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Journal of Vestibular Research 24 (2014) 17–23 DOI 10.3233/VES-130505 IOS Press

Mal de debarquement, motion sickness and the effect of an artificial horizon Dror Tala , Guy Wienera and Avi Shupaka,b,c,∗ a

The Motion Sickness and Human Performance Laboratory, The Israel Naval Medical Institute, Haifa, Israel Unit of Otoneurology, Lin Medical Center, Haifa, Israel c The Bruce Rappaport Faculty of Medicine, The Technion, Haifa, Israel b

Received 23 February 2013 Accepted 10 October 2013

Abstract. BACKGROUND: Exposure to unfamiliar motion patterns commonly results in motion sickness and a false perception of motion, termed mal de debarquement, on the return to stable conditions. OBJECTIVE: To investigate whether motion sickness severity is correlated with the duration and severity of mal de debarquement; to study the possible preventive effect of projecting earth-referenced scenes (an artificial horizon) during exposure to motion on the development of mal de debarquement. METHODS: Thirty subjects were exposed to the recorded motion profile of a boat in a 3-degrees-of-freedom ship motion simulator. During the simulated voyage, the study participants were repeatedly put through a performance test battery and completed a motion sickness susceptibility questionnaire, while self-referenced and earth-referenced scenes were projected inside the simulator cabin. Six hours post disembarkation, subjects completed a questionnaire on mal de debarquement duration and severity. RESULTS: Mal de debarquement, mostly of mild severity, was reported following 59% of the exposures to the provocative motion profile, and in 79% of cases lasted less than 6 hours. The incidence of mal de debarquement, its duration, and the severity of symptoms did not differ between the various artificial horizon projection modes. Significant correlations were found between motion sickness severity and the duration and severity of the mal de debarquement that followed. CONCLUSIONS: The significant correlations found between motion sickness severity and mal de debarquement duration and severity imply that both syndromes might stem from a failure to adapt to new motion conditions. There is a disparity between the previously reported reduction in motion sickness symptoms by an artificial horizon, and its failure to influence the duration and symptoms of mal de debarquement. This might be explained by the different response in the two syndromes, physical versus cognitive. Keywords: Mal de debarquement, motion sickness, motion perception, prevention, questionnaires, vestibular organs

1. Introduction Mal de debarquement, or “land sickness”, first reported in 1881 [14], is a feeling of postural instability that includes sensations of swaying and rocking, ∗ Corresponding author: Avi Shupak, Unit of Otoneurology, Lin Medical Center, 35 Rothschild Avenue, 3515209 Haifa, Israel. Tel.: +972 4 8568491; Fax: +972 4 8568496; E-mail: [email protected].

which some passengers and crewmembers report when they return to land after a voyage at sea or following a long flight [6,11,23]. Our current understanding views mal de debarquement as a disorder of neuroplasticity, which occurs when habituation to passive motion patterns becomes resistant to re-adaptation on the return to stable conditions, leading to a false perception of self-motion. In the majority of cases, mal de debarquement lasts no longer than minutes or hours, and this is called the mal de debarquement syndrome (MdDS) [7–

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D. Tal et al. / Mal de debarquement, motion sickness and the effect of an artificial horizon

9,22,24]. However, there have been reports of symptoms persisting for months to years [1,3,4,11]. Persistent mal de debarquement (MdD) does not originate in vestibular dysfunction, because vestibular tests are normal and the symptoms do not respond to vestibular suppressants or physical therapy [1–5,7,11,18,20,22]. Temporary improvement in symptoms on re-exposure to passive movement supports the suggested etiology of re-adaptation failure [1,3,8,11,18]. An alternative theory for the pathogenesis of MdD is that symptoms are due to the release from the hippocampus place cells of stored vestibular information pertaining to a previously experienced intense or unusual form of motion [22]. Results of transcranial magnetic stimulation used to quantify cortical excitability were recently reported in a patient suffering from MdD and compared with data retrieved from 40 controls. The findings implied that MdD may lead to alterations in the balance of intracortical properties in the direction of hyperexcitability, or alternatively that individuals with an inherent degree of hyperexcitability may be more susceptible to the development of MdD [5]. The clinical observation that only benzodiazepines provide some relief for patients suffering from MdD [2, 11], may support the notion that lasting symptoms stem from a continuously hyperactive focus. Benzodiazepines were also found to be of benefit in the treatment of motion sickness in controlled laboratory studies, although the associated decline in cognitive performance precludes their routine use [21,26]. Although MdD is not a frequent consequence of the short-term syndrome MdDS [1,3,11,16,20,23], the associated chronic symptoms often result in significant deterioration in the patient’s quality of life and also represent an economic burden [19]. The suffering of these patients and the limited options available for efficient treatment indicate that the optimum strategy with regard to MdD is prevention. Since the lasting symptoms evolve from the usually transient postdisembarkation syndrome, the first step in the search for means of preventing MdD might be the prospective and careful documentation of data regarding the frequency, duration and severity of mal de debarquement and its relation to motion sickness severity. The objectives of the present study were to document the incidence and duration of mal de debarquement, as well as the severity of symptoms, after controlled exposure to ship motion simulation, and to look for possible correlations between motion sickness severity and the parameters of mal de debarquement. Our purpose was also to study the effect of project-

ing Earth-referenced scenes (an artificial horizon, AH) during exposure to the sickness-provoking motion on the development of mal de debarquement after returning to stable conditions. We hypothesized that the duration and severity of mal de debarquement are correlated with motion sickness severity, insofar as both syndromes might stem from a failure to adapt to new motion conditions. A second hypothesis was that the AH, which was recently found to alleviate motion sickness severity [32], might reduce the occurrence and severity of mal de debarquement. The rationale behind our second hypothesis was that abolition of the conflict between vestibular and visual input by the AH would reduce the motion-induced adaptive processes required to solve this conflict. This would decrease the need for re-adaptation, whose failure is the presumed etiology of mal de debarquement, on the return to stable conditions.

2. Subjects and methods 2.1. Subjects Male volunteers between the ages of 18 and 25 years were recruited from the student population at the University of New Orleans. The study protocol and procedures were approved by the local institutional review board. All subjects signed an informed consent form describing the purpose of the research, the subject’s role, and the effects of the motion stimulus. 2.2. The ship motion simulator (SMS) Thirty subjects were exposed to the recorded motion profile of a 1,200 ton ship under moderate sea conditions with waves 150 cm high. For that purpose, we used a 3-degrees-of-freedom ship motion simulator (SMS), which generates vertical linear motion (heave) and two angular motions (pitch and roll). The maximal sinusoidal displacements required for accurate reconstruction of the recorded ship motion were 1.5 m, 2.2◦ and 7.7◦ for the heave, pitch and roll axes, respectively. These were well within the mechanical working range of the SMS, which was 3.35 m, 15◦ and 15◦ , respectively. A digitized Fourier transform was conducted for the programmed and resulting mechanical motions of the simulator cabin, and revealed matching pitch, heave and roll components.

D. Tal et al. / Mal de debarquement, motion sickness and the effect of an artificial horizon

2.3. The artificial horizon (AH) system During the 120-min simulated voyage, self-referenced and Earth-referenced visual scenes of the selected seascape (the AH) were projected inside the closed simulator cabin. The AH system comprises three projectors, their associated screens and PC-based control software, which were used to project a moving scene inside the SMS cabin surrounding the subject’s work area. The SMS cabin was configured to hold the projection system and provide work areas for two subjects. Cable connections linked the support equipment installed in the SMS control room to the AH system inside the cabin. A number of preliminary experimental runs were conducted to evaluate the motion profile and to determine the optimal run time for provoking seasickness symptoms. Different projection configurations of pictures and scale factors were evaluated during these runs. A typical seascape was selected as the projected scene for all tests in the main study. Due to limitations imposed by the size of the SMS cabin, the projected Earth-referenced scene was scaled down to 35% (AH 35%) or 75% (AH 75%) of the full recorded movement.

3. Experimental protocol Each subject was randomly exposed to three conditions using the same motion profile: two Earthreferenced AH runs with the seascape projections scaled down to 35% and 75% of the full recorded movements, and one control run with the AH projection remaining parallel to the SMS moving cabin walls (AH 0%). The SMS motion sessions were separated by an interval of 7 days. The workstations inside the cabin consisted of a flat touch-screen monitor with keyboard secured to a desk, in front of an adjustable straight-backed chair secured to the floor of the SMS. During the study runs, subjects were seated in the straight-backed chair at the workstation, secured in the seat by a 4-point restraint lap/shoulder belt system. They were put through a PCbased performance test battery every 20 min and completed a dedicated motion sickness severity questionnaire adapted from Wiker et al. [33,34]. This rates actual seasickness severity during sailing on a scale from 0 to 7, where a score of 7 is given to the most severe grade of seasickness presenting as vomiting. The 30 subjects who participated in the study had been se-

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lected from a total of 78 volunteers, who underwent a 1-h screening run in the SMS using the motion profile to be employed in the main study. Subjects selected were those able to endure the SMS motion conditions while suffering from moderate to severe motion sickness without vomiting (Wiker scale 4–6). None had a history of any disease that could cause disequilibrium or vertigo. The effects of the Earth-referenced scenes on motion sickness severity and the associated degradation in performance have already been reported in a recently published study [32]. For the purpose of the present study, a mal de debarquement questionnaire which reviews the duration of symptoms and their severity (Appendix 1) was completed by all subjects 6 hours after each of the three SMS runs. Their responses were coded on a scale of 0–3 for symptom severity and 1–6 for duration. 3.1. Statistical analysis The main outcome measures were the severity and duration of mal de debarquement after the exposure to provocative motion. Each of the mal de debarquement symptoms detailed in Appendix 1 was graded from 0 to 3 according to the severity reported for that symptom. All grades were then summed to yield a combined severity score between 0 and 21. Mal de debarquement duration was divided into the following 6 categories: No symptoms at all = 1; immediate resolution of symptoms = 2; symptoms resolved within 15 minutes = 3; symptoms lasted more than 15 minutes but less than 2 hours = 4; symptoms continued for more than 2 but less than 6 hours = 5; symptoms persisted for more than 6 hours = 6. The number of subjects reporting mal de debarquement symptoms lasting for more than 15 minutes was compared between the AH modes using the chi-square test. One-way nonparametric repeatedmeasures ANOVA (the Friedman test) was used for the analysis of variance in mal de debarquement severity scores between the AH projection conditions. The Spearman nonparametric correlation test was used to evaluate possible correlations between motion sickness severity scores during the SMS runs and the duration and severity of mal de debarquement.

4. Results For the various AH projection modes, 15–20 (50– 67%) of the subjects reported symptoms of mal de

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D. Tal et al. / Mal de debarquement, motion sickness and the effect of an artificial horizon Table 1 Number of subjects in each mal de debarquement duration category for the various artificial horizon projection modes Duration of mal de debarquement No symptoms Immediate resolution Symptoms resolved within 15 minutes Symptoms lasted more than 15 minutes but less than 2 hours Symptoms continued for more than 2 but less than 6 hours Symptoms persisted for 6 hours after exposure to motion

AH 0% 6 6 8 6 0 4

Projection condition AH 35% 7 3 6 5 4 5

AH 75% 9 6 7 4 1 3

AH 0%: the artificial horizon projection remained parallel to the SMS cabin wall; AH 35%: the artificial horizon scaled down to 35% of the full recorded movement; AH 75%: the artificial horizon scaled down to 75% of the full recorded movement.

Fig. 1. Correlation between Wiker motion sickness severity scores and duration of mal de debarquement following exposure to motion (r = 0.4, 95% Confidence Interval 0.2–0.56, p < 0.0002).

Fig. 2. Correlation between modified Wiker motion sickness severity scores and severity of mal de debarquement following exposure to motion r = 0.37, 95% Confidence Interval 0.19–0.54, p < 0.0005).

debarquement that did not resolve immediately after exposure to the SMS motion. Of these, 8–14 subjects (27–35%) had symptoms which lasted more than 15 minutes (Table 1). The proportion of subjects having symptoms of mal de debarquement for more than 15 minutes did not differ between the AH projection modes. The mal de debarquement summed severity scores ranged from 0 to 11 out of a maximum 21. The individual symptom severity level was generally mild. Only 8 (27%) of the 30 subjects recorded symptoms at level 2 or greater, 6 of these at level 2 (moderate) and 2 at level 3 (severe). Of the 90 exposures to the SMS motion profile, symptoms of mal de debarquement were reported 53 times (59%), mostly of mild severity. Moderate severity was reported 12 times (13%), and severe symptoms on 2 occasions only (2%). The most common symptoms were rocking and swaying, reported in 20 (38%) and 18 (34%) of the 53 SMS runs which resulted in mal de debarquement. Less frequent symptoms were imbalance, a tilting sensation, nausea, vision changes and vertigo, reported 12

(23%), 11 (21%), 10 (19%), 4 (8%) and 4 (8%) times, respectively. The average summed severity scores ± standard deviation were 1.17 ± 1.9, 1.87 ± 2.52, and 2.1 ± 2.98 for the self-referenced, AH 35% and AH 75% projection conditions, respectively. These differences did not reach statistical significance. The order in which the different SMS runs were performed had no effect on the mal de debarquement severity score. The Wiker motion sickness severity scores during the SMS runs were 4.73 ± 1.44, 4.5 ± 1.7 and 4.03 ± 1.87 for the self-referenced, AH 35% and AH 75% projection modes, respectively. The decrement in the motion sickness severity score for the AH75% condition was statistically significant (p < 0.03, Friedman test). Significant correlations were found between motion sickness severity during the SMS runs, as evaluated by the Wiker score, and the duration and severity of the mal de debarquement that followed (r = 0.4, 95% Confidence Interval 0.2–0.56, p < 0.0002; and r = 0.37, 95% Confidence Interval 0.19–0.54, p < 0.0005, respectively; Figs 1, and 2).

D. Tal et al. / Mal de debarquement, motion sickness and the effect of an artificial horizon

5. Discussion In the present study, mal de debarquement was reported following 59% of the 90 exposures to the provocative motion profile. A higher incidence of 73% and 72% has previously been reported in questionnaire surveys involving 116 and 234 naval crewmembers, respectively [8,9]. These studies also confirmed that mal de debarquement is more commonly reported following extended sea voyages and heavy sea states. This might explain its higher incidence in surveys of individuals who undergo frequent long exposures to sea conditions, compared with the total of only 360 minutes it took to complete the SMS runs employed in our investigation. Our results define the nature of mal de debarquement as mainly transient; in 79% of the 53 SMS runs that resulted in mal de debarquement, symptoms lasted less than 6 hours. Previous field studies reported resolution of symptoms within 6 hours of disembarkation in higher percentages of subjects, 88% [8] and 93% [9]. This difference might be explained by the retrospective nature of these studies, in which subjects had to recall their past experience, compared with the meticulous audit conducted 6 hours after the SMS run in the present study. The results of the present investigation confirm our first hypothesis, that the duration and severity of mal de debarquement are significantly correlated with motion sickness severity. The correlations found, although of statistical significance, might underscore an even stronger association as the calculated motion sickness severity scores did not take into account potentially higher grades of sickness which were avoided by early abortion of the SMS runs on request by subjects unable to tolerate the complete motion protocol. The results corroborate previous observations on the occurrence of mal de debarquement among naval crewmembers [8,9], and confirm a report of significantly higher severity of seasickness as quantified by the Wiker scale among sailors reporting mal de debarquement lasting more than 2 hours after disembarkation [24]. It has been suggested that motion sickness arises due to conflicting information processed within a multimodal sensory system, whose function is to determine the individual’s motion relative to his or her environment. The conflict can originate within a single sensory system (e.g., canal-otolith interaction) or in the interaction between two or more sensory systems (e.g., the visual and vestibular systems). This has been termed

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the “neural mismatch theory”. A sensory conflict occurs and motion sickness results when the integrated sensory signal is at variance with previously stored motion patterns [13,25,27]. This conflict activates neural mechanisms aimed at reweighting the available sensory information, and thus reducing motion sickness (“getting one’s sea legs”). The magnitude of the sensory conflict and the severity of the provoked symptoms differ between individuals, even though they may be exposed to the same motion pattern. There is also a broad distribution of the dynamics of adaptation and re-adaptation within the population; this can range from minutes to days, and occasionally even years if MdD evolves [1,11]. The results of this study do not provide support for our second hypothesis: that the AH might reduce the duration and severity of mal de debarquement. Although the AH 75% Earth-referenced scene was found significantly to decrease motion sickness symptoms [32], the number of subjects in each mal de debarquement duration category and the average severity score did not differ between the various AH projection modes. The explanation for this apparent disparity between the effect of AH 75% on motion sickness symptoms, and its failure to affect duration or symptom scores reported in the mal de debarquement questionnaire, might be found in the different responses to the changing motion environment in the two syndromes. Whereas motion sickness encompasses the modification of vestibular and postural reflexes [15,16,28–31] in combination with autonomic system and cognitive reactions [12,17], mal de debarquement presents mainly as a phantom perception of self-motion accompanied by symptoms of visual motion intolerance, fatigue, cognitive slowing, mood changes, and constant mental strain secondary to the extra attention required for control of balance [1–3,11,22]. The motion sickness-associated modification of brainstem reflex responses and reweighting of sensory information for the maintenance of posture, do not necessarily match the development of the autonomic and cognitive reactions to motion. Previous studies have documented apathy, passivity, depression, and lack of concentration termed “the sopite syndrome”, which may be the sole manifestation of motion sickness despite a negligible presentation of overt sickness [10,35]. The AH 75% projection mode, which partially abolished the intersensory conflicts, resulted in reduced motion sickness severity. However, it might not have abolished the cognitive responses to motion, as reflected by lack of improvement in performance measures [32]. The grow-

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D. Tal et al. / Mal de debarquement, motion sickness and the effect of an artificial horizon

ing discrepancy between these two components of motion sickness might have caused further difficulty in re-adaptation on the return to stable conditions, which then presented as symptoms of mal de debarquement.

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Acknowledgement The authors wish to thank Mr. Richard Lincoln of The Israel Naval Medical Institute for his skillful editing of the text.

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2. Indicate (by X) how long it took after completion of the SMS run for your symptoms to resolve.

Appendix 1 Mal de debarquement questionnaire Subject Number: Date Time 1. Indicate (by X) the degree to which you persistently experienced the following symptoms after completing the SMS run. (Do not relate to symptoms you felt during the SMS run.) None

Slight

Moderate

Severe

Rocking Swaying Imbalance Tilting Vision changes Vertigo Nausea Coding: None = 0; Slight = 1; Moderate = 2; Severe = 3.

I did not suffer from any symptoms Immediately Within 15 minutes More than 15 minutes but within 2 hours More than 2 hours but within 6 hours The symptoms have not yet resolved Coding: I did not suffer from any symptoms = 1; Immediately = 2; Within 15 minutes = 3; More than 15 minutes but within 2 hours = 4; More than 2 hours but within 6 hours = 5; The symptoms have not yet resolved = 6.

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Mal de debarquement, motion sickness and the effect of an artificial horizon.

Exposure to unfamiliar motion patterns commonly results in motion sickness and a false perception of motion, termed mal de debarquement, on the return...
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