Scale for Contraversive Pushing: Cutoff Scores for Diagnosing "Pusher Behavior" and Construct Validity

Introduction

"Pusher behavior" (PB) is a poorly understood disorder exhibitedby some people with stroke. This behavior has 3 typical features:(1) contralesional tilted posture with severe imbalance, (2)tendency to push strongly toward the paretic side with the nonaffectedlimbs, and (3) resistance to external correction of the tiltedposture.¹ Researchers have reported different findings withregard to the prevalence of PB in the acute phase after stroke.Some authors found that 5% to 10% of people receiving rehabilitationfor stroke exhibited the behavior,^2–4 but others reportednotably higher values, from 40% to 50%⁵ and 63%.⁶ Most likely,this large discrepancy is mainly attributable to the use ofdifferent criteria for diagnosis, although it also may be afunction of the interval between stroke onset and examination.Other terms that occasionally have been used to indicate posturalcontrol problems similar to PB in people who have had a strokeare "listing phenomenon"^3,7 and "lateropulsion,"⁸ but theseterms have not been used with a unique meaning. Recently, Karnath⁹made a useful terminological distinction by indicating preciselythat active pushing and resistance to correction of postureare the main features that distinguish PB from other posturaldisorders in stroke.

Although few data are available, PB may hinder or at least delayfunctional recovery, especially balance and gait functions.²Therefore, in recent years, this behavior has received increasinginterest. There is growing agreement that PB reflects some misrepresentationof verticality,^10,11 but the exact mechanism is still unclear.The orientation of the body relative to the gravito-inertialforce requires an implicit representation of verticality thatis critical for balance control. This representation is basedon visual, somesthetic, and vestibular information.¹¹ Becausepeople who have had a stroke may show a biased perception ofuprightness,¹² it has been suggested that PB may emerge as anextreme form of this misrepresentation; that is, people withPB may tend to align their body posture with a contralesionallytilted perceived vertical.¹¹ Indeed, Perennou et al¹¹ measuredthe segmental body orientation in people who had PB and whowere seated on a laterally unstable, rocking platform and wereasked to keep their bodies aligned to the vertical. The authorsfound that these people were able to align the head correctlyto the vertical but showed a remarkable tilting of the pelvistoward the contralesional side. In contrast to these results,Karnath et al¹⁰ found that people with PB, in the absence ofvision, felt that their bodies were oriented upright when theywere tilted an average of 18 degrees to the ipsilesional, ratherthan to the contralesional, side; moreover, the perceived verticalof these people was within normal limits when they were allowedto view the structured surroundings. Therefore, the authorshypothesized that the disorder may be the consequence of a conflictbetween 2 reference systems, that is, a normal visual verticaland an ipsilesionally tilted postural vertical. Not surprisingly,the rehabilitation approaches suggested on the basis of thesepathophysiological findings are quite different.^10,13

Valid and reliable assessment instruments are necessary to identifythe presence and the severity of the behavior, to study theunderlying mechanisms, to compare the effectiveness of differenttreatment strategies, and to define the prevalence and the prognosisof the disorder.

Karnath et al¹⁰ developed an assessment tool, the Scale forContraversive Pushing (SCP), aimed at diagnosing the presenceof PB and quantifying its severity. The SCP comprises 3 sections,each assessing a particular feature of the syndrome, namely,the symmetry of spontaneous body posture (section A), the useof nonaffected extremities (leg or arm) to push by abductionand extension thrust (section B), and the resistance to passivecorrection of the tilted posture (section C). For each item,the score ranges from 0 to 1. Because each feature is examinedin both sitting and standing positions, the maximum score ineach section is 2. Recently, the authors completed and integratedinstructions and task definitions for SCP administration andscoring.¹⁴ The SCP is shown in the Appendix. We evaluated somepsychometric characteristics of the SCP, namely, interraterreliability, internal consistency, and diagnostic accuracy,in a sample of 26 people who had recently had a stroke and whowere selected on the basis of the presence of postural impairment.¹⁵We found that the interobserver reliability of the SCP was veryhigh for both subscores (intraclass correlation coefficients=.944, .929, and .939 for sections A, B, and C, respectively)and total score (intraclass correlation coefficient= .971).The scale also showed excellent internal consistency (Cronbachalpha=.919).

With regard to the validity of the SCP as a diagnostic toolfor PB, we addressed the issue of the appropriate cutoff scoresfor the scale. Cutoff scores for the SCP have not been definitivelyestablished, and controversy currently exists regarding themost appropriate way to interpret SCP scores. On the basis oftheir clinical experience, in their first article on the topic,Karnath et al¹⁰ suggested a score of $≥$ 1 in each section of thescale as the cutoff criterion for making the diagnosis of PB.In their study on the natural history of PB after stroke, however,Danells et al⁶ used a much less conservative criterion and assigneda diagnosis of PB to all people who had an SCP total score ofgreater than 0, but they did not assess the validity of thiscutoff score. We investigated the validity of the original criteriaof Karnath et al¹⁰ by calculating the agreement between theclinical diagnosis, according to the recommendations of Davies,¹and the SCP diagnosis. We found that the criteria of Karnathet al¹⁰ led to many false-negative results when applied to asample of people with stroke and postural impairment. Consequently,we proposed the use of a different criterion, that is, a scoreof $≥$ 0 in each section of the SCP; this criterion improved substantiallythe validity of the scale as a diagnostic tool for PB in thatselected sample of people with stroke.¹⁵ This criterion, however,as well as the other suggested cutoff points for the SCP, needsto be tested in an unselected, more heterogeneous, and largersample of people with hemiplegia, in whom the rate of true-negativeresults (people without a diagnosis of PB) could be expectedto be very high.

The construct validity of the SCP has not been formally investigatedyet. Because PB is a distinctive disorder of postural controlin which the perception of body orientation is severely disturbed,^10,11it may be expected that the disorder will impair activitiesthat require managing gravitational force when moving the bodyto an upright posture and balancing. In the acute stage of recoveryfrom stroke, balance impairment is a strong predictor of functionin terms of activities of daily living and mobility,¹⁶ and theseverity of balance impairment correlates with the severityof disability.¹⁷ On the basis of these findings, we believedthat the construct validity of the SCP would be supported bya moderate correlation between SCP scores and balance, mobility,and disability scores.

The present study was primarily aimed at investigating the validityof the suggested cutoff scores for the SCP and at evaluatingthe construct validity of the scale. A further objective wasto estimate the prevalence of PB and its relationship to theside of the lesion in people receiving neurorehabilitation forstroke.

Method

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Method

Participants

All consecutive patients admitted for stroke to 2 inpatientrehabilitation hospitals (Villa Fiorita Hospital, Prato, Italy,and Piero Palagi Hospital, Florence, Italy) from January 2006to December 2006 were included in the study, provided that theymet the following 4 criteria: first stroke; monolateral stroke,as indicated by computed tomography scans or magnetic resonanceimaging; recent stroke ( $≤$ 30 days from onset); and presence ofat least minimal unilateral motor impairment at upper or lowerlimbs or presence of balance deficit (or presence of both),as indicated by impaired performance on the motricity and balancesections of the Fugl-Meyer Assessment Scale (FM).¹⁸ The characteristicsof the selected study participants are shown in Table 1. Participantsgave their written informed consent for collection, storage,and use of personal data.

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Table 1. Characteristics of 105 Study Participants

Assessment

At admission to the rehabilitation unit, each participant wasassessed by a staff physical therapist, who administered theFM, the mobility section of the motor assessment chart developedby Lindmark and Hamrin (LIND-MOB),¹⁹ and the Barthel Index (BI).²⁰These tests are routinely administered to all people admittedto the Villa Fiorita and Piero Palagi hospitals for stroke rehabilitation.The FM is a 226-point multiple-item scale that evaluates balanceand motricity, sensation, range of joint motion, and pain inthe paretic arms. All items are scored on a 3-point (0–2)ordinal scale, in which 0 indicates no function. The excellentpsychometric characteristics of the FM are well established.²¹The LIND-MOB evaluates an individual's abilities in rollingto the affected and nonaffected sides, sitting up from a lying-downposition and the reverse, leaning forward from a seated positionto touch the feet, standing up, and walking. Items are scoredaccording to the need for assistance in order to complete thetask on a 4-point (0–3) ordinal scale, in which 0 indicatesthe inability to perform the task. In a sample of 21 peoplewith acute stroke, the LIND-MOB showed good intrarater reliability(kappa values ranging from .68 to .84) and interrater reliability(kappa values ranging from .68 to .76).²² The BI, a 10-itemperformance-based scale that evaluates independence in basicactivities of daily living, has been shown to have excellentreliability and validity.²³ Because the presence and the severityof PB are expected to interfere with balance, mobility, andfunctional level, these evaluations were used to estimate theconstruct validity of the SCP.

Four examiners assessed the presence and severity of PB within3 days of admission. One examiner was a geriatrician with experiencein stroke rehabilitation. The others were physical therapistswith many years of experience with people who have had a stroke.At each rehabilitation unit, people were independently evaluatedby 2 examiners within a few hours of each other. One of theexaminers (MP and CB at Villa Fiorita and Piero Palagi hospitals,respectively) selected participants and made the clinical diagnosisof PB according to the recommendations of Davies.¹ The clinicalexamination in the 2 hospitals was based on the same criteriaand focused on careful observation of people while lying down,sitting, standing, weight transferring, and walking. The examinerswatched for characteristic signs of the behavior, such as whole-bodyincorrect alignment manifested as typical lengthening or shorteningof the affected or unaffected side of the trunk and active extensionin the unaffected extremities with resistance to be moved towardthe unaffected side. However, the examiners also watched forother signs, such as difficulty in placing the unaffected legin the supine position, flexion of the paretic leg while weighttransferring toward the contralateral side during standing,and adduction of the paretic leg in the swing phase of gait.People were diagnosed as having PB when at least 2 of the above-mentionedsigns were present, with one of them judged as severe.

The second examiner (LN or MB) administered the SCP and diagnosedthe participant as having PB or not having PB on the basis of3 cutoff criteria—a total SCP score of greater than 0(ie, the criterion used by Danells et al,⁶ defined as Crit_1);a score of greater than 0 in each SCP section, leading to atotal SCP score of $≥$ 1.75 (ie, the criterion suggested by Bacciniet al,¹⁵ defined as Crit_2); and a score of $≥$ 1 in each SCP section,leading to a total SCP score of $≥$ 3 (ie, the original criterionsuggested by Karnath et al,¹⁰ defined as Crit_3). The secondexaminer was unaware of all earlier assessments as well as theclinical diagnosis of PB.

Data Analysis

The agreement between the SCP diagnosis resulting from the 3different cutoff criteria and the clinical diagnosis was estimatedby calculation of the Cohen kappa coefficient ( ${kappa}$ ). From SCP scoresand clinical evaluations, sensitivity, specificity, predictivevalue of a positive test, predictive value of a negative test,positive and negative likelihood ratios, and global diagnosticaccuracy of the scale were calculated for each criterion, alongwith 95% confidence intervals. The construct validity of theSCP was estimated by calculation of the Spearman rank correlationcoefficients for the SCP total score and subscores and the balancesubscore of the FM (FM-BAL), the LIND-MOB subscore, and theBI score.

Comparisons of the prevalence of a clinical diagnosis of PBin people with right- and left-brain lesions and in people withstroke who were referred to the 2 rehabilitation units werecarried out with the chi-square test.

The level of statistical significance was set at .05. Data analyseswere performed with the statistical package SPSS Version 12.0for Windows.^* Validity indexes and 95% confidence intervalswere calculated with Microsoft Excel 2003.

Results

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Results

Validity of Different Cutoff Criteria

The Figure shows the flow diagram for the study. In the populationstudied, 17 of 105 participants (16.2%) were diagnosed as havingPB on the basis of the clinical examination. The core featuresof PB in these participants are summarized in Table 2. On thebasis of the SCP scores, however, a diagnosis of PB was madefor 65, 19, and 11 participants when Crit_1, Crit_2, and Crit_3,respectively, were used. Consequently, when different cutoffcriteria were used, the clinical and SCP diagnoses differed(Tab. 3), as did the validity indexes of the scale (Tab. 4).When Crit_1 was used, the diagnostic agreement between the SCPand the clinical examination was poor: agreement was found foronly 54.3% of participants (57/105; Cohen ${kappa}$ =.212, SE=.052). Fortywere diagnosed as not having PB and 17 were diagnosed as havingPB by both methods. With this cutoff criterion, 48 participantswere incorrectly diagnosed by the SCP as having PB. Consequently,despite perfect sensitivity, the scale had very low specificity,and the predictive value of a positive test was very low aswell.

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Figure. Flow diagram for the study of the validity of different cutoff scores for the Scale for Contraversive Pushing (SCP). Crit_1=cutoff criterion 1 (ie, total SCP score of>0), Crit_2=cutoff criterion 2 (ie, score of >0 in each of the 3 sections of the SCP), Crit_3=cutoff criterion 3 (ie, score of $≥$ 1 in each of the 3 sections of the SCP), index test=SCP, reference standard=clinical examination method.

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Table 2. Features of Pusher Behavior in 17 Participants With a Positive Clinical Diagnosis

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Table 3. Clinical Diagnosis and Scale for Contraversive Pushing (SCP) Diagnosis Made With 3 Different Cutoff Criteria^a for 105 Participants

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Table 4. Validity Indexes of the Scale for Contraversive Pushing (SCP) With 3 Different Cutoff Criteria^{^a} for 105 Participants

Both Crit_2 and Crit_3 led to much better agreement betweenSCP and clinical diagnoses. The best SCP diagnostic accuracywas found with Crit_2, which correctly diagnosed 98.1% of participants(103/105; Cohen ${kappa}$ =.933, SE=.047). With this criterion, the specificityof the scale was greatly enhanced, without any decrease in sensitivityor the predictive value of a negative test. However, Crit_2led to false-positive results in 2 participants. Crit_3 ledto correct diagnoses in 94.3% of participants (99/105; Cohen ${kappa}$ =.754, SE=.094). No false-positive results were obtained withthe scale when this more conservative criterion was used, but6 participants were classified as not having PB, contrary tothe clinical diagnosis. Therefore, when Crit_3 was used, thescale was highly specific, but its sensitivity was relativelylow.

SCP Construct Validity

Table 5 shows the Spearman rank correlation coefficients forSCP scores and functional (BI), mobility (LIND-MOB), and balance(FM-BAL) examinations. For the SCP total score, the correlationswere moderate to high, and all were significant at the .001level. The values are negative because, for the SCP, lower valuesindicate better function, whereas for the other instruments,the opposite is true. Section A scores showed distinctly highercorrelations with the other measures than section B and C scores.

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Table 5. Spearman Rank Correlation Coefficients^{^a}

Prevalence of PB in Right- and Left-Brain Lesions

According to the clinical examination, the overall prevalenceof PB in the population studied was 16.2%. Prevalence did notdiffer significantly between the 2 rehabilitation units (16.1%and 16.3% at Villa Fiorita Hospital and at Piero Palagi Hospital,respectively; P=.972). With regard to the side of the lesion,no significant differences were found between participants withright- and left-brain lesions (18.4% and 14.3%, respectively;P=.571).

Discussion

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Discussion

Conclusion

Appendix.

References

The main purpose of the present study was to determine the validityof 3 cutoff criteria suggested for using the SCP as a diagnostictool for PB. The results confirmed that the cutoff score usedby Danells et al,⁶ which assigned a diagnosis of PB to all peoplewith an SCP score of greater than 0, is absolutely inadequate,leading to a large number of false-positive diagnoses. Thisresult is not surprising, because most people who have had astroke show an asymmetric posture, with less weight bearingby the affected leg than by the unaffected leg.^24,25 A lateraltilting in itself, however, does not indicate the presence ofclear PB. As indicated in our earlier article,¹⁵ the presenceof all of the typical features of the syndrome seems to be necessaryfor correctly diagnosing PB in people after stroke. The findingsin the present study strongly support this assumption.

The results also indicated that the criterion we suggested inprevious research¹⁵ seems to be the most suitable for makinga correct diagnosis, even when applied in an unselected, morerepresentative sample of people with hemiplegia. However, althoughcorrectly classifying 98.1% of people, this cutoff score misdiagnosed2 participants as having PB. Therefore, when this criterionis used, the presence of a minimal number of false-positivediagnoses cannot be excluded. Conversely, when the originalcutoff score suggested by Karnath et al¹⁰ was used, no false-positivediagnoses emerged. This more conservative criterion proved tobe less accurate than the former because it failed to detectthe presence of the behavior in 6 of 17 people (35%). However,in this larger and heterogeneous sample of people with stroke,it was significantly more suitable than we found it to be inour previous research.¹⁵ This result also was expected becausein the general population of people with stroke and receivingrehabilitation, the rate of true-negative results is expectedto be much higher than that in a sample of people with strokeand selected for the presence of postural disorders.

On the basis of these findings, we suggest that SCP cutoff criteriabe selected according to the aim of the evaluation. For epidemiologicalpurposes, we believe that the cutoff criterion that proved tobe the most accurate, that is, a score of greater than 0 ineach section of the scale (Crit_2), is the most suitable. Thiscriterion may be useful for studies aimed at investigating theprevalence of the syndrome or its association with other features,such as the side of a cerebral lesion or the presence of neglect.There is considerable disagreement among researchers about thesetopics,^2,4–6 and it may be argued that conflicting findingsmay be partially attributable to different criteria for diagnosingPB.

On the other hand, in research about the pathophysiology ofPB, a correct diagnosis is a prerequisite to drawing correctinferences. For example, there is much debate about a hypotheticalbias in the perceived postural or visual vertical and whetherthe bias is contralesional or ipsilesional.^10,11,24,25 We suggestthat, in studies aimed at investigating these issues, the useof both Crit_2 and Crit_3 for diagnosing the syndrome wouldbe advisable. The more conservative Crit_3 should be used forselecting people who definitely exhibit PB, whereas Crit_2 shouldbe used to include people without PB. In this way, people withan uncertain diagnosis would be excluded, and the risk of anincorrect allocation of people to the PB group or the non-PBgroup would be minimized.

The preceding discussion is based on the assumption that theclinical diagnoses were correct. A limitation of the presentstudy was that we did not formally assess the reliability ofthe method used to make the clinical diagnoses. Therefore, possiblebias related to slightly different criteria used in the clinicalexaminations cannot be excluded.

Our findings also provide evidence regarding SCP construct validity,because SCP scores correlated significantly with functional,mobility, and balance evaluations. Not surprisingly, the strongestcorrelation was found with balance scores, because balance isdirectly affected by PB. People with PB, in fact, use theirnonaffected extremities to push toward the contralateral sideand eventually fall.⁹ Differences in the strength of the correlationsfound for the 3 sections of the SCP most likely reflected theparticular aspects of the disorder being investigated. As mentionedabove, active pushing and resistance to passive correction ofposture (assessed in sections B and C) are distinguishing featuresof PB,⁹ whereas laterally tilted posture and falling (assessedin section A) are not.¹⁵ Indeed, symmetry of posture and abilityto sit and stand upright were impaired in a significant proportionof people without PB. These people performed poorly in the balance,mobility, and functional tests but usually scored 0 in sectionsB and C of the SCP. Overall, it may be speculated that PB influencesperformance insofar as it affects the ability to balance. However,a direct effect of active pushing on performance, such as theability to roll and rise from a lying-down position or to transfer,may be present as well.

Recently, a modified form of the SCP was published and validated.²⁶In a small sample of people with hemiplegia (N=19), the authorsfound low to moderate correlations between the revised SCP scoresand balance and functional scores at both admission (r=.52 andr=.43, respectively) and discharge (r=.49 and r=.45, respectively).These values are distinctly lower than the values that we foundfor the original scale. Indeed, the modified version of theSCP is different enough from the original scale to be rathera completely new assessment tool. Our results indicate thatthe original version of the SCP seems to be preferable becauseit correlates better with functional and postural abilities.Moreover, the cutoff score for diagnosing PB with the modifiedscale has not been empirically investigated.

The validity of the SCP also seems to be slightly higher thanthe validity of a lateropulsion scale (LS) developed by D'Aquilaet al.⁸ In a convenience sample of 85 people with stroke evaluatedat admission to a rehabilitation unit, the authors reportedr=.57 for LS and FM-BAL scores and r=.56 for LS and mobility(Functional Independence Measure) scores. Overall, the 13 motoror mobility items of the Functional Independence Measure thatassess self-care, sphincter control, transfer, and locomotionare quite similar to the items of the BI. Both of these valuesare lower than the values found in the present study. In additionto reliability and validity, however, evaluation instrumentsshould demonstrate good responsiveness, that is, the abilityto detect changes over time.^27,28 Further research should beaimed at comparing the SCP and the LS with regard to this importantpsychometric feature.

Finally, the similar prevalences of PB found in people withright- and left-brain lesions are consistent with other findings.The mean interval from stroke onset in the sample studied was13.7 (SD=6.2) days, and other research has shown that in thissubacute phase, the syndrome affects people with right hemiplegiaand left hemiplegia equally.^2,5 The clinical impression thatPB is more frequently exhibited by people with right-brain injuryis most likely attributable to the fact that the behavior maypersist longer in people with right-brain lesions than in thosewith left-brain lesions. When assessed several weeks from strokeonset, in fact, PB was found to be significantly more frequentin people with left hemiparesis.⁵

Conclusion

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Discussion

Conclusion

Appendix.

References

The data presented here indicate that the SCP cutoff score suggestedin our previous study¹⁵ is superior to other criteria for correctlyclassifying nearly all people with stroke as having PB or nothaving PB. However, the use of the more conservative originalcriterion of Karnath et al¹⁰ is advisable when the absolutecertainty of no false-positive diagnoses is requested. The constructvalidity of the SCP seems to be slightly higher than that ofother published scales for PB. The sensitivity to change ofthe SCP and of the other scales still needs to be addressed.

Appendix.

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Discussion

Conclusion

Appendix.

References

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Appendix. Scale for Contraversive Pushing (SCP)^10,14^a
^a Reprinted with permission of Lippincott Williams & Wilkins from: Karnath HO, Ferber S, Dichgans J. The origin of contraversive pushing: evidence for a second graviceptive system in humans. Neurology. 2000;55:1298–1304.
^b For sitting, ask the patient to glide the buttocks on the mattress toward the nonparetic side, to transfer from bed to wheelchair toward the nonparetic side, or both. For standing, ask the patient to start walking. If pushing already occurs when the patient is rising from the sitting position, section B is given the value of 1 for standing.
^c Touch the patient at the sternum and the back. Give the following instructions: "I will move your body sideward. Please permit this movement."

Footnotes

Mr Baccini, Mr Paci, and Mr Rinaldi provided concept/idea/researchdesign. Mr Baccini provided writing and data analysis. Mr Baccini,Mr Paci, Dr Nannetti, and Ms Biricolti provided data collection.Mr Baccini and Mr Rinaldi provided project management. Mr Rinaldiprovided facilities/equipment. All authors provided consultation(including review of manuscript before submission).

^* SPSS Inc, 233 S Wacker Dr, Chicago, IL 60606.

Microsoft Corp, One Microsoft Way, Redmond, WA 98052-6399.

References

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