Pedersen et al., 1996; Lafosse et al., 2005) and are not aware that their active pushing is counterproductive and makes it impossible for them to stand without assistance (D'Aquila

New Insights for a Better Understanding

(Johannsen et al., 2006a).

this scale (Lagerqvist &Skargren, 2006).

of the Pusher Behavior: From Clinical to Neuroimaging Features 241

was called 'variable B', and its standing assessment was described as follows: 'The examiner first observes whether the ipsilesional leg is spontaneously (already when rising from the sitting position) abducted and extended. If so, variable B is given the value 1 for standing. If abduction and extension of the nonparetic leg are not spontaneously performed, the examiner asks the patient to start walking. The examiner observes whether the patient now abducts and extends the ipsilesional leg. If so, variable B is given the value 0.5 for standing'. Because the instructions above do not consider the reaction of the arm/hand in standing position and does not include any recommendation for the examiner's performance during the assessment, we suggest the following additional instructions that we found very helpful for the SCP assessment: (1) while the patient is in the standing position, his/her paretic/plegic leg should be supported by using a knee extension split or by the examiner's stabilization (see figure 1); (2) also in the standing position, the examiner should guarantee the presence of a surface next to the patient to observe the behavior of the ipsilesional arm/hand in searching for contact with the surface and achieving extension of the elbow. Another slight but noteworthy detail that should be remembered when assessing the SCP in the sitting position is that patients should be evaluated with plantar support. Nevertheless, an additional bedside tool to detect PB is the investigation of the pusher patients' leg-totrunk orientation (Johannsen et al., 2006a). When seated upright without contact with the ground, an ipsiversive tilt of the non-paretic leg in relation to the trunk of about 9° is observed. The inclined leg position is maintained throughout the entire tilt cycle. This reaction was not observed in non-brain-damaged subjects, in patients with acute unilateral vestibular dysfunction, or in patients with stroke without PB and vestibular dysfunction

The Modified Scale for Contraversive Pushing (mSCP) consists of a composite score that quantifies the PB and includes four functional conditions: (1) static sitting at the bedside with the feet on the floor; (2) static standing with a fully erect posture; (3) transferring from the bed to a chair or wheelchair (with armrests) while maintaining hip flexion; (4) transferring from the bed to a chair or wheelchair by coming to a full standing position and stepping or pivoting 90 degrees (Lagerqvist &Skargren, 2006). Each part is scored separately and the degree of pushing is evaluated on a scale from 0 to 2 points, where 0 indicates no symptoms, and 2 indicates very severe symptoms. The highest possible score is 8 and the recommended diagnostic cutoff score is 3 (Lagerqvist &Skargren, 2006). As suggested by Baccini et al. (Baccini et al., 2006), this modified version is so different from the original SCP that it should be considered a different instrument. Adding transfers and using specific scoring criteria may help examiners of patients whose PB tends to manifest with dynamic balance activities. The concurrent validity of the mSCP with Berg Balance Scale and Swedish Physiotherapy Clinical Outcome was low to moderate, and the inter-rater reliability was moderate to good. Although the mSCP seems to be practical and more sensitive for small changes in the PB's status, further studies are needed because the sample size of its only clinimetric properties' study was small, and all patients exhibited signs of PB. Moreover, sensitivity/specificity data, internal consistency and responsiveness are not available for

The Burke Lateropulsion Scale (BLS) was first developed in 1993 and revised several times by the physiotherapist team of the Burke Rehabilitation Hospital (D'Aquila et al., 2004). This scale is rated according to the severity of resistance to passive correction of the posture or the presence of PB sensed by the examiner during supine rolling, sitting, standing, transferring and walking (0, 1=mild, 2=moderate, 3=severe). According to the authors, to

et al., 2004). Thus, the listing phenomenon, thalamic astasia and Wallenberg's syndrome need to be considered in the differential diagnosis of PB. Although the PB was originally described in association with neglect and anosognosia as a syndrome that is related to right encephalic lesions by the physical therapist Davies (Davies, 1985), several studies have demonstrated that it can occur in patients with lesions in both hemispheres and is distinct from those neuropsychological deficits (Pedersen et al., 1996; Karnath et al., 2000b, 2000a; Premoselli et al., 2001; Pérrenou, 2002; Bohannon, 2004; Santos-Pontelli et al., 2004). Since the definition of 'syndrome' is "a set of qualities, events or behaviors that is typical of a particular kind of problem' (Longman dictionary of Contemporary English; 1995) and the diagnostic criteria for PB are presence of the 3 behaviors observed by the examiner described above, the term 'pusher syndrome' can be considered appropriate. Alternative labels of the PB are 'contraversive pushing' (Santos-Pontelli et al., 2004; Lafosse et al., 2005; Baccini et al., 2006; Karnath &Brotz, 2007), 'ipsilateral pushing' (Pedersen et al., 1996) and 'lateropulsion' (Babyar et al., 2009). D'Aquila et al (2004) (D'Aquila et al., 2004) referred to this behavior as being synonymous with the 'listing phenomenon', but Brunnstrum's first description mentions neither the behavior of active pushing away from the nonparetic side nor the resistance to posture correction (Brunnstrom, 1970).

Since it was first described in 1985 (Davies, 1985) , interest in PB has been increasing. The aim of this review is to summarize and critically discuss several aspects of this intriguing disorder that are described in the literature.

#### **2. Assessment**

The assessment of PB has been conducted either by clinical examination according the recommendations of the physiotherapist Davies (Pedersen et al., 1996; Lafosse et al., 2005; Baccini et al., 2006) or by ordinal scales (Babyar et al., 2009). According to the systematic review by Babyar and coworkers, there are three appropriate clinical examination scales for evaluation of PB (Babyar et al., 2009): the Scale for Contraversive Pushing (SCP), the Modified Scale for Contraversive Pushing (mSCP) and the Burke Lateropulsion Scale (BLS). Based on the Davies' criteria, Karnath et al. (Karnath et al., 2001) created the SCP that assesses three distinct aspects of postural control: A) symmetry of spontaneous posture while sitting and standing, B) the use of the ipsilesional extremities to abduct and extend the area of physical contact with the surface (arm/hand on mattress; leg/foot on floor) while sitting and standing, and C) resistance to passive correction of posture while sitting and standing. The authors made the diagnosis of PB if all three criteria were present, reaching a total score of at least 1 in each criterion (sitting plus standing in the three situations).

By analyzing the clinimetric properties of the SCP, Baccini et al. (Baccini et al., 2006) found that a cutoff score of greater than 0 in each SCP section might be more appropriate for studies aimed at investigating the prevalence of the PB or its association with other features, such as presence of neglect because this cutoff enhanced the specificity without any decrease in sensitivity or the predictive value of a negative test. Nevertheless, this cutoff criterion requires further investigation in an unselected group of acute neurologically injured patients (Karnath &Brotz, 2007). Since the original cutoff score suggested by Karnath et al. has no false-positive diagnoses (Baccini et al., 2006), it should be better used for pathophysiological studies or investigations about the neural substrates involved with the PB.

Recently, more specific instructions of the SCP were published (Karnath &Brotz, 2007). The use of the nonparetic extremities to bring about the pathological lateral tilt of the body axis

et al., 2004). Thus, the listing phenomenon, thalamic astasia and Wallenberg's syndrome need to be considered in the differential diagnosis of PB. Although the PB was originally described in association with neglect and anosognosia as a syndrome that is related to right encephalic lesions by the physical therapist Davies (Davies, 1985), several studies have demonstrated that it can occur in patients with lesions in both hemispheres and is distinct from those neuropsychological deficits (Pedersen et al., 1996; Karnath et al., 2000b, 2000a; Premoselli et al., 2001; Pérrenou, 2002; Bohannon, 2004; Santos-Pontelli et al., 2004). Since the definition of 'syndrome' is "a set of qualities, events or behaviors that is typical of a particular kind of problem' (Longman dictionary of Contemporary English; 1995) and the diagnostic criteria for PB are presence of the 3 behaviors observed by the examiner described above, the term 'pusher syndrome' can be considered appropriate. Alternative labels of the PB are 'contraversive pushing' (Santos-Pontelli et al., 2004; Lafosse et al., 2005; Baccini et al., 2006; Karnath &Brotz, 2007), 'ipsilateral pushing' (Pedersen et al., 1996) and 'lateropulsion' (Babyar et al., 2009). D'Aquila et al (2004) (D'Aquila et al., 2004) referred to this behavior as being synonymous with the 'listing phenomenon', but Brunnstrum's first description mentions neither the behavior of active pushing away from the nonparetic side

Since it was first described in 1985 (Davies, 1985) , interest in PB has been increasing. The aim of this review is to summarize and critically discuss several aspects of this intriguing

The assessment of PB has been conducted either by clinical examination according the recommendations of the physiotherapist Davies (Pedersen et al., 1996; Lafosse et al., 2005; Baccini et al., 2006) or by ordinal scales (Babyar et al., 2009). According to the systematic review by Babyar and coworkers, there are three appropriate clinical examination scales for evaluation of PB (Babyar et al., 2009): the Scale for Contraversive Pushing (SCP), the Modified Scale for Contraversive Pushing (mSCP) and the Burke Lateropulsion Scale (BLS). Based on the Davies' criteria, Karnath et al. (Karnath et al., 2001) created the SCP that assesses three distinct aspects of postural control: A) symmetry of spontaneous posture while sitting and standing, B) the use of the ipsilesional extremities to abduct and extend the area of physical contact with the surface (arm/hand on mattress; leg/foot on floor) while sitting and standing, and C) resistance to passive correction of posture while sitting and standing. The authors made the diagnosis of PB if all three criteria were present, reaching a

total score of at least 1 in each criterion (sitting plus standing in the three situations).

studies or investigations about the neural substrates involved with the PB.

By analyzing the clinimetric properties of the SCP, Baccini et al. (Baccini et al., 2006) found that a cutoff score of greater than 0 in each SCP section might be more appropriate for studies aimed at investigating the prevalence of the PB or its association with other features, such as presence of neglect because this cutoff enhanced the specificity without any decrease in sensitivity or the predictive value of a negative test. Nevertheless, this cutoff criterion requires further investigation in an unselected group of acute neurologically injured patients (Karnath &Brotz, 2007). Since the original cutoff score suggested by Karnath et al. has no false-positive diagnoses (Baccini et al., 2006), it should be better used for pathophysiological

Recently, more specific instructions of the SCP were published (Karnath &Brotz, 2007). The use of the nonparetic extremities to bring about the pathological lateral tilt of the body axis

nor the resistance to posture correction (Brunnstrom, 1970).

disorder that are described in the literature.

**2. Assessment** 

was called 'variable B', and its standing assessment was described as follows: 'The examiner first observes whether the ipsilesional leg is spontaneously (already when rising from the sitting position) abducted and extended. If so, variable B is given the value 1 for standing. If abduction and extension of the nonparetic leg are not spontaneously performed, the examiner asks the patient to start walking. The examiner observes whether the patient now abducts and extends the ipsilesional leg. If so, variable B is given the value 0.5 for standing'. Because the instructions above do not consider the reaction of the arm/hand in standing position and does not include any recommendation for the examiner's performance during the assessment, we suggest the following additional instructions that we found very helpful for the SCP assessment: (1) while the patient is in the standing position, his/her paretic/plegic leg should be supported by using a knee extension split or by the examiner's stabilization (see figure 1); (2) also in the standing position, the examiner should guarantee the presence of a surface next to the patient to observe the behavior of the ipsilesional arm/hand in searching for contact with the surface and achieving extension of the elbow. Another slight but noteworthy detail that should be remembered when assessing the SCP in the sitting position is that patients should be evaluated with plantar support. Nevertheless, an additional bedside tool to detect PB is the investigation of the pusher patients' leg-totrunk orientation (Johannsen et al., 2006a). When seated upright without contact with the ground, an ipsiversive tilt of the non-paretic leg in relation to the trunk of about 9° is observed. The inclined leg position is maintained throughout the entire tilt cycle. This reaction was not observed in non-brain-damaged subjects, in patients with acute unilateral vestibular dysfunction, or in patients with stroke without PB and vestibular dysfunction

(Johannsen et al., 2006a). The Modified Scale for Contraversive Pushing (mSCP) consists of a composite score that quantifies the PB and includes four functional conditions: (1) static sitting at the bedside with the feet on the floor; (2) static standing with a fully erect posture; (3) transferring from the bed to a chair or wheelchair (with armrests) while maintaining hip flexion; (4) transferring from the bed to a chair or wheelchair by coming to a full standing position and stepping or pivoting 90 degrees (Lagerqvist &Skargren, 2006). Each part is scored separately and the degree of pushing is evaluated on a scale from 0 to 2 points, where 0 indicates no symptoms, and 2 indicates very severe symptoms. The highest possible score is 8 and the recommended diagnostic cutoff score is 3 (Lagerqvist &Skargren, 2006). As suggested by Baccini et al. (Baccini et al., 2006), this modified version is so different from the original SCP that it should be considered a different instrument. Adding transfers and using specific scoring criteria may help examiners of patients whose PB tends to manifest with dynamic balance activities. The concurrent validity of the mSCP with Berg Balance Scale and Swedish Physiotherapy Clinical Outcome was low to moderate, and the inter-rater reliability was moderate to good. Although the mSCP seems to be practical and more sensitive for small changes in the PB's status, further studies are needed because the sample size of its only clinimetric properties' study was small, and all patients exhibited signs of PB. Moreover, sensitivity/specificity data, internal consistency and responsiveness are not available for this scale (Lagerqvist &Skargren, 2006).

The Burke Lateropulsion Scale (BLS) was first developed in 1993 and revised several times by the physiotherapist team of the Burke Rehabilitation Hospital (D'Aquila et al., 2004). This scale is rated according to the severity of resistance to passive correction of the posture or the presence of PB sensed by the examiner during supine rolling, sitting, standing, transferring and walking (0, 1=mild, 2=moderate, 3=severe). According to the authors, to

New Insights for a Better Understanding

sitting, standing, weight transferring and walking (table 1).

repeated afterwards during several weeks after the ictus onset.

**4. Demographic and clinical characteristics** 

the assessments of PB and their cutoffs.

encephalic lesion.

**3. Incidence** 

of the Pusher Behavior: From Clinical to Neuroimaging Features 243

standing, a score of 2 indicated PB when standing and sitting and a score of 3 indicated PB when standing, sitting and lying. Measurement of inter-rater reliability revealed a percentage of agreement of 88.4% and a Kendall's coefficient of concordance of 0.83 (Lafosse et al., 2005). According to the authors, this assessment of PB is closely related to the SCP. However, it also has no available data about sensitivity, specificity, internal consistency and responsiveness.

Among the studies that considered the PB according to Davies' description, the incidence of this disorder ranges from 1.5 % to 63 % of patients with acute encephalic lesions (Table 1) (Pedersen et al., 1996; Danells et al., 2004; Santos-Pontelli et al., 2004; Lafosse et al., 2005; Baccini et al., 2006). Pedersen et al. (Pedersen et al., 1996) found an incidence of 5.3 % of PB in all stroke patients who were admitted in study period and 10.4 % of patients without lower extremity paresis on admission, when early death or early recovery were excluded. Danells et al. (Danells et al., 2004) found a PB incidence of 23% and 63% among 65 stroke patients with moderate to severe hemiparesis depending on the assessment cutoff. We found 1.5 % of pusher patients among all neurological inpatients of an emergency hospital (Santos-Pontelli et al., 2004), and Lafosse et al. (Lafosse et al., 2005) found an incidence of 40 % of left-brain-damaged patients and 52% of right brain damaged patients at a rehabilitation center. More recently, Baccini and coworkers (Baccini et al., 2006) compared the incidence of the PB based on 4 different criteria: 3 different cutoffs of the SCP (SCP > 0; SCP≥ 1,75; SCP ≥ 3) and a clinical examination according to Davies' recommendations that focused on careful observation of patients while lying down,

The comparison of the reported frequencies of PB is very complicated due to the differences in the timing of the first post ictal evaluation, inclusion/exclusion criteria, characteristics of the institutions where patients were investigated, etiologies included in the screening and

The post ictal timing of the first identification of PB is an important aspect for incidence analysis. PB may not be observed if the assessment is done in outpatients or after several weeks because of early resolution of the behavior. On the other hand, if the assessment is conducted too early, pusher behavior can appear as a fluctuated symptom. Therefore, the screening of this behavior should be conducted as soon as clinical conditions allow and

The comparison of demographic and clinical characteristics between series of pusher patients is complicated not only because of the several selection criteria discussed above but also due to the differences among the designs of the studies. Nevertheless, we summarized some demographic and clinical characteristics that have been published so far (table 2). Pusher behavior has been found more frequently in older patients (table 2). More recently, Barbieri et al. found a correlation between age and perception of posture in healthy subjects (Barbieri et al., 2009). If the internal model of verticality is less robust in elderly people, it would be possible that this population could be more vulnerable to present PB. Though, the incidence of strokes is much greater in old than in young adults. It remains unclear the influence of the deterioration of postural control related to aging on the development of PB. Moreover, there is no investigation about the occurrence of PB in children with an acute

test sitting and standing, the patient is passively tilted 30° (15–20° for standing) towards his/her paretic side (contralesional tilt) and then brought back to vertical alignment. Scores are then based on any voluntary or reflex movements noted in trunks, arms or legs according to the angle from true vertical where the resistance starts. For example, the sitting scores are as follows: 0=no resistance; 1=resistance starts at 5° tilt before full vertical; 2=resistance starts at 10° tilt before full vertical; and 3 is scored if they sense true vertical between 30° and 10° (D'Aquila et al., 2004). Total scores range from 0 for those without resistance to a maximum score of 17. Patients scoring 2 or greater are considered to exhibit PB (lateropulsion).

Fig. 1. A patient with left brain damage and severe pusher behavior. Examiner stabilizes the paretic leg of the patient in order to evaluate PB sings in standing position. The absence of this stabilization makes the observation of the characteristics of the disorder significantly difficult. Also, the examiner should guarantee the presence of a surface besides the patient in standing position, in order to observe the behavior of ipsilesional arm/hand activity to search for contact with the surface and of achieving extension of the elbow.

D`Aquila et al. (2004) analyzed the concurrent validity of the BLS with Fugl-Meyer Balance score, Functional Independence Measure and length of rehabilitation stay is moderate and the inter-rater reliability is very high. However, there are no available data about sensitivity, specificity, internal consistency and responsiveness for this scale. According to the authors, one of the weaknesses of the BLS is that the assessments are subjective and can be affected by both patient and therapist comfort and familiarity with the test protocol (D'Aquila et al., 2004). It could be difficult for untrained examiners to interpret the 5 or 10-degree increments from true vertical to determine the resistance to passive correction during functional activities. Nevertheless, this is the only scale that includes PB evaluation during supine rolling and walking.

Another assessment of PB was proposed by Lafosse et al.11 based on Davies' criteria (Lafosse et al., 2005), including (a) the presence of an asymmetrical posture or the midline of the body towards the hemiplegic side, and (b) the presence of resistance against any attempt at passive correction of any of these postures across the midline of the body towards the 'non-affected' or ipsilesional side. A patient is classified as having PB if both criteria are present. No ordinal scale is specified in this analysis. Further differentiation is used with the help of a 4-point scale that is based on the number of postures (standing, sitting and/or lying) in which contraversive pushing is present as follows: a score of 0 indicated no PB, a score of 1 indicated PB when standing, a score of 2 indicated PB when standing and sitting and a score of 3 indicated PB when standing, sitting and lying. Measurement of inter-rater reliability revealed a percentage of agreement of 88.4% and a Kendall's coefficient of concordance of 0.83 (Lafosse et al., 2005). According to the authors, this assessment of PB is closely related to the SCP. However, it also has no available data about sensitivity, specificity, internal consistency and responsiveness.
