ORIGINAL ARTICLE

Ralf Werner Baumgartner Æ Urs EichenbergerPeter Bartsch

Postural ataxia at high altitude is not related to mildto moderate acute mountain sickness

Accepted: 10 September 2001 / Published online: 28 November 2001� Springer-Verlag 2001

Abstract To evaluate the role of acute mountain sick-ness (AMS) in the pathogenesis of stance abnormalitiesoccurring at high altitude, static posturography wasapplied to 22 healthy subjects at an altitude of 450 mand during a 3-day sojourn at 4559 m. Subjects stood ona platform and sway velocity (S), and sway velocity inthe antero-posterior (SAP) and medio-lateral (SML) di-rections was recorded for 20 s with eyes open (EO) and20 s with eyes closed (EC). Arterialized blood from anear lobe was analyzed to determine the arterial partialpressures of oxygen (PaO2) and carbon dioxide, andoxygen saturation (SaO2). AMS was assessed by theenvironmental symptom questionnaire (ESQ) of Samp-son (cerebral AMS, AMS-C score >0.7). AMS affectedfour subjects on day 1, ten subjects on day 2, and fivesubjects on day 3. Posturographic findings showed nodifference between subjects with AMS and healthysubjects, and no correlation with the ESQ score. PaO2

and SaO2 showed non-significant trends toward lowervalues in subjects with AMS than in those without AMS.Posturographic parameters significantly worsened onthe 1st (EO-S, P<0.001; EC-S, P<0.01; EO-SML,P<0.05), 2nd (EO-S, EC-S and EO-SML, P<0.01) and3rd days (EC-S, P<0.05) at high compared to lowaltitude. Differences in AMS-C score, SaO2 and PaO2

were significant between low and high altitude(P<0.0001). Our data suggest that AMS is not impor-

tant in the pathogenesis of postural ataxia occurring athigh altitude.

Keywords Altitude illness Æ Cerebral dysfunction ÆHypoxia Æ Posturography

Introduction

Subjects who rapidly ascend to altitudes above 2500 mmay develop acute mountain sickness (AMS; Houstonand Dickinson 1975; Singh et al. 1969). The cerebralfeatures of AMS are characterized by headache, nausea,lassitude, dizziness, insomnia and ataxia (Hackett et al.1976). Changes of postural stance occurring at high al-titude are assessed by means of questionnaires (Roachet al. 1993; Sampson et al. 1983), and simple clinicalexaminations like the heel-to-toe (Bartsch et al. 1990)and Romberg tests (Ferrazzini et al. 1989). These meansof assessing postural stance have limitations for the as-sessment of mild ataxia, as quantification is relativelysimple and depends upon the subjective impression ofthe examiner. Static platform posturography is an easyapplicable technique that quantifies postural stabilitywithin a few minutes, may be repeated as often as nec-essary, and may be used for measuring clinically unde-tectable abnormalities of stance (Dichgans et al. 1976;Diener et al. 1984; Scott and Dzendolet 1972; Sheldon1963; Terekhow 1976; Therapeutics and TechnologyAssessment Subcommittee of the American Academy ofNeurology 1993). The platforms are equipped withstrain gauges and record body sway during quiet stance.Static posturography has been used to study sway innormal subjects (Baloh et al. 1994; Bergin et al. 1995;Dichgans et al. 1976; Diener et al. 1984; Scott andDzendolet 1972) and to record the influence of variousdiseases on postural stability (Bergin et al. 1995; Blackand Wall 1981; Di Fabio 1995, 1996; Dichgans andDiener 1985; Norre et al. 1987; Wall and Black 1983).

Severe or moderate postural ataxia is noted in severeAMS (Hackett et al. 1976), whereas mild or no ataxia

Eur J Appl Physiol (2002) 86: 322–326DOI 10.1007/s00421-001-0534-8

R.W. Baumgartner (&)Department of Neurology, University Hospital,Frauenklinikstrasse 26, 8091 Zurich, SwitzerlandE-mail: ralf.baumgartner@nos.usz.chTel.: +41-1-2555686Fax: +41-1-2558864

U. EichenbergerDepartment of Radiology,University of Bern, Switzerland

P. BartschDepartment of Internal Medicine,Division of Sports Medicine,University of Heidelberg, Germany

occurs in mild to moderate AMS (Bartsch et al. 1988;Singh et al. 1969). In previous studies performed in theCapanna Regina Margherita at an altitude of 4559 m,we found that about half of subjects developed mild tomoderate AMS (Bartsch et al. 1988), defined as AMSwithout signs or symptoms of high-altitude cerebraledema (Hackett et al. 1976). To investigate the role ofmild to moderate AMS in the pathogenesis of posturalataxia, static posturography was applied to healthysubjects at an altitude of 490 m and during a 3-day stayat an altitude of 4559 m.

Methods

Subjects and study design

Twenty-two healthy subjects (5 women, 17 men) with a mean (SD)age of 42 (10) years (range 21–54 years) living at altitudes below500 m volunteered to participate in this study, which was approvedby the Ethical Committee of the University Hospital in Bern. Theywere recruited by personal contact and gave written informedconsent to participate. The baseline investigations were performedat an altitude of 450 m in Bern, and the altitude studies were car-ried out in the Capanna Regina Margherita laboratory, which islocated at an altitude of 4559 m [mean (SD) barometric pressure440 (5) mmHg] in the Alps Valais. Baseline investigations consistedof a general physical examination, completion of an environmentalsymptom questionnaire (Sampson et al. 1983) and a clinical ataxiascore, static posturography, and arterial blood sampling. Within 2–4 weeks after the baseline investigations the subjects ascended to4559 m over a 24-h period. From an altitude of 1130 m they weretransported by cable car to 3200 m and stayed overnight at 3600 m[mean (SD) barometric pressure 440 (5) mmHg]. After a technicallyeasy climb over glaciers that took 4–5 h, they arrived at the high-altitude research laboratory (4559 m). There, the above-mentionedinvestigations were repeated after 3 h of rest (day 1) and on thenext two mornings (days 2 and 3).

Static posturography

For each test the subjects stood shoeless for 20 s with eyes open(EO) and then 20 s with eyes closed (EC) on a force-measuringplatform (Stabilometrie Plattform, Toennies, Freiburg, Germany)with their feet placed parallel, 7 cm apart. They were instructed tolook straight ahead at the surrounding room with arms at the sidesand were allowed to stand on the platform until they felt secure.Strain gauges at the four corners of the platform measured thedisplacement of the center of foot pressure in antero-posterior andmedio-lateral directions. The sway velocity (S), as well as the swayvelocity components in the antero-posterior (SAP) and medio-lat-eral (SML) directions of the center of foot pressure were calculatedwith the aid of a computer program (Epson PC AX). In order todetect the effects of high altitude on the different neuronal systemsthat control postural balance, the Romberg quotient for S wascalculated as EC-S/EO-S (Dichgans et al. 1976; Diener et al. 1984).The results for S, SAP and SML are given in cm/s, and for theRomberg quotient as absolute values.

Clinical assessment of AMS and postural ataxia

The environmental symptom questionnaire of Sampson (1983) wastranslated into German and used as described previously (Bartschet al. 1990). Each subject was classified every day at high altitudeaccording to the corresponding cerebral AMS (AMS-C) score aseither having AMS (AMS-C score >0.70) or not (AMS-C score£ 0.7) (Sampson et al. 1983).

Postural ataxia was also quantified using the heel-to-toe testwith a rating scale of 0–4 points. A normal test gave 0 points;staggering gait with balancing movements gave 1 point; inability tofollow the line gave 2 points; a fall gave 3 points; inability to standgave 4 points.

Arterial blood gas analysis

Arterialized blood was sampled from an ear lobe and analyzedimmediately in a blood gas analyzer (‘‘278’’ Ciba Corning Diag-nostics, Dietlikon, Switzerland) to determine arterial partial pres-sures of oxygen (PaO2) and carbon dioxide (PaCO2) as well asarterial oxygen saturation (SaO2).

Statistical analysis

Measurements obtained at high altitude were compared withbaseline values by non-parametric analysis of variance using theFriedman and Wilcoxon signed-rank tests. Differences betweensubjects with and without AMS were compared by non-parametricanalysis of variance (Mann–Whitney U-test). The correlation be-tween different parameters was examined using Pearson’s andSpearman’s rank correlation coefficients. Simple regression analysiswas used to discern a relationship between posturographic pa-rameters and the clinical ataxia score, and the AMS-C score andSaO2, PaO2 and PaCO2 values. P values of less than 0.05 wereconsidered to be statistically significant.

Results

Thirteen subjects were affected for 1–4 days by AMS: 4subjects on the 1st day, 10 subjects on the 2nd day, and5 subjects on the 3rd day at high altitude. Thus, AMSwas present during 19 of 66 subject-days, and absentduring 47 of 66 subject-days. One subject also sufferedfrom high-altitude pulmonary edema on the 2nd day athigh altitude, and five subjects had high-altitude pul-monary edema on the 3rd day at high altitude. Allsubjects were able to complete each posturographic in-vestigation without interruption related to ataxia.

Healthy subjects compared to subjects with AMS

Posturographic findings, clinical ataxia and AMS-Cscores, and arterial blood gas analyses obtained in sub-jects with and without AMS on days 1–3 at high altitudeare given in Table 1. The corresponding data for allsubject-days are shown in Table 2. Posturographic pa-rameters showed no significant difference at high alti-tude when comparing healthy subjects with subjectsaffected by AMS. Subjects with AMS had significantlyhigher AMS-C scores (P<0.01 to P<0.0001), and atrend toward lower SaO2 and PaO2 values compared tosubjects without AMS.

There were no differences between clinical ataxiascores at high altitude when comparing healthy subjectswith subjects affected by AMS. Out of 19 clinical ataxiatests performed in subjects affected by AMS, 15 (79%)were normal (score 0), 3 (16%) had a score of 1, and 1(5%) a score of 2. Out of 47 tests of clinical ataxiaperformed at high altitude in subjects without AMS, 35

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(75%) were normal, 11 (23%) had a score of 1, and 1(2%) had a score of 3.

There was no significant correlation between anyposturographic parameter, AMS-C scores or arterialblood gases. Simple regression analysis showed weakrelationships between all posturographic parameters andclinical ataxia scores (EO-S: r2=0.307; EO-SAP: r2=0.278; EO-SML: r2=0.061; EC-S: r2=0.264; EC-SAP:r2=0.199; EC-SML: r2=0.025; Romberg quotient:r2=0.072), and AMS-C scores and SaO2 (r2=–0.410),PaO2 (r2=–0.521) and PaCO2 (r2=–0.087; wherer2=coefficient of determination).

High- compared to low-altitude findings

Sway velocities increased at high altitude compared tobaseline values. This trend was significant on the 1st

(EO-S, P<0.001; EO-SML, P<0.05; EC-S, P<0.01),2nd (EO-S, EO-SML and EC-S, P<0.01) and 3rd days(EC-S, P<0.05) at high altitude. The Romberg quo-tients remained unchanged at high altitude. Clinicalataxia scores showed a non-significant trend to increaseat high altitude compared to baseline values. The AMS-C scores were higher during the whole sojourn at 4559 mthan at baseline (P<0.001). PaO2 and SaO2 were lower,and PaCO2 was higher at high altitude than at low al-titude (P<0.0001).

High altitude findings

Posturographic parameters, clinical ataxia scores, andAMS-C scores showed no significant change during thestay at high altitude.PaO2 was higher on the 3rd day thanon the 1st (P<0.05) and 2nd days (P<0.01) at high alti-

Table 1 Posturographic findings, clinical ataxia scores, AMS-Cscores, and arterial blood gases in 22 subjects with and withoutacute mountain sickness (AMS) on days 1–3 at high altitude. Eachsubject was classified every day as either having AMS (AMS-C

score >0.7) or having no AMS (AMS-C score £ 0.7). Data arepresented as the mean (SEM). (AP Antero-posterior, ML medio-lateral, PaO2 arterial partial pressure of oxygen, SaO2 arterial ox-ygen saturation, PaCO2 arterial partial pressure of carbon dioxide)

Table 2 Posturographic find-ings, AMS-C scores, clinicalataxia scores, and arterial bloodgases in 22 subjects with andwithout AMS during a 3-daysstay at high altitude. There were19 out of 66 subject-days withAMS and 47 out of 66 subject-days without AMS

Parameter AMS (n=19) No AMS (n=47)

Posturography eyes open sway (cm/s) 92.2 (7.1) 82.0 (2.9)Ap sway (cm/s) 16.8 (2.0) 15.3 (1.0)Ml sway (cm/s) 8.1 (1.4) 6.8 (0.4)Eyes closed sway (cm/s) 153.9 (18.3) 162.2 (11.7)AP sway (cm/s) 33.3 (3.7) 37.1 (4.0)ML sway (cm/s) 10.9 (2.1) 10.0 (0.8)Romberg quotienta 1.7 (0.1) 1.9 (0.1)Clinical ataxia scoreb 0.4 (0.2) 0.3 (0.1)AMS-C score 1.6 (0.1)*** 0.2 (0.0)***PaO2 (Torr)

c 42.8 (1.5)* 47.3 (0.1)*SaO2 (%) 74.7 (2.1) 78.4 (1.0)PaCO2 (Torr)

c 27.6 (0.4) 27.9 (0.4)

*,**Difference between both groups is significant atP<0.05 andP<0.0001, respectively (Friedman test)aQuotient sway velocity eyes open/sway velocity eyes closedbHeel-to-toe test; for details see Methodsc1 Torr=133.32 N/m2

Parameter Day 1 Day 2 Day 3

AMS(n=4)

No AMS(n=18)

AMS(n=5)

No AMS(n=17)

AMS(n=10)

No AMS(n=12)

Posturography eyesopen sway (cm/s)

74.5 (7.8) 83.4 (4.3) 94.1 (9.1) 86.0 (6.5) 105.3 (27.5) 77.9 (5.1)

Ap sway (cm/s) 14.3 (2.0) 15.6 (2.0) 16.0 (2.6) 15.8 (1.8) 21.5 (5.8) 14.8 (1.2)Ml sway (cm/s) 5.5 (0.3) 7.2 (0.6) 8.3 (1.6) 7.2 (0.9) 10.3 (5.3) 6.2 (0.5)Eyes closed sway (cm/s) 127.8 (10.3) 168.2 (19.8) 171.1 (30.2) 156.8 (18.2) 137.0 (31.3) 159.6 (22.0)AP sway (cm/s) 32.0 (4.2) 38.3 (7.2) 33.8 (6.2) 36.2 (6.4) 33.5 (6.7) 36.6 (7.0)ML sway (cm/s) 7.3 (1.7) 10.4 (1.6) 13.8 (3.3) 9.3 (1.0) 7.5 (2.6) 10.1 (1.4)Romberg quotienta 1.8 (0.2) 2.0 (0.1) 1.8 (0.2) 1.8 (0.2) 1.3 (0.1) 2.0 (0.2)Clinical ataxia scoreb 0.0 (0.0) 0.4 (0.2) 0.3 (0.2) 0.3 (0.5) 0.8 (0.4) 0.2 (0.1)AMS-C Score 1.3 (0.4)* 0.3 (0.1)* 1.5 (0.2)** 0.3 (0.1)** 1.9 (0.3)*** 0.2 (0.1)***PaO2 (Torr)

c 44.6 (2.6) 45.7 (1.4) 42.3 (1.9) 45.0 (1.8) 42.5 (3.9) 50.7 (1.7)SaO2 (%) 76.5 (2.5) 77.3 (1.4) 75.5 (2.8) 78.1 (2.5) 71.7 (5.9) 79.7 (1.7)PaCO2 (Torr)

c 28.7 (0.5) 28.5 (0.6) 27.6 (0.6) 28.9 (0.4) 26.8 (0.8) 26.6 (0.6)

*,**,*** Difference between both groups is significant at P<0.01, P<0.001 and P<0.0001, respectively (Mann–Whitney U-test)aQuotient sway velocity eyes open/sway velocity eyes closedbHeel-to-toe test; for details see Methodsc1 Torr=133.32 N/m2

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tude. PaCO2 was lower on the 3rd day compared with the1st (P<0.001) and 2nd days (P<0.01) at high altitude.

Discussion

In the present study, stability of stance (as assessed bystatic posturography) showed no difference betweensubjects affected by mild to moderate AMS and healthysubjects, and there was no correlation between postu-rographic findings and the AMS-C score. Conversely,stability of stance was significantly decreased at highcompared to low altitude.

Inappropriate sensitivity of static posturographymight explain the finding that stability of stance was notdifferent between subjects with and without AMS. Thereported sensitivities of static posturography for de-tecting different oto-neurological diseases range between47% and 100% (Bergin et al. 1995; Black and Wall 1981;Di Fabio 1995; Norre et al. 1987; Wall and Black 1983).The wide variation of sensitivities depends upon theseverity and type of the underlying disease (Di Fabio1995, 1996). The lack of internationally accepted defi-nitions of abnormal balance may also contribute to thediscrepant levels of sensitivity. In the present study,several posturography parameters and heel-to-toe testscores showed a trend to increase at high altitude. Thistrend was only significant for posturographic findings,which confirms the results of previous studies suggestingthat static posturography may be used to disclose clini-cally undetectable postural ataxia (Dichgans et al. 1976;Diener et al. 1984; Sheldon 1963; Terekhow 1976). Thus,it is unlikely that using posturography, a clinically rel-evant difference of stability of stance between healthysubjects and subjects with AMS was missed. Conse-quently, our findings suggest that mild to moderateAMS is probably not relevant for the development ofataxia occurring at high altitude.

Hypoxia or hypoxia-triggered events are assumed torepresent the main cause of neurological deficits occur-ring at high altitude (Severinghaus 1995). Thus, thesubstantial decreases in PaO2 and SaO2 that occurredafter the ascent to high altitude are likely to be the maincause of the concomitant impairment of postural bal-ance. Compared with changes occurring when goingfrom low to high altitude, differences in PaO2 and SaO2

between subjects with and without AMS were small, andcomparable with the results of previous studies per-formed in the same high-altitude research laboratory(Baumgartner et al. 1994; Hohenhaus et al. 1994).Therefore, we assume that the small difference in PaO2

and SaO2 between subjects with and without AMS didnot impose a relevant influence on postural stability.

It is interesting to note that in this study 90% of allheel-to-toe tests performed in subjects with AMS werenormal or mildly abnormal, as indicated by scores of0–1, and the two highest ataxia scores of 3 and 4 werenot achieved by sick subjects. Singh et al. (1969) did notmention postural ataxia as a sign of AMS. Houston and

Dickinson (1975) reported the occurrence of gait ataxiain 12 patients with a ‘‘cerebral form of high-altitudeillness’’. The clinical signs and symptoms, lumbar pres-sure and autopsy findings brought the authors to theconclusion that ‘‘the primary problem seems to havebeen cerebral edema’’ (Houston and Dickinson 1975).Hackett et al. (1976) reported the presence of ataxia in 5of 278 unacclimatized hikers suffering from ‘‘severe’’AMS. However, these authors defined ‘‘severe’’ AMS asthe presence of cerebral edema and pulmonary edema,and all ataxic hikers had cerebral edema (Hackett et al.1976). Houston (1976) mentions ataxia as a typical signof high-altitude cerebral edema (HACE), but does notstate that ataxia is a sign of AMS. In summary, ours andthe above-mentioned studies indicate that mild tomoderate AMS is generally associated with normal ormildly abnormal postural stance at clinical examination,whereas severe ataxia may essentially occur in thepresence of HACE.

The deterioration of postural stance observed in thepresent study consisted of an increase in the sway ve-locity parameters S and SML, whereas SAP and theRomberg quotient remained unchanged. It is importantto note that posturography was used as a general mea-sure for postural stability, because this technique maynot be used to localize dysfunctions and lesions in thenervous system (Di Fabio 1995; Gagey 1991; Thera-peutics and Technology Assessment Subcommittee ofthe American Academy of Neurology 1993). Thus, theabove-mentioned pattern of posturographic changes isprobably not revealing.

In conclusion, stability of stance as assessed by staticposturography significantly deteriorated at high com-pared to low altitude, but showed no difference betweensubjects with and without mild to moderate AMS, sug-gesting that AMS is not important in the pathogenesis ofpostural ataxia found at high altitude.

Acknowledgement The authors declare that the experiments com-ply with the current laws of the country in which the experimentswere performed.

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