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Postural dynamics and habituation to seasickness
Neuroscience Letters 479 (2010) 134–137
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Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Postural dynamics and habituation to seasickness Dror Tal a , Ronen Bar a , Zohar Nachum a , Amnon Gil a , Avi Shupak a,b,c,∗ a
Motion Sickness and Human Performance Laboratory, The Israel Naval Medical Institute, Haifa, Israel Unit of Otoneurology, Lin Medical Center, 35 Rothschild Avenue, Haifa 35152, Israel c The Bruce Rappaport Faculty of Medicine, The Technion, Haifa, Israel b
a r t i c l e
i n f o
Article history: Received 26 March 2010 Received in revised form 3 May 2010 Accepted 13 May 2010 Keywords: Habituation Motion sickness Computerized dynamic posturography (CDP) Vestibular organs
a b s t r a c t The computerized dynamic posturography (CDP) test examines the response pattern to simultaneous, multimodal sensory stimulation. The purpose of this prospective, controlled study was to investigate whether postural dynamics evaluated by CDP are related to seasickness severity and the process of habituation to sea conditions. Subjects included 74 naval personnel assigned to service aboard ship and 29 controls designated for shore-based positions. Study participants performed a baseline CDP test, and subsequent follow-up examinations 6 and 12 months after completion of their training. On those occasions they also completed a seasickness severity questionnaire. Longitudinal changes in postural parameters were examined, as well as a possible correlation between baseline CDP results and final seasickness severity scores. The results indicated longitudinal habituation to seasickness. Reduced scores were found for sensory organization sub-tests 3 and 5 in the first follow-up examination, reflecting increased weighting of visual and somatosensory input in the maintenance of balance. Scores in the second follow-up examination were above baseline values, indicating increased reliance on vestibular cues. These significant bimodal changes were found only in study subjects having the highest degree of habituation to seasickness. A significant decrease in motor response strength was found in parallel with increased habituation to seasickness. Baseline CDP results and postural control dynamics were not correlated with subjects’ final seasickness severity score. These results suggest a potential role for CDP in monitoring the process of habituation to unusual motion conditions. © 2010 Elsevier Ireland Ltd. All rights reserved.
Motion sickness is a normal, universal physiological response to unfamiliar motion patterns, whether real or apparent [12]. The most dramatic form of motion sickness is seasickness; other forms are space sickness, airsickness, carsickness, and the recently described cybersickness, which is common in virtual environment systems that present an optical depiction of inertial motion [1]. The development of seasickness symptoms follows a sequence that varies with the intensity of the stimulus and the susceptibility of the individual. Its main signs and symptoms include epigastric awareness, perioral and facial pallor, cold sweating, salivatory changes, retching, and recurrent vomiting. Repeated exposure to the provocative stimulus results in habituation, in which decreased susceptibility to rough sea conditions may be maintained in spite of significant intervals between voyages, sometimes as much as several weeks [15]. Our current understanding views motion sickness as the result of a conflict between the information processed within a multimodal sensory system, whose function is to determine the individual’s motion relative to the environment. This has been
∗ Corresponding author at: Unit of Otoneurology, Lin Medical Center, 35 Rothschild Avenue, Haifa 35152, Israel. Tel.: +972 4 8568491; fax: +972 4 8568496. E-mail address: [email protected] (A. Shupak). 0304-3940/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2010.05.044
termed the “neural mismatch theory” [11]. A sensory conflict occurs when the integrated sensory signal is at variance with previously stored motion patterns. This results in motion sickness. The conflict is eventually settled when the anticipated relations between the sensory inputs are updated. This induces habituation to the new motion patterns, including a modified motor response [6]. Although the neural mismatch theory is the most widely accepted explanation for the development of motion sickness, there are other hypotheses which might add to our understanding of its pathogenesis. Riccio and Stoffregen [13] suggested that motion sickness is caused by instability of body postural control. This theory predicts an increased incidence of sickness when external motion is imposed at a frequency of 0.1–0.3 Hz, because this interferes with the naturally occurring sway activity. The increased sensitivity to this frequency range has been verified by field studies showing that the greatest incidence of seasickness on board conventional ships is associated with heave, surge and sway acceleration frequencies of about 0.2 Hz [5,10]. Both theories are compatible with the hypothesis that postural responses might reflect both susceptibility to motion sickness and the habituation process. A previous cross-sectional study conducted in our laboratory [14] searched for possible relations between postural control and seasickness susceptibility. The computerized dynamic posturography (CDP)
D. Tal et al. / Neuroscience Letters 479 (2010) 134–137
test was employed to evaluate the response pattern to simultaneous, multimodal sensory stimulation. The results suggested that seasickness-susceptible subjects depend more on somatosensory and visual input, and less on vestibular input, for maintenance of balance. The hypotheses underlying the present study were that postural strategy would be modified with repeated exposure to sea conditions, that these changes would reflect increased habituation to the non-terrestrial motion, and that baseline postural parameters would be correlated with future susceptibility to seasickness. Subjects were 120 male naval recruits aged 18–22 years. The study group included 90 men in basic training, who had been assigned to serve aboard naval vessels which would be making regular voyages. Their training included multiple voyages aboard small vessels in the Mediterranean, mostly in moderate sea conditions. Subjects were engaged in the various activities normally undertaken by naval crew during a voyage, and most of the time were alert and physically active. The control group consisted of 30 recruits designated for shore-based positions. A detailed history was taken from all study participants to exclude previous cochlear or vestibular pathology. Otoneurological examination included otoscopy, bedside testing for static, dynamic, positional and positioning nystagmus, and postural tests. Pure tone air and bone, speech and impedance audiometry were carried out. Exclusion criteria included past vestibular or cochlear pathology, positive findings on otoneurological examination, and hearing loss or abnormal findings in impedance audiometry. All study participants performed a baseline CDP test when recruited to the study, and subsequent follow-up examinations 6 and 12 months after completion of their training (first and second follow-up examinations, respectively). CDP was performed using the EquiTest system (NeuroCom International Inc., Clackmas, OR) according to the standard test protocol [3]. The device has a computer-controlled force platform, which is able to move abruptly in translational or pitch directions as well as in synchrony with a visual surround. The force data are collected and analyzed automatically by the system’s computer. The vertical and horizontal forces applied to the platform are measured by transducers, and the data collected are used to locate the center of foot pressure. The patient’s height and force data are used to estimate the vertical location of the body’s center of gravity and the angle of sway. The CDP procedure is divided into two parts. The sensory organization test (SOT) assesses the use of sensory information by measuring postural sway under conditions in which visual and somatosensory feedback is altered. The change in sway angle is used to move a visual surround or the support surface in synchrony with the individual’s sway. The influence of a lack of somatosensory and visual information on stability is evaluated, as is the subject’s ability to use vestibular input to maintain balance. The SOT is organized into a series of six conditions of increasing difficulty. The first three conditions are performed on a firm surface with eyes open, eyes closed, and finally with the subject’s vision sway-referenced. The final three conditions are performed with the support swayreferenced, with eyes open, eyes closed, and with the subject’s vision sway-referenced. Results of the SOT are calculated based on the maximum peak-to-peak anterior-posterior sway expressed as an equilibrium score ranging from 0 to 100, with 0 indicating loss of balance and 100 indicating perfect stability. The test conditions are described in Table 1. The second part of the CDP is the Motor Control Test (MCT). Successful mobility in the environment requires an individual to react to sudden external disturbances of balance. The MCT evaluates maintenance of balance, expressed by the motor responses to unexpected backward and forward translations and up-anddown pitch movements of the support surface. The latency of the response and the ability to minimize sway are a functional cor-
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Table 1 Sensory organization test conditions. Parameter
Condition 1 Condition 2 Condition 3 Condition 4 Condition 5 Condition 6 Composite
Description Platform
Eyes
Visual surround
Stable Stable Stable Moving Moving Moving Average of conditions 1–6
Open Closed Open Open Closed Open
Stationary Stationary Moving Stationary Stationary Moving
relate of the long loop pathways, including the peripheral nerves, ascending and descending spinal pathways, and brain structures. The adaptation protocol exposes the subject to 5 trials each of pitch perturbations towards the subject and towards the ground. Rotation causes the subject to sway by repeatedly rotating the force plate about its X-axis. This demonstrates the subject’s ability to adapt automatic movement responses to recurring surface movements. The sway induced by the platform’s translations generates angular momentum. To counteract this sway, the subject generates an active response in the opposite direction. The Response Strength parameter measured in degrees/second is the angular momentum produced by the subject’s response. The study participants did not take any medications for at least 48 h before CDP testing. None consumed drugs or alcohol. The CDP follow-up tests in the study group were conducted at least 72 h after disembarking from a voyage, and it was verified that the subject had no symptoms of mal de debarquement [9]. Susceptibility of the study group subjects to seasickness was determined by a seasickness questionnaire, which they completed after their initial exposure to sea conditions and immediately before the follow-up CDP examinations. The questionnaire, adapted from Wiker et al. [19], scores actual seasickness severity during sailing. Seasickness is rated on a scale from 0 to 7, where a score of 7 is given to the most severe grade of seasickness. All participants received a comprehensive explanation of the study’s goals and testing procedures, and gave their informed consent before they started the tests. The Israel Defense Forces Medical Corps Human Research Committee approved the study protocol and testing procedures. Longitudinal changes in seasickness severity scores and CDP parameters were studied by repeated measures one-way ANOVA. A possible correlation between baseline CDP parameters and the Wiker scores found after the initial sailing experience and the first and second follow-up evaluations were examined by the Spearman non-parametric correlation test. The extent to which the variance in SOT and MCT results in the course of the study may be explained by improvement in the Wiker scores was analyzed by repeated measures two-way ANOVA. For this analysis, subjects were assigned to two habituation groups according to the difference between their baseline and final scores on the seasickness severity scale. The factors used for the two-way ANOVA were the time points and the habituation group. Statistical analysis was performed using SPSS software (SPSS, Inc., Chicago, IL) on a personal computer. The baseline and two follow-up examinations were completed by 74 subjects (61.7%) in the study group and 29 (97%) in the control group. The dropouts in the follow-up examinations were due to the unique occupational conditions of the study population. As military personnel, some of the subjects were deployed in remote bases following their training period, and follow-up examinations were very difficult to complete. Others changed their occupation, and were not exposed to sea conditions during the whole of the study period, while still others transferred from the Navy to other
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D. Tal et al. / Neuroscience Letters 479 (2010) 134–137
branches of the Israel Defense Forces. Data analysis comparing the baseline and follow-up tests in the study and control groups was carried out only for subjects who completed all of the tests. After the initial exposure to open sea conditions, the Wiker score for the study group was 6 ± 1.7 (mean ± SD). There was subsequent habituation to sea conditions, as evidenced by a decrease in the sea sickness severity score to 4.77 ± 2.3 after 6 months of regular sailing and 4.11 ± 2.2 after 12 months of sea-going experience. The differences between the average baseline Wiker score and later scores were of statistical significance (p < 0.001, one-way repeated measures ANOVA). Significant dynamics in SOT parameters were found only in the study group. The composite SOT equilibrium score, representing the body’s general postural control ability, declined from a baseline value of 85 ± 4.2% (mean ± SD) to 83.9 ± 5.7% in the first follow-up evaluation, with a subsequent increase to 86.1 ± 3% in the second follow-up examination (p < 0.002, one-way repeated measures ANOVA). These dynamics reflect mainly significant changes in the scores of SOT conditions 3 and 5, which showed a similar bimodal pattern of decrement after 6 months of sailing followed by an increase to above baseline values after 12 months (94 ± 2.6%, 92.7 ± 2.9%, 94.1 ± 2.2%, and 71.4 ± 9.1%, 71.2 ± 11.5%, 75.5 ± 7% for the baseline, first, and second follow-up scores; p > 0.003 respectively; p < 0.003, one-way repeated measures ANOVA). The MCT adaptation protocol showed decreased latency of the motor response to sudden pitch perturbations in the followup examinations when compared with baseline latency values. The average latency for the motor response to sudden pitch perturbations towards the subject and towards the ground in the study group decreased from baseline values of 70.1 ± 10.2 and 49.2 ± 9.9 ms, respectively to 62.9 ± 10.7 and 46.6 ± 8.2 ms in the first follow-up examination and 59.9 ± 11.9 and 44.8 ± 7.9 ms in the second follow-up examination (p < 0.002, one-way repeated measures ANOVA). Improved adaptation scores were also found in the control group, where the average latency for the motor responses to pitch perturbations towards the subject and towards the ground decreased from baseline values of 71 ± 10.6 and 50.3 ± 10.7 ms, respectively to 65.1 ± 15.1 and 49.2 ± 9.7 ms in the first followup examination and 60.6 ± 7.7 and 46.6 ± 8.2 ms in the second follow-up examination (p < 0.001, one-way repeated measures ANOVA). The response strength, which measured the subject’s generated angular momentum counteracting the platform’s movements, decreased significantly between the baseline and follow-up tests only in the study group (9.7 ± 3.1◦ /s, 8.7 ± 3.2◦ /s, 8.7 ± 3.1◦ /s for the baseline, first, and second follow-up examinations, respectively; p < 0.01 ne-way repeated measures ANOVA). The observed longitudinal changes in postural control, as reflected by the SOT and MCT test results, were not related to subjects’ initial seasickness severity scores or the scores at the first and second follow-up evaluations. In order to investigate possible interactions between habituation to seasickness and changes in CDP parameters, we examined whether the variance in SOT and MCT results in the course of the study may be explained by the improvement in seasickness severity. For this analysis, we re-divided the study group into four categories of seasickness severity instead of the seven categories in the Wiker classification. This was dictated by the fact that very few subjects were included in Wiker groups 2 and 5, whereas the main parameters differentiating between the groups were severity of nausea and the appearance of vomiting. The modified classification included 19 subjects in group A (Wiker categories 0–2: no nausea), 17 in group B (Wiker category 3: mild nausea), 21 in group C (Wiker categories 4–6: moderate-to-severe nausea), and 17 in group D (Wiker category 7: frank vomiting). Subjects were assigned to two habituation groups according to the difference between their baseline score and final score on the modified seasickness severity scale. Subjects whose score did not change or
Table 2 Results of the sensory organization test for conditions 2, 3, 5, and the composite score in the habituation and no-habituation groups. Parameter
Habituation
Condition 2 Baseline 1st FU 2nd FU
90.2 ± 3.2* 88.3 ± 7.3* 91.3 ± 2.5*
92.6 ± 2.9 a 91.5 ± 2.7a 90.3 ± 3.4a
Condition 3 Baseline 1st FU 2nd FU
93.5 ± 4.2§ 91.7 ± 4§ 95.1 ± 2.3§
94.3 ± 2.3b 93.6 ± 2.5b 94.2 ± 2.2b
Condition 5 Baseline 1st FU 2nd FU
67.9 ± 9.7¶ 62.2 ± 16.9¶≈ 74.6 ± 6.7¶
71.4 ± 12.5c 73.3 ± 8.3≈c 76.3 ± 7.1c
Composite Baseline 1st FU 2nd FU
83 ± 6.3† 80 ± 9.7† 85.9 ± 3.6†
84.5 ± 4.8d 84.7 ± 4.4 86.6 ± 2.4d
No-habituation
d
Results are mean ± SD. Scores for test conditions 2, 3, 5 and composite score are the percentage of stability, a perfect score (100) being given for an angular sway of 0◦ . Composite = composite score of the sensory organization test. 1st FU = first follow up examination; 2nd FU = second follow-up examination. *§¶†‡ p < 0.02, ≈ p < 0.03, # abcde p < 0.04, p < 0.03.
improved by one category only were included in the no-habituation group; subjects who improved by 2 or 3 categories were included in the habituation group. There were 41 subjects (55.9%) in the no-habituation group and 33 (44.1%) in the habituation group. Time points and habituation groups were the factors used in repeated measures two-way ANOVA. The analysis showed significant differences between the habituation and no-habituation groups for the dynamics of SOT performance on the composite score, conditions 2, 3 and 5. Whereas the habituation group showed significant bimodal changes, with score decrements after 6 months of sailing followed by an increase to scores above baseline values after 12 months (p < 0.02), the no-habituation group demonstrated significant linear changes (p < 0.03, Table 2). When SOT parameters were compared between the groups, scores in the no-habituation group were higher for SOT condition 2 in the baseline evaluation (p < 0.03, one-way ANOVA), with higher scores on SOT condition 5 and a higher composite score in the first follow-up examination (p < 0.03, one-way ANOVA). The normalized maximal changes in SOT scores between baseline and follow-up evaluations were calculated for the SOT sub-tests that showed statistically significant changes. The greatest change of 18.2% was found in the habituation group for SOT condition 5. This change was also reflected in the composite score, which had a maximal change of 7.1%. For the other SOT conditions in the habituation group, and all conditions in the no-habituation group, the normalized maximal changes were not greater than 4.2%. The main finding of the present study is the significant bimodal changes in subjects’ reliance on vestibular input for postural control, which has been observed with repeated exposure to sea conditions. This result is in agreement with the hypothesis that postural strategy would be modified with repeated exposure to sea conditions. Postural dynamics were characterized by an initial decrease in the scores on SOT sub-tests 3 and 5, with a consequent reduction in the SOT composite score. This reflected increased weighting of visual and somatosensory input in the maintenance of balance while ignoring vestibular information. This change in postural strategy found in the first follow-up examination was followed by an increase to scores above baseline values for SOT subtests 3 and 5 and a higher composite score in the second follow-up examination, indicating increased reliance on vestibular cues for postural control.
D. Tal et al. / Neuroscience Letters 479 (2010) 134–137
Further analysis showed that significant bimodal changes in SOT vestibular (SOT sub-tests 3 and 5) and somatosensory (SOT sub-test 2) parameters were unique to the study subjects having the highest degree of habituation to seasickness. This observation supports the hypothesis that longitudinal changes in postural strategy are related to increased habituation to seasickness. The largest modulations took place in SOT sub-test 5. This implies that mainly vestibular, and to a lesser extent somatosensory information, is partially ignored as a strategy to attenuate the sensory conflict leading to seasickness. The significant role of vestibular input in the evolution of motion sickness is supported by reports of immunity to motion sickness in animals and humans lacking functioning vestibular end-organs [7,8], while blind persons remain vulnerable to unusual motion conditions despite the lack of visual information [4]. The vestibular system response parameters consolidated during the process of evolution are appropriate to terrestrial conditions. These parameters do not match motion conditions at sea, and thus introduce a sensory conflict leading to seasickness. Downregulation of the vestibular response, as demonstrated in the results of the present study, is a prerequisite for habituation to sea conditions. Successful habituation to seasickness is related to restoration of the reliance on both vestibular and somatosensory information. A previous study on the effects of immersion in virtual reality on postural control reported similar results. When the process of adaptation to the visual–vestibular conflict in these conditions was completed, there was an increase in the contribution of vestibular and somatosensory input to postural control while ignoring visual input [2]. In contrast to our habituation group, the no-habituation group showed inconsistent linear changes in SOT parameters. This might reflect significant efforts, albeit unsuccessful, to reach optimal sensory weighting that would reduce the sensory conflict and thus induce habituation to sea conditions. There was no significant correlation between the baseline CDP parameters or postural dynamics we found and subjects’ initial Wiker seasickness severity score or the scores at the first and second follow-up evaluations. Thus, this result does not support the hypothesis that baseline postural parameters would be correlated with future susceptibility to seasickness. These data imply that the complex, clinical spectrum of seasickness cannot be predicted by postural parameters matching conditions on land before exposure to the unusual motion characteristics at sea. Other studies [16–18] found that patterns of sway in the absence of any motion stimulation could differentiate between subjects susceptible and non-susceptible to motion sickness during imposed or virtual motion. Although we did not find a direct correlation between baseline CDP parameters and the magnitude of future seasickness severity, we did demonstrate a significant relation between such parameters and the process of habituation to sea conditions. The results at the first follow-up examination in the present study concur with those of a previous investigation, in which lower scores for SOT sub-test 5 were reported in a cohort of seasicknesssusceptible subjects [14]. In a cross-sectional study of a mixed population of sea-going subjects, it may be assumed that a significant number of the participants will not complete the process of habituation to sea conditions. A single CDP test would reflect an incomplete habituation status, similar to that of our subjects at the first follow-up examination. It has been proposed that postural instability precedes motion sickness, with postural sway occurring in reaction to vestibular or visual movement cues. It is suggested motion sickness will persist so long as individuals remain motivated to control their
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posture when presented with an unstable environment [13,16]. Correspondingly, it is suggested that when individuals refrain from attempting to control their posture and yield control to the motion environment, motion sickness will cease to exist. The significant decrease we found in the MCT response strength, which measures the angular momentum produced by the subject to counteract the platform’s movements, parallels the process of habituation to seasickness and supports this suggestion. Whereas significant longitudinal changes in the composite score and the scores on SOT sub-tests 3 and 5, as well as a significant decrease in the MCT response strength, were documented in the study group but not in the control group, follow-up examinations in both groups revealed similar significant reductions in the latency of the motor response to sudden pitch perturbations. These changes in the MCT adaptation parameters are most probably related to a learning curve phenomenon. Acknowledgements The authors wish to thank Mrs. Iris Zamir, MA for conducting the statistical analysis of the study results and Mr. Richard Lincoln for his skillful editing of the text. References [1] H. Akiduki, S. Nishiike, H. Watanabe, K. Matsuoka, T. Kubo, N. Takeda, Visual–vestibular conflict induced by virtual reality in humans, Neurosci. Lett. 340 (2003) 197–200. [2] H. Akizuki, A. Uno, K. Arai, S. Morioka, S. Ohyama, S. Nishiike, K. Tamura, N. Takeda, Effects of immersion in virtual reality on postural control, Neurosci. Lett. 379 (2005) 23–26. [3] EquiTest System, Version 4. 0: Data Interpretation Manual, NeuroCom International, Inc., Clackamas, OR, 1991, 47 pp. [4] A. Graybiel, Susceptibility to acute motion sickness in blind persons, Aerosp. Med. 41 (1970) 650–653. [5] M.J. Griffin, K.L Mills, Effect of frequency and direction of horizontal oscillation on motion sickness, Aviat. Space Environ. Med. 73 (2002) 537–543. [6] I.P. Howard, Interactions within and between the spatial senses, J. Vestib. Res. 7 (1997) 311–345. [7] M. Igarashi, Role of the vestibular end organs in experimental motion sickness: a primate model, in: G.H. Crampton (Ed.), Motion and Space Sickness, CRC Press, Inc., Boca Raton, 1990, pp. 43–48. [8] R.S. Kennedy, A. Graybiel, R.C. McDonough, F.D. Beckwith, Symptomatology under storm conditions in the North Atlantic in control subjects and in persons with bilateral labyrinthine defects, Acta Otolaryngol. 66 (1968) 533–540. [9] Z. Nachum, A. Shupak, V. Letichevsky, J. Ben David, D. Tal, A. Tamir, Y. Talmon, C.R. Gordon, M. Luntz, Mal de debarquement and posture: reduced reliance on vestibular and visual cues, Laryngoscope 114 (2004) 581–586. [10] J.F. O’Hanlon, M.E. McCauley, Motion sickness incidence as a function of the frequency and acceleration of vertical sinusoidal motion, Aerosp. Med. 45 (1974) 366–369. [11] C.M. Oman, Motion sickness: a synthesis and evaluation of the sensory conflict theory, Can. J. Physiol. Pharmacol. 68 (1990) 294–303. [12] J.T. Reason, J.J. Brand, Motion Sickness, Academic Press, London, 1975, 310 pp. [13] G.E. Riccio, T.A. Stoffregen, An ecological theory of motion sickness and postural instability, Ecol. Psychol. 3 (1991) 195–240. [14] B. Shahal, Z. Nachum, O. Spitzer, J. Ben-David, H. Duchman, L. Podoshin, A. Shupak, Computerized dynamic posturography and seasickness susceptibility, Laryngoscope 109 (1999) 1996–2000. [15] A. Shupak, C.R. Gordon, Motion sickness: advances in pathogenesis, prediction, prevention, and treatment, Aviat, Space Environ. Med. 77 (2006) 1213– 1223. [16] T.A. Stoffregen, L.J. Smart Jr., Postural instability precedes motion sickness, Brain Res. Bull. 47 (1998) 437–448. [17] T.A. Stoffregen, L.J. Hettinger, M.W. Haas, M.M. Roe, L.J. Smart, Postural instability and motion sickness in a fixed-based flight simulator, Hum. Factors 42 (2000) 458–469. [18] S.J. Villard, M.B. Flanagan, G.M. Albanese, T.A. Stoffregen, Postural instability and motion sickness in a virtual moving room, Hum. Factors 50 (2008) 332–345. [19] S.F. Wiker, R.S. Kennedy, M.E. McCauley, R.L. Pepper, Reliability, validity and application of an improved scale for assessment of motion sickness severity, Report No. CG-D-29-79, US Department of Transportation, United States Coast Guard, Office of Research and Development, Washington, DC, 1979, 33 pp.
Contents lists available at ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Postural dynamics and habituation to seasickness Dror Tal a , Ronen Bar a , Zohar Nachum a , Amnon Gil a , Avi Shupak a,b,c,∗ a
Motion Sickness and Human Performance Laboratory, The Israel Naval Medical Institute, Haifa, Israel Unit of Otoneurology, Lin Medical Center, 35 Rothschild Avenue, Haifa 35152, Israel c The Bruce Rappaport Faculty of Medicine, The Technion, Haifa, Israel b
a r t i c l e
i n f o
Article history: Received 26 March 2010 Received in revised form 3 May 2010 Accepted 13 May 2010 Keywords: Habituation Motion sickness Computerized dynamic posturography (CDP) Vestibular organs
a b s t r a c t The computerized dynamic posturography (CDP) test examines the response pattern to simultaneous, multimodal sensory stimulation. The purpose of this prospective, controlled study was to investigate whether postural dynamics evaluated by CDP are related to seasickness severity and the process of habituation to sea conditions. Subjects included 74 naval personnel assigned to service aboard ship and 29 controls designated for shore-based positions. Study participants performed a baseline CDP test, and subsequent follow-up examinations 6 and 12 months after completion of their training. On those occasions they also completed a seasickness severity questionnaire. Longitudinal changes in postural parameters were examined, as well as a possible correlation between baseline CDP results and final seasickness severity scores. The results indicated longitudinal habituation to seasickness. Reduced scores were found for sensory organization sub-tests 3 and 5 in the first follow-up examination, reflecting increased weighting of visual and somatosensory input in the maintenance of balance. Scores in the second follow-up examination were above baseline values, indicating increased reliance on vestibular cues. These significant bimodal changes were found only in study subjects having the highest degree of habituation to seasickness. A significant decrease in motor response strength was found in parallel with increased habituation to seasickness. Baseline CDP results and postural control dynamics were not correlated with subjects’ final seasickness severity score. These results suggest a potential role for CDP in monitoring the process of habituation to unusual motion conditions. © 2010 Elsevier Ireland Ltd. All rights reserved.
Motion sickness is a normal, universal physiological response to unfamiliar motion patterns, whether real or apparent [12]. The most dramatic form of motion sickness is seasickness; other forms are space sickness, airsickness, carsickness, and the recently described cybersickness, which is common in virtual environment systems that present an optical depiction of inertial motion [1]. The development of seasickness symptoms follows a sequence that varies with the intensity of the stimulus and the susceptibility of the individual. Its main signs and symptoms include epigastric awareness, perioral and facial pallor, cold sweating, salivatory changes, retching, and recurrent vomiting. Repeated exposure to the provocative stimulus results in habituation, in which decreased susceptibility to rough sea conditions may be maintained in spite of significant intervals between voyages, sometimes as much as several weeks [15]. Our current understanding views motion sickness as the result of a conflict between the information processed within a multimodal sensory system, whose function is to determine the individual’s motion relative to the environment. This has been
∗ Corresponding author at: Unit of Otoneurology, Lin Medical Center, 35 Rothschild Avenue, Haifa 35152, Israel. Tel.: +972 4 8568491; fax: +972 4 8568496. E-mail address: [email protected] (A. Shupak). 0304-3940/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2010.05.044
termed the “neural mismatch theory” [11]. A sensory conflict occurs when the integrated sensory signal is at variance with previously stored motion patterns. This results in motion sickness. The conflict is eventually settled when the anticipated relations between the sensory inputs are updated. This induces habituation to the new motion patterns, including a modified motor response [6]. Although the neural mismatch theory is the most widely accepted explanation for the development of motion sickness, there are other hypotheses which might add to our understanding of its pathogenesis. Riccio and Stoffregen [13] suggested that motion sickness is caused by instability of body postural control. This theory predicts an increased incidence of sickness when external motion is imposed at a frequency of 0.1–0.3 Hz, because this interferes with the naturally occurring sway activity. The increased sensitivity to this frequency range has been verified by field studies showing that the greatest incidence of seasickness on board conventional ships is associated with heave, surge and sway acceleration frequencies of about 0.2 Hz [5,10]. Both theories are compatible with the hypothesis that postural responses might reflect both susceptibility to motion sickness and the habituation process. A previous cross-sectional study conducted in our laboratory [14] searched for possible relations between postural control and seasickness susceptibility. The computerized dynamic posturography (CDP)
D. Tal et al. / Neuroscience Letters 479 (2010) 134–137
test was employed to evaluate the response pattern to simultaneous, multimodal sensory stimulation. The results suggested that seasickness-susceptible subjects depend more on somatosensory and visual input, and less on vestibular input, for maintenance of balance. The hypotheses underlying the present study were that postural strategy would be modified with repeated exposure to sea conditions, that these changes would reflect increased habituation to the non-terrestrial motion, and that baseline postural parameters would be correlated with future susceptibility to seasickness. Subjects were 120 male naval recruits aged 18–22 years. The study group included 90 men in basic training, who had been assigned to serve aboard naval vessels which would be making regular voyages. Their training included multiple voyages aboard small vessels in the Mediterranean, mostly in moderate sea conditions. Subjects were engaged in the various activities normally undertaken by naval crew during a voyage, and most of the time were alert and physically active. The control group consisted of 30 recruits designated for shore-based positions. A detailed history was taken from all study participants to exclude previous cochlear or vestibular pathology. Otoneurological examination included otoscopy, bedside testing for static, dynamic, positional and positioning nystagmus, and postural tests. Pure tone air and bone, speech and impedance audiometry were carried out. Exclusion criteria included past vestibular or cochlear pathology, positive findings on otoneurological examination, and hearing loss or abnormal findings in impedance audiometry. All study participants performed a baseline CDP test when recruited to the study, and subsequent follow-up examinations 6 and 12 months after completion of their training (first and second follow-up examinations, respectively). CDP was performed using the EquiTest system (NeuroCom International Inc., Clackmas, OR) according to the standard test protocol [3]. The device has a computer-controlled force platform, which is able to move abruptly in translational or pitch directions as well as in synchrony with a visual surround. The force data are collected and analyzed automatically by the system’s computer. The vertical and horizontal forces applied to the platform are measured by transducers, and the data collected are used to locate the center of foot pressure. The patient’s height and force data are used to estimate the vertical location of the body’s center of gravity and the angle of sway. The CDP procedure is divided into two parts. The sensory organization test (SOT) assesses the use of sensory information by measuring postural sway under conditions in which visual and somatosensory feedback is altered. The change in sway angle is used to move a visual surround or the support surface in synchrony with the individual’s sway. The influence of a lack of somatosensory and visual information on stability is evaluated, as is the subject’s ability to use vestibular input to maintain balance. The SOT is organized into a series of six conditions of increasing difficulty. The first three conditions are performed on a firm surface with eyes open, eyes closed, and finally with the subject’s vision sway-referenced. The final three conditions are performed with the support swayreferenced, with eyes open, eyes closed, and with the subject’s vision sway-referenced. Results of the SOT are calculated based on the maximum peak-to-peak anterior-posterior sway expressed as an equilibrium score ranging from 0 to 100, with 0 indicating loss of balance and 100 indicating perfect stability. The test conditions are described in Table 1. The second part of the CDP is the Motor Control Test (MCT). Successful mobility in the environment requires an individual to react to sudden external disturbances of balance. The MCT evaluates maintenance of balance, expressed by the motor responses to unexpected backward and forward translations and up-anddown pitch movements of the support surface. The latency of the response and the ability to minimize sway are a functional cor-
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Table 1 Sensory organization test conditions. Parameter
Condition 1 Condition 2 Condition 3 Condition 4 Condition 5 Condition 6 Composite
Description Platform
Eyes
Visual surround
Stable Stable Stable Moving Moving Moving Average of conditions 1–6
Open Closed Open Open Closed Open
Stationary Stationary Moving Stationary Stationary Moving
relate of the long loop pathways, including the peripheral nerves, ascending and descending spinal pathways, and brain structures. The adaptation protocol exposes the subject to 5 trials each of pitch perturbations towards the subject and towards the ground. Rotation causes the subject to sway by repeatedly rotating the force plate about its X-axis. This demonstrates the subject’s ability to adapt automatic movement responses to recurring surface movements. The sway induced by the platform’s translations generates angular momentum. To counteract this sway, the subject generates an active response in the opposite direction. The Response Strength parameter measured in degrees/second is the angular momentum produced by the subject’s response. The study participants did not take any medications for at least 48 h before CDP testing. None consumed drugs or alcohol. The CDP follow-up tests in the study group were conducted at least 72 h after disembarking from a voyage, and it was verified that the subject had no symptoms of mal de debarquement [9]. Susceptibility of the study group subjects to seasickness was determined by a seasickness questionnaire, which they completed after their initial exposure to sea conditions and immediately before the follow-up CDP examinations. The questionnaire, adapted from Wiker et al. [19], scores actual seasickness severity during sailing. Seasickness is rated on a scale from 0 to 7, where a score of 7 is given to the most severe grade of seasickness. All participants received a comprehensive explanation of the study’s goals and testing procedures, and gave their informed consent before they started the tests. The Israel Defense Forces Medical Corps Human Research Committee approved the study protocol and testing procedures. Longitudinal changes in seasickness severity scores and CDP parameters were studied by repeated measures one-way ANOVA. A possible correlation between baseline CDP parameters and the Wiker scores found after the initial sailing experience and the first and second follow-up evaluations were examined by the Spearman non-parametric correlation test. The extent to which the variance in SOT and MCT results in the course of the study may be explained by improvement in the Wiker scores was analyzed by repeated measures two-way ANOVA. For this analysis, subjects were assigned to two habituation groups according to the difference between their baseline and final scores on the seasickness severity scale. The factors used for the two-way ANOVA were the time points and the habituation group. Statistical analysis was performed using SPSS software (SPSS, Inc., Chicago, IL) on a personal computer. The baseline and two follow-up examinations were completed by 74 subjects (61.7%) in the study group and 29 (97%) in the control group. The dropouts in the follow-up examinations were due to the unique occupational conditions of the study population. As military personnel, some of the subjects were deployed in remote bases following their training period, and follow-up examinations were very difficult to complete. Others changed their occupation, and were not exposed to sea conditions during the whole of the study period, while still others transferred from the Navy to other
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branches of the Israel Defense Forces. Data analysis comparing the baseline and follow-up tests in the study and control groups was carried out only for subjects who completed all of the tests. After the initial exposure to open sea conditions, the Wiker score for the study group was 6 ± 1.7 (mean ± SD). There was subsequent habituation to sea conditions, as evidenced by a decrease in the sea sickness severity score to 4.77 ± 2.3 after 6 months of regular sailing and 4.11 ± 2.2 after 12 months of sea-going experience. The differences between the average baseline Wiker score and later scores were of statistical significance (p < 0.001, one-way repeated measures ANOVA). Significant dynamics in SOT parameters were found only in the study group. The composite SOT equilibrium score, representing the body’s general postural control ability, declined from a baseline value of 85 ± 4.2% (mean ± SD) to 83.9 ± 5.7% in the first follow-up evaluation, with a subsequent increase to 86.1 ± 3% in the second follow-up examination (p < 0.002, one-way repeated measures ANOVA). These dynamics reflect mainly significant changes in the scores of SOT conditions 3 and 5, which showed a similar bimodal pattern of decrement after 6 months of sailing followed by an increase to above baseline values after 12 months (94 ± 2.6%, 92.7 ± 2.9%, 94.1 ± 2.2%, and 71.4 ± 9.1%, 71.2 ± 11.5%, 75.5 ± 7% for the baseline, first, and second follow-up scores; p > 0.003 respectively; p < 0.003, one-way repeated measures ANOVA). The MCT adaptation protocol showed decreased latency of the motor response to sudden pitch perturbations in the followup examinations when compared with baseline latency values. The average latency for the motor response to sudden pitch perturbations towards the subject and towards the ground in the study group decreased from baseline values of 70.1 ± 10.2 and 49.2 ± 9.9 ms, respectively to 62.9 ± 10.7 and 46.6 ± 8.2 ms in the first follow-up examination and 59.9 ± 11.9 and 44.8 ± 7.9 ms in the second follow-up examination (p < 0.002, one-way repeated measures ANOVA). Improved adaptation scores were also found in the control group, where the average latency for the motor responses to pitch perturbations towards the subject and towards the ground decreased from baseline values of 71 ± 10.6 and 50.3 ± 10.7 ms, respectively to 65.1 ± 15.1 and 49.2 ± 9.7 ms in the first followup examination and 60.6 ± 7.7 and 46.6 ± 8.2 ms in the second follow-up examination (p < 0.001, one-way repeated measures ANOVA). The response strength, which measured the subject’s generated angular momentum counteracting the platform’s movements, decreased significantly between the baseline and follow-up tests only in the study group (9.7 ± 3.1◦ /s, 8.7 ± 3.2◦ /s, 8.7 ± 3.1◦ /s for the baseline, first, and second follow-up examinations, respectively; p < 0.01 ne-way repeated measures ANOVA). The observed longitudinal changes in postural control, as reflected by the SOT and MCT test results, were not related to subjects’ initial seasickness severity scores or the scores at the first and second follow-up evaluations. In order to investigate possible interactions between habituation to seasickness and changes in CDP parameters, we examined whether the variance in SOT and MCT results in the course of the study may be explained by the improvement in seasickness severity. For this analysis, we re-divided the study group into four categories of seasickness severity instead of the seven categories in the Wiker classification. This was dictated by the fact that very few subjects were included in Wiker groups 2 and 5, whereas the main parameters differentiating between the groups were severity of nausea and the appearance of vomiting. The modified classification included 19 subjects in group A (Wiker categories 0–2: no nausea), 17 in group B (Wiker category 3: mild nausea), 21 in group C (Wiker categories 4–6: moderate-to-severe nausea), and 17 in group D (Wiker category 7: frank vomiting). Subjects were assigned to two habituation groups according to the difference between their baseline score and final score on the modified seasickness severity scale. Subjects whose score did not change or
Table 2 Results of the sensory organization test for conditions 2, 3, 5, and the composite score in the habituation and no-habituation groups. Parameter
Habituation
Condition 2 Baseline 1st FU 2nd FU
90.2 ± 3.2* 88.3 ± 7.3* 91.3 ± 2.5*
92.6 ± 2.9 a 91.5 ± 2.7a 90.3 ± 3.4a
Condition 3 Baseline 1st FU 2nd FU
93.5 ± 4.2§ 91.7 ± 4§ 95.1 ± 2.3§
94.3 ± 2.3b 93.6 ± 2.5b 94.2 ± 2.2b
Condition 5 Baseline 1st FU 2nd FU
67.9 ± 9.7¶ 62.2 ± 16.9¶≈ 74.6 ± 6.7¶
71.4 ± 12.5c 73.3 ± 8.3≈c 76.3 ± 7.1c
Composite Baseline 1st FU 2nd FU
83 ± 6.3† 80 ± 9.7† 85.9 ± 3.6†
84.5 ± 4.8d 84.7 ± 4.4 86.6 ± 2.4d
No-habituation
d
Results are mean ± SD. Scores for test conditions 2, 3, 5 and composite score are the percentage of stability, a perfect score (100) being given for an angular sway of 0◦ . Composite = composite score of the sensory organization test. 1st FU = first follow up examination; 2nd FU = second follow-up examination. *§¶†‡ p < 0.02, ≈ p < 0.03, # abcde p < 0.04, p < 0.03.
improved by one category only were included in the no-habituation group; subjects who improved by 2 or 3 categories were included in the habituation group. There were 41 subjects (55.9%) in the no-habituation group and 33 (44.1%) in the habituation group. Time points and habituation groups were the factors used in repeated measures two-way ANOVA. The analysis showed significant differences between the habituation and no-habituation groups for the dynamics of SOT performance on the composite score, conditions 2, 3 and 5. Whereas the habituation group showed significant bimodal changes, with score decrements after 6 months of sailing followed by an increase to scores above baseline values after 12 months (p < 0.02), the no-habituation group demonstrated significant linear changes (p < 0.03, Table 2). When SOT parameters were compared between the groups, scores in the no-habituation group were higher for SOT condition 2 in the baseline evaluation (p < 0.03, one-way ANOVA), with higher scores on SOT condition 5 and a higher composite score in the first follow-up examination (p < 0.03, one-way ANOVA). The normalized maximal changes in SOT scores between baseline and follow-up evaluations were calculated for the SOT sub-tests that showed statistically significant changes. The greatest change of 18.2% was found in the habituation group for SOT condition 5. This change was also reflected in the composite score, which had a maximal change of 7.1%. For the other SOT conditions in the habituation group, and all conditions in the no-habituation group, the normalized maximal changes were not greater than 4.2%. The main finding of the present study is the significant bimodal changes in subjects’ reliance on vestibular input for postural control, which has been observed with repeated exposure to sea conditions. This result is in agreement with the hypothesis that postural strategy would be modified with repeated exposure to sea conditions. Postural dynamics were characterized by an initial decrease in the scores on SOT sub-tests 3 and 5, with a consequent reduction in the SOT composite score. This reflected increased weighting of visual and somatosensory input in the maintenance of balance while ignoring vestibular information. This change in postural strategy found in the first follow-up examination was followed by an increase to scores above baseline values for SOT subtests 3 and 5 and a higher composite score in the second follow-up examination, indicating increased reliance on vestibular cues for postural control.
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Further analysis showed that significant bimodal changes in SOT vestibular (SOT sub-tests 3 and 5) and somatosensory (SOT sub-test 2) parameters were unique to the study subjects having the highest degree of habituation to seasickness. This observation supports the hypothesis that longitudinal changes in postural strategy are related to increased habituation to seasickness. The largest modulations took place in SOT sub-test 5. This implies that mainly vestibular, and to a lesser extent somatosensory information, is partially ignored as a strategy to attenuate the sensory conflict leading to seasickness. The significant role of vestibular input in the evolution of motion sickness is supported by reports of immunity to motion sickness in animals and humans lacking functioning vestibular end-organs [7,8], while blind persons remain vulnerable to unusual motion conditions despite the lack of visual information [4]. The vestibular system response parameters consolidated during the process of evolution are appropriate to terrestrial conditions. These parameters do not match motion conditions at sea, and thus introduce a sensory conflict leading to seasickness. Downregulation of the vestibular response, as demonstrated in the results of the present study, is a prerequisite for habituation to sea conditions. Successful habituation to seasickness is related to restoration of the reliance on both vestibular and somatosensory information. A previous study on the effects of immersion in virtual reality on postural control reported similar results. When the process of adaptation to the visual–vestibular conflict in these conditions was completed, there was an increase in the contribution of vestibular and somatosensory input to postural control while ignoring visual input [2]. In contrast to our habituation group, the no-habituation group showed inconsistent linear changes in SOT parameters. This might reflect significant efforts, albeit unsuccessful, to reach optimal sensory weighting that would reduce the sensory conflict and thus induce habituation to sea conditions. There was no significant correlation between the baseline CDP parameters or postural dynamics we found and subjects’ initial Wiker seasickness severity score or the scores at the first and second follow-up evaluations. Thus, this result does not support the hypothesis that baseline postural parameters would be correlated with future susceptibility to seasickness. These data imply that the complex, clinical spectrum of seasickness cannot be predicted by postural parameters matching conditions on land before exposure to the unusual motion characteristics at sea. Other studies [16–18] found that patterns of sway in the absence of any motion stimulation could differentiate between subjects susceptible and non-susceptible to motion sickness during imposed or virtual motion. Although we did not find a direct correlation between baseline CDP parameters and the magnitude of future seasickness severity, we did demonstrate a significant relation between such parameters and the process of habituation to sea conditions. The results at the first follow-up examination in the present study concur with those of a previous investigation, in which lower scores for SOT sub-test 5 were reported in a cohort of seasicknesssusceptible subjects [14]. In a cross-sectional study of a mixed population of sea-going subjects, it may be assumed that a significant number of the participants will not complete the process of habituation to sea conditions. A single CDP test would reflect an incomplete habituation status, similar to that of our subjects at the first follow-up examination. It has been proposed that postural instability precedes motion sickness, with postural sway occurring in reaction to vestibular or visual movement cues. It is suggested motion sickness will persist so long as individuals remain motivated to control their
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posture when presented with an unstable environment [13,16]. Correspondingly, it is suggested that when individuals refrain from attempting to control their posture and yield control to the motion environment, motion sickness will cease to exist. The significant decrease we found in the MCT response strength, which measures the angular momentum produced by the subject to counteract the platform’s movements, parallels the process of habituation to seasickness and supports this suggestion. Whereas significant longitudinal changes in the composite score and the scores on SOT sub-tests 3 and 5, as well as a significant decrease in the MCT response strength, were documented in the study group but not in the control group, follow-up examinations in both groups revealed similar significant reductions in the latency of the motor response to sudden pitch perturbations. These changes in the MCT adaptation parameters are most probably related to a learning curve phenomenon. Acknowledgements The authors wish to thank Mrs. Iris Zamir, MA for conducting the statistical analysis of the study results and Mr. Richard Lincoln for his skillful editing of the text. References [1] H. Akiduki, S. Nishiike, H. Watanabe, K. Matsuoka, T. Kubo, N. Takeda, Visual–vestibular conflict induced by virtual reality in humans, Neurosci. Lett. 340 (2003) 197–200. [2] H. Akizuki, A. Uno, K. Arai, S. Morioka, S. Ohyama, S. Nishiike, K. Tamura, N. Takeda, Effects of immersion in virtual reality on postural control, Neurosci. Lett. 379 (2005) 23–26. [3] EquiTest System, Version 4. 0: Data Interpretation Manual, NeuroCom International, Inc., Clackamas, OR, 1991, 47 pp. [4] A. Graybiel, Susceptibility to acute motion sickness in blind persons, Aerosp. Med. 41 (1970) 650–653. [5] M.J. Griffin, K.L Mills, Effect of frequency and direction of horizontal oscillation on motion sickness, Aviat. Space Environ. Med. 73 (2002) 537–543. [6] I.P. Howard, Interactions within and between the spatial senses, J. Vestib. Res. 7 (1997) 311–345. [7] M. Igarashi, Role of the vestibular end organs in experimental motion sickness: a primate model, in: G.H. Crampton (Ed.), Motion and Space Sickness, CRC Press, Inc., Boca Raton, 1990, pp. 43–48. [8] R.S. Kennedy, A. Graybiel, R.C. McDonough, F.D. Beckwith, Symptomatology under storm conditions in the North Atlantic in control subjects and in persons with bilateral labyrinthine defects, Acta Otolaryngol. 66 (1968) 533–540. [9] Z. Nachum, A. Shupak, V. Letichevsky, J. Ben David, D. Tal, A. Tamir, Y. Talmon, C.R. Gordon, M. Luntz, Mal de debarquement and posture: reduced reliance on vestibular and visual cues, Laryngoscope 114 (2004) 581–586. [10] J.F. O’Hanlon, M.E. McCauley, Motion sickness incidence as a function of the frequency and acceleration of vertical sinusoidal motion, Aerosp. Med. 45 (1974) 366–369. [11] C.M. Oman, Motion sickness: a synthesis and evaluation of the sensory conflict theory, Can. J. Physiol. Pharmacol. 68 (1990) 294–303. [12] J.T. Reason, J.J. Brand, Motion Sickness, Academic Press, London, 1975, 310 pp. [13] G.E. Riccio, T.A. Stoffregen, An ecological theory of motion sickness and postural instability, Ecol. Psychol. 3 (1991) 195–240. [14] B. Shahal, Z. Nachum, O. Spitzer, J. Ben-David, H. Duchman, L. Podoshin, A. Shupak, Computerized dynamic posturography and seasickness susceptibility, Laryngoscope 109 (1999) 1996–2000. [15] A. Shupak, C.R. Gordon, Motion sickness: advances in pathogenesis, prediction, prevention, and treatment, Aviat, Space Environ. Med. 77 (2006) 1213– 1223. [16] T.A. Stoffregen, L.J. Smart Jr., Postural instability precedes motion sickness, Brain Res. Bull. 47 (1998) 437–448. [17] T.A. Stoffregen, L.J. Hettinger, M.W. Haas, M.M. Roe, L.J. Smart, Postural instability and motion sickness in a fixed-based flight simulator, Hum. Factors 42 (2000) 458–469. [18] S.J. Villard, M.B. Flanagan, G.M. Albanese, T.A. Stoffregen, Postural instability and motion sickness in a virtual moving room, Hum. Factors 50 (2008) 332–345. [19] S.F. Wiker, R.S. Kennedy, M.E. McCauley, R.L. Pepper, Reliability, validity and application of an improved scale for assessment of motion sickness severity, Report No. CG-D-29-79, US Department of Transportation, United States Coast Guard, Office of Research and Development, Washington, DC, 1979, 33 pp.