Cervicocephalic kinaesthesia: reliability of a new test ... · proprioceptive system as a pain...

224 Physiotherapy Research International, 6(4) 224–235, 2001 © Whurr Publishers Ltd

Cervicocephalic kinaesthesia: reliabilityof a new test approach

EYTHOR KRISTJANSSON Faculty of Medicine, University of Iceland, Reykjavík,Iceland

PAUL DALL’ALBA and GWENDOLEN JULL Department of Physiotherapy, Universityof Queensland, Brisbane, Australia

ABSTRACT Background and Purpose. Relocating either the natural head posture(NHP) or predetermined points in range are clinical tests of impaired neck proprioceptionbut memory might influence these tests. Three new tests, reasoned to be more challengingfor the proprioceptive system, were developed. The objectives were to assess the reliabilityof all tests and whether the three new tests were more challenging for the proprioceptivesystem. Method. A test–retest design was used to assess the reproducibility and errors ofall five tests. Twenty asymptomatic volunteers were assessed a week apart, using an elec-tromagnetic movement sensor system, the 3-Space Fastrak. A measure of error magnitudewas used to detect kinaesthetic sensibility. Comparison of the means and their correspond-ing dispersion were analysed descriptively. The between-day intraclass correlationcoefficients (ICCs) were calculated and plots of mean differences between days 1 and 2were conducted to estimate test reliability. Multivariate analysis of variance (MANOVA)and least significant difference (LSD) pairwise comparisons were performed to comparethe test accuracy between different target positions. Results. ICCs were between 0.35 and0.9, but plotting the data modified the interpretation in some tests. Relocating a NHP waseasier when the trunk was in a neutral position than when pre-rotated (error 2.46˚ (±0.2˚)versus 5.95˚ (±0.7˚). Relocating a 30˚ rotation position (error 5.8˚ (±0.6˚) and repeatedlymoving through a target (error 4.82˚ (±0.7˚) was also difficult. Conclusions. The new testswere more challenging than relocating the NHP but the reliability of tests relocatinguncommon positions was questionable.

Key words: kinaesthesia, neck, proprioception, reliability

INTRODUCTION

Altered proprioceptive function associatedwith trauma or degenerative change may bean important factor contributing tosymptoms associated with neck disorders

(Revel et al., 1991; McLain, 1994). Theneck mechanoreceptors are essential forsensing cervical positions and movementsas well as for overall postural control withtheir strong connections with the visual andvestibular systems (Dutia, 1991; Gimse et

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al., 1996). Clinically, the consequences ofaltered cervical mechanoreceptor sensibilitymay be symptoms of dizziness and light-headedness (Oostendorp et al., 1993;Karlberg et al., 1995), disordered balance(Karlberg et al., 1996) or diminished neuro-muscular protection of articular tissues(Proske et al., 1988; Bosjen-Møller, 1991;O’Conner et al., 1992). The function of theproprioceptive system as a pain modulatormust not be forgotten (Wall, 1989). Simple,reliable and valid tests of cervicocephalickinaesthesia are needed to measure bothaltered neck proprioception and outcomesof specif ic rehabilitation programmesaiming to restore normal proprioception.

When measuring cervicocephalickinaesthesia, previous studies have usedsimple neck movements from a startingposition resembling a natural head posture(NHP) (Revel et al., 1991; Loudon et al.,1997; Rogers 1997; Heikkilä and Wen-ngren, 1998). The aim has been to relocateNHP after an active movement (Revel et al.,1991) or to actively relocate a positionwithin a movement plane (Loudon et al.,1997). The reliability of the test to relocatethe NHP (Revel et al., 1991) has not beenestablished but the test to relocate a point inrange has been shown to have good reliabil-ity (ICCs) (Loudon et al., 1997).

Recent research suggests that humanshave a remarkable ability to relocateremembered targets by central motor pro-grammes alone (Gandevia and Burke, 1992;Adamovich et al., 1999). The NHP mighttherefore be relocated without reliance onproprioceptive information. Simple move-ments and common tasks, which have beenstored in the long-term memory, can also beperformed without proprioceptive informa-tion (Rothwell et al., 1982; Nougier et al.,1996). The converse is true for non-learnedcomplex movements (Gandevia and Burke,1992; Nougier et al., 1996). Based on this

knowledge three new tests were developedwhich might place more demand on theproprioceptive system.

The first were tests of complex move-ments where subjects drew an infinity sign(figure-of-eight on its side (∞)) with move-ment of the head. In the first test, subjectsrelocated the NHP following this complexmovement. In the second, subjects repeat-edly targeted the NHP as they passedthrough the centre of the figure-of-eight,during three successive movements. To theauthors’ knowledge kinaesthesia has notbeen tested before during movement. Athird test was adapted from the smooth pur-suit neck torsion test (SPNT) (Gimse et al.,1996; Rosenhall et al., 1996). The SPNTwas devised to differentiate patients withdizziness of cervical origin from patientswith diseases involving the posteriorintracranial fossa and Ménière’s disease(Tjell and Rosenhall, 1998). The tests ofmovement of a subject’s eyes as they fol-lowed a target, were compared in NHP andone in which the neck was rotated beneaththe stationary head. The test detected pro-prioceptive deficits only when the neck waspre-positioned in rotation. In the presentadaptation for a kinaesthetic test, the headwas maintained in the mid-line, whereas theneck or trunk was positioned in 30˚ of rota-tion. The subject’s task was to relocate theneutral head, neck trunk position and thenreturn to the start position (that is, a relative30˚ position). It was reasoned that thechanged head–trunk alignment would placemore demand on the neck proprioceptivesystem.

The present study assessed the repro-ducibility and relocation errors of the threenew tests as well as the two more conven-tional tests (Revel et al., 1991; Loudon etal., 1997). It was undertaken to give someinsight as to whether the three new testsmight pose a greater challenge to the pro-

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prioceptive system in asymptomatic sub-jects in the first instance.

METHOD

A test–retest study design was used toassess the reliability of the measurements.

Subjects

Twenty asymptomatic volunteers weredrawn from a pool of students and stafffrom The University of Queensland, Aus-tralia. Subjects with a current or pasthistory of musculoskeletal pain in the neckand upper limbs were not considered. Ethi-cal clearance was obtained from theUniversity Medical Ethics Committee andall subjects provided informed consent toparticipate. Even though all reported to beasymptomatic at the time of testing, it waslater revealed that one subject had a longhistory of intermittent neck pain. She wasomitted from the analyses and seven malesand 12 females, mean age 31.5 (±10) years(2 standard deviations (SDs)) were retainedin the study.

Instrumentation and measurements

A 3-Space Fastrak system was used in thepresent study (Polhemus Navigation Sci-ence Division, Kaiser Aerospace, Vermont).The Fastrak is a non-invasive electromag-netic measuring instrument, which tracksthe positions of sensors relative to a sourcein three dimensions. It has previously beenused to assess position sense in the trunkand the lumbar spine (Maffey-Ward et al.,1996; Swinkels and Dolan, 1998). In thepresent study, one sensor was placed on theforehead and the other over the spinousprocess of C7. The electromagnetic source(transmitter) was placed in a box attached tothe back of a wooden chair. A previous

study has demonstrated that the 3-SpaceIsotrak system, which is similar equipment,is accurate to within ±0.2˚ (Pearcy andHindle, 1989). The Fastrak was connectedto an IBM-compatible personal computerand continually recorded the positions ofthe sensors relative to the source during theentire test sequence.

A software program was written toformat and process the data for analysis.The software program made it possible toconvert the data directly into angle files andgraphs and to visualize the entire testprocess in real time on the screen. The rateat which individuals performed the move-ments was not formally controlled althoughall subjects were instructed to move at acomfortable slow pace. The data obtainedfrom the Fastrak consisted of a 3 × 3 matrixof direction cosines for the orientation ofthe forehead electrode relative to the elec-trode placed on C7. These matrices werethen analysed to give successive angularrotations (Euler angles) of the head relativeto C7, about three orthogonal axes. In thisway, the primary movement of axial rota-tion and the simultaneous coupled rotationsof flexion or extension and lateral flexionwere recorded, representing the accuracywith which the subjects could relocate thetarget positions in each task.

Tests of cervicocephalic kinaesthesia

The movement of axial rotation was chosenas the predominant test movement ashumans use rotation most commonly inexploring the external environment (Taylorand McCloskey, 1990; Rubin et al., 1995).

Test 1 Relocation to the NHP (Revel et al.,1991)

The starting position was sitting with thehead in NHP. Subjects were asked to per-

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form full active cervical rotation to the leftand right in turn and then to return and indi-cate when they considered they had relocatedthe starting position as accurately as possible.This point was recorded by activation of theelectronic marker switch. Between each testmovement, the subject’s head was manuallyadjusted back to the original starting positionby the principal researcher who was guidedby the real-time computer display. The exam-iner’s accuracy in relocating subjects’ headswas within ±0.2˚, as indicated by the marker,which changed colour from red to greenwhen the accuracy was within the set limits(Figure 1).

Test 2 Relocation to the 30˚ rotation position and to NHP (Loudon et al., 1997)

In this test, the examiner pre-positioned thesubject’s head in 30˚ left rotation and subse-quently in right rotation. The computervisual display unit (VDU) guided theresearcher. A marker was placed to indicatethe 30˚ position. Subjects were permitted toconcentrate on this position of reference fora few seconds. They then turned their headto NHP and then returned to the 30˚ rota-tion position. Recordings were taken oneach occasion subjects returned to the NHPand to the 30˚ position.


FIGURE 1: Relocating a subject’s head to natural head posture (NHP).

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Test 3 Preset trunk rotation

Subjects sat on a chair positioned on a spe-cially constructed platform. A familiarizationsession was conducted before the formal test.Subjects first concentrated on their NHP.Whilst the researcher held the subject’s headsteady, the platform (and therefore the sub-ject’s trunk) was rotated to a pre-marked 30˚position of left rotation. Subjects wererequired to relocate their NHP with respectto the body and then return to the startingposition (30˚ relative neck rotation). Follow-ing three trials in left trunk rotation, the testwas repeated with the trunk rotated to theright.

Test 4 Figure-of-eight relocation test

Subjects were taught to perform a discreetfigure-of-eight movement by moving thehead. As a guide, a 10-cm diameter diagramof a figure-of-eight lying on its side (∞)was placed on a stand one metre in front ofthe subject. Subjects were instructed totrace the figure-of-eight with their nose toconfine movement predominantly to theupper cervical spine. Each subject was per-mitted three practice trials of the movementwith their eyes open. The examiner cor-rected the performance if the movementwas too little or too large, that is, involvingthe lower cervical spine. In the formal test,subjects performed the movement threetimes and, after each trial, were required torelocate to the start position as accurately aspossible.

Test 5 Figure-of-eight movement test

In this test, subjects repeated the figure-of-eight movement three times, withoutstopping, as consistently as possible. Eachtime a crossover was made in the figure-of-

eight movement, subjects were asked topass through their NHP as accurately aspossible. They therefore crossed the startingposition f ive times in the test sequence.There was no practice in advance of thistest.

Procedure

Two researchers conducted the testing. Onegave instructions to subjects and the otheroperated the computer and applied themarker in response to subjects’ instructionsin each test. Tests 1–4, aiming at relocationof target positions of the head were con-ducted first, followed by Test 5 where theaim was to move repeatedly through thetarget position. Three trials of each test wereperformed to the left and then to the right.For tests 4 and 5, three repetitions of thefigure-of-eight movements were performed.

Subjects were seated for all tests on awooden chair with a backrest with handsresting in their laps. They wore a light-weight, adjustable helmet for attachment ofthe forehead sensor. This ensured the sameplacement of the forehead sensor duringhead or neck movements and prevented leadtraction on the sensor. The sensor placedover the C7 spinous process was fastenedwith a double-sided tape so there was nomovement of the sensor on the skin, and thelead from the sensor was secured.

The procedure was similar for all tests.For consistency, the researcher read theinstructions of the particular task inadvance of each test. Before each testsequence, subjects were blindfolded. Theblindfold was removed after the trials to theleft and right as well as between tests. Sub-jects sat relaxed with the head naturallypositioned to the front for tests involvingrelocating their NHP. They concentrated onthat position for a few seconds and this

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position was recorded by the Fastrak as thezero starting position. This was the positionof reference, both for subjects and the cal-culations of repositioning error. The sameprocedure was undertaken for the 30˚ base-line starting positions of tests 2 and 3,except that the researcher positioned thesubject’s head manually. Following the per-formance of each test, subjects were askedto say ‘Yes’ clearly when the starting targetposition was relocated. This point wasmarked on the computer. No verbal cueswere given to subjects about their actualperformance. All subjects were examined inthe afternoon within the same week for boththe test and the retest trials.

Data management and analyses

The criterion variable used to measurekinaesthetic sensibility was a measure oferror magnitude (test accuracy) for reloca-tion of the target position. In tests 1–4,relocation accuracy to NHP was analysed.Tests 2 and 3 also tested reproduction of the30˚ rotation position. The absolute value ofthe error was calculated for the angularmotion of axial rotation for each trial. ForTest 5, the ability to repeatedly movethrough a target, both the angular values forthe error in axial rotation and the linear dis-tance of the forehead sensor from thecrossover point were calculated from 3-DCartesian co-ordinates. The crossover pointwas defined as the point at which this dis-tance was smallest from the original startingposition (NHP).

The mean error of the three trials for eachtest was calculated for each individual. Thebetween-day intraclass correlation coeffi-cients (ICCs) were calculated according toShrout and Fleiss (1979), Model 2,1. Plotswere also derived for the mean differences (2SD) between repeated measurements on days

1 and 2 using the method of Bland andAltman (1986) as agreement between twomeasurements is better represented by plot-ting the data. A multivariate ANOVA (Pillai’sTrace) was used to investigate whether therewere any differences in the relocation errorsbetween the different tests. Post hoc LSDpairwise comparisons were performed toinvestigate any differences demonstratedbetween tests in the formal analysis.

RESULTS

Relocation accuracy

For the initial analysis, data from days 1 and2 were combined. Table 1 documents themean relocation errors in axial rotation forall tests. These data suggest that errors weregreater in relocating the 30˚ positions intests 2 and 3 and NHP in Test 3 (presettrunk rotation) compared with relocatingNHP in tests 1, 2 and 4. The magnitude oferror in Test 5 was between that of thesetwo groups, but closer to the higher values.The results of the ANOVA revealed therewere significant differences between testpositions (F(6.0,13) = 8.4; p = 0.001). Thepost hoc analyses (LSD pairwise compar-isons) revealed that of the 21 possiblecombinations, there were statistically signif-icant differences between 14 pairs of tests.The tests that did not demonstrate signifi-cant differences were the following:

• Test 1 versus Test 4• Test 3 (NHP) versus Test 2 (30˚)• Test 3 (NHP) versus Test 3 (30˚)• Test 3 (NHP) versus Test 5• Test 2 (30˚) versus Test 3 (30˚)• Test 2 (30˚) versus Test 5• Test 3 (30˚) versus Test 5

which confirmed preliminary observations.


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Reliability

Table 2 presents the relocation errors aver-aged over all trials for each test on days 1and 2 and the corresponding between-dayICCs. The results indicated that there weresome differences between tests in betweenday reproducibility but the ICCs for all testslay from 0.35 to 0.90. Any observed differ-ences between tests to the left and rightwere not statistically significant (post hocpaired Student’s t-tests).

Three tests were chosen to demonstratethe plots of the mean differences and 2 SDsof the differences between days 1 and 2.

These were Test 1, relocating the NHP fromthe left (Figure 2), Test 3, for relocation ofthe 30˚ position from the left (Figure 4) andTest 5, the movement test (Figure 4).

They were chosen as they demonstratedfair to excellent agreement according totheir ICC values (0.44, 0.61 and 0.90,respectively). In interpreting the plots, eachdot represents an individual score. Theactual differences between days 1 and 2 areon the y axes and mean values for Day 1plus Day 2 are on the x axes. The plotsdemonstrate that the variance between dayswas much greater in Test 3 with an ICCscore of 0.61 (Figure 3) than in Test 1 with

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TABLE 2: Within-days average relocation error after axial rotation and the ICCs for between-day agreement (n=19)

Test Target position Direction of movement Mean relocation error Mean relocation error ICCDay 1 (SD) Day 2 (SD)

Test 1 NHP From left 2.16˚ (1.36˚) 2.96˚ (1.20˚) 0.44NHP From right 2.45˚ (1.48˚) 2.26˚ (1.18˚) 0.35



Test 4 NHP After ∞ 2.04˚ (1.46˚) 2.81˚ (1.62˚) 0.67Test 2 30˚ To left 7.19˚ (3.87˚) 5.8l˚ (4.20˚) 0.74

30˚ To right 5.03˚ (3.37˚) 5.39˚ (3.71˚) 0.69Test 3 30˚ To left 7.05˚ (5.73˚) 6.68˚ (5.63˚) 0.61

30˚ To right 4.80˚ (3.20˚) 5.31˚ (5.03˚) 0.52Test 5 ∞ During movement 4.77˚ (3.19˚) 4.86˚ (3.05˚) 0.90

TABLE 1: Mean axial rotation relocation error (n=19)

Test Target position Mean 1 SD

Test 1 NHP 2.46˚ 1.32˚Test 2 NHP 3.29˚ 2.23˚Test 3 NHP 5.95˚ 4.10˚Test 4 NHP 2.43˚ 1.57˚Test 2 30˚ 5.85˚ 3.81˚Test 3 30˚ 5.96˚ 4.65˚Test 5 ∞ 4.82˚ 3.08˚

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FIGURE 2: Plot of the agreement between days in relocating NHP from left rotation in Test 1. Mean differ-ence is –0.8˚ and 2 SD (±3.0˚).

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FIGURE 3: Plot of the agreement between days in relocating the left 30˚ position in Test 3. Mean difference is0.37˚ and 2 SD (±12.0˚).

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an ICC score of 0.44 (Figure 2). Neverthe-less, the plot and the ICC (0.90) for Test 5both demonstrated good agreement betweendays (Figure 4). The plots between the trialsperformed on days 1 and 2 showed the samepattern as plotting the averaged of threetrials between days, confirming the appro-priateness of using averaged values to plotthe difference between days.

DISCUSSION

The present results demonstrate that thekinaesthetic tests assessed in this study maybe divided into two classes with respect todifficulty. Best accuracy was demonstratedin relocating NHP when the trunk was inneutral (tests 1, 2 and 4) (see Table 1). Fur-thermore, the magnitude of the relocation

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error for NHP in these tests was similar tothat reported for asymptomatic subjects intwo other kinaesthetic studies relocating theneutral position of the lumbar spine wherethe same equipment was used (Maffey-Ward et al., 1996; Swinkels and Dolan,1998). Subjects demonstrated greater relo-cation errors in the tests in which the trunkwas preset in rotation, whether they wererequested to relocate to NHP or a 30˚ rota-tion position (Test 3). Relocating the 30˚neck rotation position (Test 2) and movingaccurately through a target (Test 5) provedas difficult and there were no statisticallysignificant differences between these tests.These tests also demonstrated more vari-ability (see Table 1).

The smaller relocation error in testsrequiring return to a familiar NHP (tests 1,2 and 4) as compared to those involving anon-familiar posture (Test 3) or unfamiliartask (Test 5) reflects previous research(Bizzi et al., 1992; Gandevia and Burke,1992; Nougier et al., 1996; Adamovich etal., 1999) and may support the basis fordeveloping these new tests. However, theaccuracy in relocating NHP after complex

movement (Test 4) was unexpected. Thefamiliar target of the NHP may have beenthe overriding influence. Experimentalbrain research indicates that ascendingafferent signals can be selectively gated atall levels of the central nervous system(CNS) according to the relevance of theincoming information (Collins et al., 1998;Loeb et al., 1999). It could also be reasonedthat moving the neck in a complex patternmight input a massive stimulation to theneck mechanoreceptors (Prochazka andGorassini, 1998). Recent research has alsorevealed attenuation of ‘muscular sense’during active movements, which is mostevident during large, rapid movements(Collins et al., 1998). This may indicate thatTest 4 did not challenge the proprioceptivesystem in the way it was postulated to do soin this study.

The ‘between-day’ reliability (ICCs) ofall tests was between 0.35 and 0.90 (seeTable 2). However an overriding factor wasrevealed in the plots of the differencesbetween days for tests 1, 3 and 5 (see figures2–4). These showed that the standard devia-tion of the difference was much greater in

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FIGURE 4: Plot of the agreement between days in moving through the target in Test 5. Mean difference is0.09˚ and 2 SD (±3.7˚).

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Test 3 with a higher ICC than in Test 1 with alower ICC. Greater fluctuation in the scoreson Day 2 compared with Day 1 in Test 3indicates that this target position may be toounreliable to monitor changes in cervico-cephalic kinaesthesia. These results confirmthat reliability of repeated measurementscannot be evaluated by correlation coeffi-cients alone (Keating and Matyas, 1998).The ICCs do not indicate the magnitude ofscore fluctuations in degrees. This informa-tion is highly relevant if the tests advocatedhere are to be used to monitor changes incervicocephalic kinaesthesia in patients withcervical musculoskeletal disorders. By alsocalculating the mean difference and the stan-dard deviation of the difference betweenrepeated measurements in accordance withBland and Altman (1986), it is possible toknow whether an observed change representsreal change in cervicocephalic kinaesthesiaor is a fluctuation typically observed in thetest. The results of the present study supportthis method. The results of the plot and ICCfor Test 5 are, however, an example whereboth statistical methods demonstrate goodagreement.

The usefulness of a test is dependent onits ability to detect both people with theimpairment and without the impairment.The target positions in Test 3 (a new test)and the 30˚ target position in Test 2 (a pre-viously introduced test) demonstratedgreater errors and variability than someother targets in this study. Therefore thesetests seem to be unreliable. Nevertheless,Test 2 has detected a difference betweenasymtomatic subjects and whiplash patients(Loudon et al., 1997). The error and vari-ability in Test 3 reflects the problemencountered when designing a test reasonedto rely more on proprioceptive function.The function of easier tests used to detectimpaired position sense may already be

stored in the long-term memory. Thus thedilemma, which requires further study, isthe choice between tests with greater vari-ability but with some evident sensitivity andtests with more accuracy but which mayrely more on memory than genuine kinaes-thetic sense.

When reviewing the methodology of thepresent study, the 3-Space Fastrak devicewas chosen for its accuracy (Pearcy andHindle, 1989). Previous studies have used alight beam (laser light) fastened to the top ofthe head by a helmet (Revel et al., 1991) anda simple cervical range-of-motion device(CROM) (Loudon et al., 1997). Direct com-parisons of results are therefore not possible.The use of a lightweight helmet to attach theforehead sensor may have given subjectssome exteroceptive cues due to the circum-ferential pressure on the skin (McNair et al.,1996; Birmingham et al., 1998). Any influ-ence of the lightweight helmet cannot bedifferentiated in the present study. Theamount of practice was the same for all sub-jects but differed for each test according tohow difficult it was to understand its perfor-mance. The ordering of tests was notrandomized, which may have resulted insome learning effects across tests.

CONCLUSION

The kinaesthetic tests examined in the pre-sent study may be divided into two classeswith respect to difficulty. Relocating theNHP was significantly more accurate thanrelocating uncommon postures and movingthrough a target. The discrepancies in theICCs and plots of data, question the use ofICCs as the only measure of reliability. Afuture dilemma appears to be a compromisein choice between tests which may rely onmemory and tests that challenge the propri-oceptive system.


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ACKNOWLEDGEMENTS

The authors would like to acknowledge the financialsupport of Centre of National Research on Disabilityand Rehabilitation Medicine (CONROD, Queens-land, Australia) to this research and also by part theAssociation of Icelandic Insurance Companies. Thetechnical assistance in writing the software programswas given by Mr Scott Magee.

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Address for correspondence: Eythor Kristjansson,Faculty of Medicine, University of Iceland, LÊkna-gardur IS-101, ReykjavÌk, Iceland (E-mail:[email protected]).

Submitted June 2000; accepted March 2001

PRI 6(4) crc 4/12/01 3:26 pm Page 235

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