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Persistent pusher behavior after a stroke

CASE REPORT

Persistent pusher behavior after a stroke

Taiza E. G. Santos-PontelliI; Octavio M. Pontes-NetoI; Draulio B. de AraujoII; Antonio Carlos SantosI; Joao P. LeiteI

IUniversity of São Paulo School of Medicine at Ribeirão Preto, Department of Neuroscience and Behavior, Ribeirão Preto/SP, Brazil

IIFederal University of Rio Grande do Norte (UFRN), Brain Institute Natal/RN, Brazil

INTRODUCTION

Pusher behavior (PB) is a postural control disorder characte rized by actively pushing away from the nonparetic side and resisting passive correction with a tendency to fall toward the paral yzed side.1These patients have no awareness that their active pushing is counterproductive, which precludes the patients from standing without assistance.

Several studies have already demonstrated that PB can occur in patients with lesions in both hemispheres, and PB is distinct from neglect and anosognosia.2-8The high fre quency of the association between PB and neurophysiological deficits might reflect an increased vulnerability of certain regions to stroke-induced injury rather than any direct involvement with the occurrence of PB. 9,10

Tradit ionally, PB has only been reported in stroke patients; however, it has also been described under nonstroke c onditions.8Previous imaging studies have sug gested the posterolateral thalamus as the brain structure that is typically damaged in pusher patients.4,11Never theless, other cortical and subcortical areas, such as the insular cortex and post-central gyrus, have also been highlighted as structures that are potentially involved in the pathophysiology of PB.2,12-16

The mechanisms underlying PB have been attributed to vertical perception dysfunction that leads to postural reactive behavior.3,14,17-19 Nevertheless, the true changes in the verticality perception of these patients are still unclear. In this context, Karnath et al. identified five patients with severe PB who experience their body (subjective postural vertical [SPV]) as oriented ‘‘upright’’ when it is actually tilted approximately 18˚ toward the side of the brain lesion and with no subjective visual vertical (SVV) bias. 3Johansen et al. also found no SVV bias in 15 PB patients.20In contrast, Pé rrenou et al. found SPV, SVV, and subjective haptic vertical (SHV) biases toward the side opposite the brain lesion in six pusher patients.21It is clear that, to state which vertical perception is disturbed in PB patients, the studies’ designs require a meticulous methodology, including the analysis of neglect and the influence of haptics on SVV in a large sample of PB patients.

Until now, PB has only been reported as a temporary and transitory phenomenon with a maximum recovery time of six months.8,22-24 Moreover, it has been suggested that PB does not negatively influence the functional outcomes of rehabilitation.10,22 Nevertheless, thos e assumptions have primaril y emerged from case series of stroke patients admitted to stroke units or followed in rehabilitation centers in developed countries.10,22-24Therefore, the actual impact of the disorder on stroke patients in developing countries may be underestimated. Here, we report three cases of stroke patients that had persistent PB with important disabling consequences on their functional outcomes.

CASE DESCRIPTION

Patient 1: A 77-year-old right-handed male with a history of hypertension was admitted after being found confused and left-hemiparetic with an NIH stroke scale 25score of 20. Cra nial CT revealed a right-middle cerebral artery ischemic stro ke (Figure 1a; Table 1). The PB was identified 10 days after the onset of ictus with a Scale for Contraversive Pushing (SCP)3 score of 6, and he was discharged 10 days later. The patient was reevaluated 318 days after the onset of ictus and still presented severe PB (SCP = 6) and a Barthel Inde x25score of zero. He died because of pneumonia a few weeks after his last reevaluation.


Patient 2: A 74-year-old right-handed male with a history of alcohol and tobacco abuse was admitted with right hemipar esis and aphasia. A CT scan revealed ischemic strokes in the branches of his left-anterior and middle cere bral arteries (Figure 1b; Table 1). PB was identified nine day s after the onset of ictus (SCP = 6). He was discharged after 20 days. Upon his last reevaluation 763 days after the onset of ictus, severe PB was still present, and he had a Barthel Index score of zero.

Patient 3: A 65-year-old right-handed man with a history of a ruptured right-middle cerebral artery aneurysm treated by surgical clipping in another institution was referred to our outpatient stroke clinic 1.6 years after the onset of ictus when severe PB was identified (Figure 1c; Table 1). Severe PB was still present 729 days after the onset of ictus, and he had a Barthel Index score of 10. (The patient had occasional bladder and bowel incontinence.) He was found dead by his family members a few weeks after his final evaluation.

In all of the cases, after the identification of PB, the patients were referred to public rehabilitation centers, but their adherence to their rehabilitation programs was neither optimized nor controlled. All of the patients had restricted access to physiotherapy (the mean number of sessions per week was less than 1) and remained lying in bed almost the entire day. Furthermore, upon their final reevaluations, all of the patients were completely dependent on their activities of daily living with a modified Rankin scale score of 5, the strengths of their arms and legs opposite their brain lesions did not change over time, and they had a persistent fear of falling.

DISCUSSION

This is the first demonstration that PB can persist for more than two years, with disastrous impacts on functional outcomes. Certainly, the factors that negatively influenced the duration of PB were the limited frequency of physiother apy and the absence of specific strategies for treating PB. In fact, some well-described physiotherapy approaches have been proposed,23,26-29 but there have been no randomized control trials that have confirmed their effectiveness. Still, there is strong evidence that str oke rehabilitation that is initiated early after onset and sustained across the healthcare continuum significantly reduces the probability of disability within the first year.30,31 Furthermore, the poor socioeco nomic conditions of the patients restricted their home care and led to the patients lying in bed almost the entire day, despite their physiotherapeutic recommendations. Thus, the privation of experience in the vertical position after their strokes could have negatively influenced the patients’ prognoses. This observation raises the question of whether the duration of PB could be shortened by the simple attitude of remaining in a vertical position for several daylight hours.

PB has been considered to be a neurological behavior that is not strongly associated with the recovery of motor control in the upper and lower limbs.24,32Nevertheless, we observed poor concomitant PB recovery and other neurological deficits, which might reflect the maladaptive mechanisms underlying the lack of plasticity. Additional studies will be needed to understa nd the neuroplastic mechanisms of PB recovery using brain-act ivation techniques (functional magnetic resonance, single-photon emis sion computed tomography, positron emission tomography, magnetoencephalography, and eventrelated potential) and tran scranial magnetic stimulation techniqu es.

Spatial neglect has been identified as a factor that worsens the prognosis of PB,6,10,24 and this clinical characteristic was found in two of our patients. Thus, we cannot suggest that the poor recovery observed in our patients could be entirely due to the presence of spatial neglect. Moreover, we were unable to evaluate the perception of verticality. Future studies should explore whether the vertical misperceptions of the pus her patients influence the duration and severity of PB.

The a bsence of sitting balance soon after stroke has consistently been shown to predict a poor re covery. 33Mor eover, predicting the outcome of a stroke is important for triage decisions, prognostic estimates for the family, and the appropriate utilization of resources.34It is noteworthy that while the patients presented PB, all of their daily life activities were compromised. Thus, this study highlights that PB can be much more incapacitating than generally believed.

ACKNOWLEDGMENTS

The authors acknowledge CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and FAPESP (Fundação de Amparo a' Pesquisa do Estado de São Paulo) for their financial support.

AUTHOR CONTRIBUTIONS

Santos-Pontelli TEG and Pontes-Neto designed and conceived the study, collected, analyzed, interpreted the data, and drafted the manuscript. Araujo DB and Santos AC designed the study, analyzed, interpreted the data and revised the manuscript. Leite JP designed and conceived the study, analyzed and interpreted the data, and revised the manuscript.

REFERENCES

1. Davies PM. Steps to follow: a guide to the treatment of adult hemiplegia. New York: Springer 1985.

2. Pedersen PM, Wandel A, Jorgensen HS, Nakayama H, Raaschou HO, Olsen TS. Ipsilateral pushing in stroke: incidence, relation to neuropsychological symptoms, and impact on rehabilitation. The Copenhagen Stroke Study. Arch Phys Med Rehabil. 1996;77:25-8, doi: 10.1016/S0003 9993(96)90215-4.

3. Karnath HO, Ferber S, Dichgans J. The origin of contraversive pushing: evidence f or a second graviceptive system in humans. Neurology. 2000;55:1298-304.

4. Karnath HO, Ferber S, Dichgans J. The neural representation of postural control in humans. Proc Natl Acad Sci U S A. 2000;97:13931-6, doi: 10. 1073/pnas.240279997.

5. Premoselli S, Cesana L, Cerri C. Pusher syndrome in stroke: clinical, neuropsychological, and neurophysiological investigation. Eur Med Phys. 2001;37:143-51.

6. Pérrenou DA, Laassel B, Benaim EM, Herisson C, Pelissier C. J. Understanding the pusher behavior of some stroke patients with spatial deficit: A pilot study. Phys Med Rehabil. 2002;83:570-5, doi: 10.1053/ apmr.2002. 31198.

7. Bohannon RW. Pusher syndrome. Phys Ther. 2004;84:580-1; author reply 2-3.

8. Santos-Pon telli TE, Pontes-Neto OM, Colafemina JF, de Araujo DB, Santos AC, Leite JP. Cont raversive pushing in non-stroke patients. J Neurol. 2004;251:1324-8, doi: 10.1007/s00415-004-0532-y.

9. Rorden C, Karnath HO. Using human brain lesions to infer function: a relic from a past era in the fMRI age? Nature reviews. 2004;5:813-9, doi: 10.1038/nr n1521.

10. Karnath HO. Pusher syndrome-a frequent but little-known disturbance of body orientation perception. J Neurol. 2007;254:415-24, doi: 10.1007/ s00415-006-0341-6.

11. Karnath HO, Johannsen L, Broetz D, Kuker W. Posterior thalamic hemorrhag e induces ‘‘pusher syndrome’’. Neurology. 2005;64:1014-9, doi: 10.1212/01.WNL.0000154527.72841.4A.

12. Reding M, David A, Volpe B. Neuroimaging study of the pusher syndrome post stroke. XVI World Congress of Neurology, Buenos Aires, Argentina, September 14-19. J Neurol Sci. 1997;150:S129, doi: 10.1016/ S0022-510X(97)85489-5.

13. Johannsen L, Broetz D, Naegele T, Karnath HO. ‘‘Pusher syndrome’’ following cortical lesions that spare the thalamus. J Neurol. 2006;253:455 63, doi: 10.1007/s00415-005-0025-7.

14. Saj A, Honore J, Coello Y, Rousseaux M. The visual vertical in the pusher syndrome: influence of hemispace and body position. J Neurol. 2005;252:885-91, doi: 10.1007/s00415-005-0716-0.

15. Paci M, Nannetti L. The pusher syndrome in a patient with cerebellar infarction. Physiother Res Int. 2005;10:176-7, doi: 10.1002/pri.8.

16. Karnath HO, Suchan J, Johannsen L. Pusher syndrome after ACA territory infarction. Eur J Neurol. 2008;15:e84-5, doi: 10.1111/j.1468-1331. 2008.02187.x.

17. Karnath HO, Broetz D. Understanding and treating ‘‘pusher syndrome’’. Phys Ther. 2003;83:1119-25.

18. Johannsen L, Broetz D, Karnath HO. Leg orientation as a clinical sign for pusher syndrome. BMC Neurol. 2006;6:30, doi: 10.1186/1471-2377-6-30.

19. Perennou DA, Amblard B, Leblond C, Pelissier J. Biased postural vertical in humans with hemispheric cerebral lesions. Neurosci Lett. 1998;252:75 8, doi: 10.1016/S0304-3940(98)00501-1.

20. Johannsen L, Fruhmann Berger M, Karnath HO. Subjective visual vertical (SVV) determined in a representative sample of 15 patients with p usher syndrome. J Neurol. 2006;253:1367-9, doi: 10.1007/s00415-006 0 216-x.

21. Perennou DA, Mazibrada G, Chauvineau V, Greenwood R, Rothwell J, G resty MA, et al. Lateropulsion, pushing and verticality perception in hemispher e stroke: a causal relationship? Brain. 2008;131:2401-13, doi: 10. 1093/brain /awn170.

22. Karnath HO, Johannsen L, Broetz D, Ferber S, Dichgans J. Prognosis of contraversi ve pushing. J Neurol. 2002;249:1250-3, doi: 10.1007/s00415 002-0824-z.

23. Broetz D, Johannsen L, Karnath HO. Time course of ’pusher syndrome’ under visual feedback treatment. Physiother Res Int. 2004;9:138-43, doi: 10.1002/pr i.314.

24. Danells CJ, Black SE, Gladstone DJ, McIlroy WE. Poststroke ‘‘pushing’’: natural history and relationship to motor and functional recovery. S troke; a journal of cerebral circulation. 2004;35:2873-8, doi: 10.1161/01. S TR.0000147724.83468.18.

25. Cincura C , Pontes-Neto OM, Neville IS, Mendes HF, Menezes DF, Mariano DC, et al. Validation of the National Institutes of Health Stroke Scale, modified Rankin Scale and Barthel Index in Brazil: the role of cultural adaptation and structured interviewing. Cerebrovascular dis eases (Basel, Switzerland). 2009;27:119-22, doi: 10.1159/000177918.

26. Paci M, Nannetti L. Physiotherapy for pusher behaviour in a patient with post-stroke hemiplegia. J Rehabil Med. 2004;36:183-5, doi: 10.1080/ 16501970410029762.

27. Paci M, Rinaldi LA. Physiotherapy for pusher behaviour. NeuroRehabilitation. 2005;20:347.

28. Broetz D, Karnath HO. New aspects for the physiotherapy of pushing behaviour. NeuroRehabilitation. 2005;20:133-8.

29. Shepherd RB, Carr JA. New aspects for the physiotherapy of pushing b ehaviour, D. Broetz and H.-O. Karnath, Neurorehabilitation 20 (2005), 133-138. NeuroRehabilitation. 2005;20:343-5.

30. Miller EL, Murray L, Richards L, Zorowitz RD, Bakas T, Clark P, et al. Comprehe nsive overview of nursing and interdisciplinary rehabilitation c are of the stroke patient: a scientific statement from the American Heart Association. Stroke; a journal of cerebral circulation. 2010;41:2402-48, doi: 1 0.1161/STR.0b013e3181e7512b.

31. Cumming TB, Thrift AG, Collier JM, Churilov L, Dewey HM, Donnan GA, et al. Very early mobilization after stroke fast-tracks return to w alking: further results from the phase II AVERT randomized controlled t rial. Stroke; a journal of cerebral circulation. 2011;42:153-8, doi: 10.1161/ STROKEA HA.110.594598.

32. Santos-Pon telli TE, Pontes-Neto OM, Colafemina JF, Araujo DB, Santos AC, Leite JP. Pushing behavior and hemiparesis: which is critical for f unctional recovery in pusher patients? Case report. Arq Neuropsiquiatr. 2 007;65:536-9, doi: 10.1590/S0004-282X2007000300035.

33. Tyson SF. Measurement error in functional balance and mobility tests for people with stroke: what are the sources of error and what is the best way to minimize error? Neurorehabil Neural Repair. 2007;21:46-50, doi: 10.1177/15 45968306290662.

34. Wright CJ, Swinton LC, Green TL, Hill MD. Predicting final disposition after stroke using the Orpington Prognostic Score. Can J Neurol Sci. 2004;31:494-8.

35. Kerkhoff G. Spatial hemineglect in humans. Prog Neurobiol. 2001;63:127, doi: 10.1016/S0301-0082(00)00028-9.

No potential conflict of interest was reported.

Email: taiza@fmrp.usp.br

Tel.: 55 16 3602-1222

  • 2. Pedersen PM, Wandel A, Jorgensen HS, Nakayama H, Raaschou HO, Olsen TS. Ipsilateral pushing in stroke: incidence, relation to neuropsychological symptoms, and impact on rehabilitation. The Copenhagen Stroke Study. Arch Phys Med Rehabil. 1996;77:25-8, doi: 10.1016/S0003 9993(96)90215-4.
  • 3. Karnath HO, Ferber S, Dichgans J. The origin of contraversive pushing: evidence f or a second graviceptive system in humans. Neurology. 2000;55:1298-304.
  • 4. Karnath HO, Ferber S, Dichgans J. The neural representation of postural control in humans. Proc Natl Acad Sci U S A. 2000;97:13931-6, doi: 10. 1073/pnas.240279997.
  • 5. Premoselli S, Cesana L, Cerri C. Pusher syndrome in stroke: clinical, neuropsychological, and neurophysiological investigation. Eur Med Phys. 2001;37:143-51.
  • 6. Pérrenou DA, Laassel B, Benaim EM, Herisson C, Pelissier C. J. Understanding the pusher behavior of some stroke patients with spatial deficit: A pilot study. Phys Med Rehabil. 2002;83:570-5, doi: 10.1053/ apmr.2002. 31198.
  • 7. Bohannon RW. Pusher syndrome. Phys Ther. 2004;84:580-1; author reply 2-3.
  • 8. Santos-Pon telli TE, Pontes-Neto OM, Colafemina JF, de Araujo DB, Santos AC, Leite JP. Cont raversive pushing in non-stroke patients. J Neurol. 2004;251:1324-8, doi: 10.1007/s00415-004-0532-y.
  • 9. Rorden C, Karnath HO. Using human brain lesions to infer function: a relic from a past era in the fMRI age? Nature reviews. 2004;5:813-9, doi: 10.1038/nr n1521.
  • 10. Karnath HO. Pusher syndrome-a frequent but little-known disturbance of body orientation perception. J Neurol. 2007;254:415-24, doi: 10.1007/ s00415-006-0341-6.
  • 12. Reding M, David A, Volpe B. Neuroimaging study of the pusher syndrome post stroke. XVI World Congress of Neurology, Buenos Aires, Argentina, September 14-19. J Neurol Sci. 1997;150:S129, doi: 10.1016/ S0022-510X(97)85489-5.
  • 14. Saj A, Honore J, Coello Y, Rousseaux M. The visual vertical in the pusher syndrome: influence of hemispace and body position. J Neurol. 2005;252:885-91, doi: 10.1007/s00415-005-0716-0.
  • 15. Paci M, Nannetti L. The pusher syndrome in a patient with cerebellar infarction. Physiother Res Int. 2005;10:176-7, doi: 10.1002/pri.8.
  • 16. Karnath HO, Suchan J, Johannsen L. Pusher syndrome after ACA territory infarction. Eur J Neurol. 2008;15:e84-5, doi: 10.1111/j.1468-1331. 2008.02187.x.
  • 18. Johannsen L, Broetz D, Karnath HO. Leg orientation as a clinical sign for pusher syndrome. BMC Neurol. 2006;6:30, doi: 10.1186/1471-2377-6-30.
  • 19. Perennou DA, Amblard B, Leblond C, Pelissier J. Biased postural vertical in humans with hemispheric cerebral lesions. Neurosci Lett. 1998;252:75 8, doi: 10.1016/S0304-3940(98)00501-1.
  • 20. Johannsen L, Fruhmann Berger M, Karnath HO. Subjective visual vertical (SVV) determined in a representative sample of 15 patients with p usher syndrome. J Neurol. 2006;253:1367-9, doi: 10.1007/s00415-006 0 216-x.
  • 21. Perennou DA, Mazibrada G, Chauvineau V, Greenwood R, Rothwell J, G resty MA, et al. Lateropulsion, pushing and verticality perception in hemispher e stroke: a causal relationship? Brain. 2008;131:2401-13, doi: 10. 1093/brain /awn170.
  • 22. Karnath HO, Johannsen L, Broetz D, Ferber S, Dichgans J. Prognosis of contraversi ve pushing. J Neurol. 2002;249:1250-3, doi: 10.1007/s00415 002-0824-z.
  • 25. Cincura C , Pontes-Neto OM, Neville IS, Mendes HF, Menezes DF, Mariano DC, et al. Validation of the National Institutes of Health Stroke Scale, modified Rankin Scale and Barthel Index in Brazil: the role of cultural adaptation and structured interviewing. Cerebrovascular dis eases (Basel, Switzerland). 2009;27:119-22, doi: 10.1159/000177918.
  • 26. Paci M, Nannetti L. Physiotherapy for pusher behaviour in a patient with post-stroke hemiplegia. J Rehabil Med. 2004;36:183-5, doi: 10.1080/ 16501970410029762.
  • 27. Paci M, Rinaldi LA. Physiotherapy for pusher behaviour. NeuroRehabilitation. 2005;20:347.
  • 28. Broetz D, Karnath HO. New aspects for the physiotherapy of pushing behaviour. NeuroRehabilitation. 2005;20:133-8.
  • 29. Shepherd RB, Carr JA. New aspects for the physiotherapy of pushing b ehaviour, D. Broetz and H.-O. Karnath, Neurorehabilitation 20 (2005), 133-138. NeuroRehabilitation. 2005;20:343-5.
  • 30. Miller EL, Murray L, Richards L, Zorowitz RD, Bakas T, Clark P, et al. Comprehe nsive overview of nursing and interdisciplinary rehabilitation c are of the stroke patient: a scientific statement from the American Heart Association. Stroke; a journal of cerebral circulation. 2010;41:2402-48, doi: 1 0.1161/STR.0b013e3181e7512b.
  • 31. Cumming TB, Thrift AG, Collier JM, Churilov L, Dewey HM, Donnan GA, et al. Very early mobilization after stroke fast-tracks return to w alking: further results from the phase II AVERT randomized controlled t rial. Stroke; a journal of cerebral circulation. 2011;42:153-8, doi: 10.1161/ STROKEA HA.110.594598.
  • 32. Santos-Pon telli TE, Pontes-Neto OM, Colafemina JF, Araujo DB, Santos AC, Leite JP. Pushing behavior and hemiparesis: which is critical for f unctional recovery in pusher patients? Case report. Arq Neuropsiquiatr. 2 007;65:536-9, doi: 10.1590/S0004-282X2007000300035.
  • 33. Tyson SF. Measurement error in functional balance and mobility tests for people with stroke: what are the sources of error and what is the best way to minimize error? Neurorehabil Neural Repair. 2007;21:46-50, doi: 10.1177/15 45968306290662.
  • 34. Wright CJ, Swinton LC, Green TL, Hill MD. Predicting final disposition after stroke using the Orpington Prognostic Score. Can J Neurol Sci. 2004;31:494-8.
  • 35. Kerkhoff G. Spatial hemineglect in humans. Prog Neurobiol. 2001;63:127, doi: 10.1016/S0301-0082(00)00028-9.

Publication Dates

  • Publication in this collection
    20 Dec 2011
  • Date of issue
    2011
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