7 Ref 3
7 Ref 3
7 Ref 3
DOI:10.3233/VES-200005
IOS Press
f
3
roo
4 Yoon-Hee Chaa,1,∗ , John Goldingb,1 , Behrang Keshavarzc,1 , Joseph Furmand , Ji-Soo Kime ,
5 Jose A. Lopez-Escamezf,g,h , Måns Magnussoni , Bill J. Yatesj , Ben D. Lawsonk ,
Advisors: Jeffrey Staabl and Alexandre Bisdorffm,1
rP
6
7
a Department of Neurology, University of Minnesota, Minneapolis, MN, USA
8
b Psychology, School for Social Sciences, University of Westminster, London UK
9
c Toronto Rehabilitation Institute – University Health Network, Toronto, ON, Canada; Department of Psychology,
tho
11
d Department of Otolaryngology, University of Pittsburgh, Pittsburgh, PA, USA
12
e Department of Neurology Seoul National University, Seoul, Republic of Korea
13
f Department of Surgery, Division of Otolaryngology, Universidad de Granada, Granada, Spain
14
g Otology and Neurotology Group CTS495, Department of Genomic Medicine, Centre for Genomics and Oncology
19
j Department of Otolaryngology, University of Pittsburgh, Pittsburgh, PA, USA
20
k Naval Submarine Medical Research Laboratory, Naval Submarine Base New London, Groton CT, USA
d
22
21
l Department of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, USA
m Department of Neurology, Centre Hospitalier Emile Mayrisch, L-4005 Esch-sur-Alzette, Luxembourg
cte
23
24
Received 11 August 2020
Accepted 8 February 2021
25 Abstract. We present diagnostic criteria for motion sickness, visually induced motion sickness (VIMS), motion sickness
rre
26 disorder (MSD), and VIMS disorder (VIMSD) to be included in the International Classification of Vestibular Disorders.
27 Motion sickness and VIMS are normal physiological responses that can be elicited in almost all people, but susceptibility
28 and severity can be high enough for the response to be considered a disorder in some cases. This report provides guidelines
29 for evaluating signs and symptoms caused by physical motion or visual motion and for diagnosing an individual as having a
30 response that is severe enough to constitute a disorder.
co
31 The diagnostic criteria for motion sickness and VIMS include adverse reactions elicited during exposure to physical motion
32 or visual motion leading to observable signs or symptoms of greater than minimal severity in the following domains: nausea
33 and/or gastrointestinal disturbance, thermoregulatory disruption, alterations in arousal, dizziness and/or vertigo, headache
34 and/or ocular strain. These signs/symptoms occur during the motion exposure, build as the exposure is prolonged, and
Un
35 eventually stop after the motion ends. Motion sickness disorder and VIMSD are diagnosed when recurrent episodes of
1 Except for the first three authors and the last author, all authors
36 motion sickness or VIMS are reliably triggered by the same or similar stimuli, severity does not significantly decrease after
37 repeated exposure, and signs/symptoms lead to activity modification, avoidance behavior, or aversive emotional responses.
38
Motion sickness/MSD and VIMS/VIMSD can occur separately or together. Severity of symptoms in reaction to physical
39
motion or visual motion stimuli varies widely and can change within an individual due to aging, adaptation, and comorbid
40
disorders. We discuss the main methods for measuring motion sickness symptoms, the situations conducive to motion sickness
41
and VIMS, and the individual traits associated with increased susceptibility. These additional considerations will improve
42
diagnosis by fostering accurate measurement and understanding of the situational and personal factors associated with MSD
43
and VIMSD.
f
roo
36 1. Introduction dramatically in the early 20th century due to the 76
37 The Classification Committee of the Bárány So- ported by sea, air, and land. The initiation of space 78
38 ciety was charged with establishing standardized travel in the 1960s further spurred interest in motion 79
39 international clinical diagnostic criteria for motion si- sickness research, fostering some of the assessment 80
rP
40 ckness and visually induced motion sickness (VIMS) tools and countermeasures that are used today [6]. 81
41 and when these conditions constitute disorders. These Motion sickness that is mainly caused by stimu- 82
42 criteria were developed by an international group of lation of the visual system, often in the absence of 83
43 vestibular specialists, scientists, and therapists for the physical motion, has received increased recognition 84
Bárány Society in order to promote a common refer- recently [7, 8]. Symptoms of VIMS were reported as
tho
44 85
45 ence frame across disciplines involved in the care of early as the 19th century in the haunted swing amuse- 86
46 the general public and of individuals with high sus- ment ride and documented during adaptation to visual 87
47 ceptibility to motion sickness and VIMS. Though a rearrangement and subsequent readaptation to nor- 88
48 common phenomenon, sickness induced by physical mal vision [9–11]. These early reports noted symp- 89
Au
49 motion of the person or visual motion can adversely toms such as dizziness, nausea, and vertigo, each of 90
50 affect otherwise healthy individuals and decrease which is still featured today in the most widely-used 91
51 safety in situations that require high levels of concen- simulator sickness state questionnaire [12]. Modern 92
52 tration. The establishment of these criteria recognizes scientific studies of VIMS were first documented in 93
53 that motion sickness and VIMS, while being normal the 1950s in the laboratory and the military domains 94
physiologic responses, can have profound negative when optokinetic stimuli and flight simulators were
d
54 95
55 effects when symptoms are severe, and can some- found to cause motion sickness-like symptoms (nau- 96
times be considered a motion sickness disorder sea, dizziness, vertigo/disorientation, blurred vision,
cte
56 97
57 (MSD) or visually induced motion sickness disorder headache, and drowsiness) [13–17]. Due to recent 98
63 texts mention symptoms of seasickness such as nau- Motion sickness and VIMS are polysymptomatic 104
64 sea, vomiting, faintness, difficulty concentrating, and syndromes driven by the interaction between a spe- 105
65 lack of initiative which are still considered valid today cific stimulus and individual susceptibility. While 106
66 [1]. Theories to explain such reactions to motion there is no single, universally accepted theory of 107
Un
67 evolved over the centuries from pre-scientific ideas to motion sickness or VIMS, several hypotheses exist 108
68 later explanations concerning the effects of inner ear concerning the evolutionary origins and immediate 109
69 overstimulation or disrupted multisensory integration etiology of motion sickness and VIMS [6, 7, 17–21]. 110
70 [1–3]. It has long been known that the vestibular The sensory conflict/neural mismatch hypothesis 111
71 organs are implicated in seasickness [4] and that peo- of motion sickness is the most cited explanation. 112
72 ple without vestibular function are not susceptible to It posits that motion sickness is caused by a con- 113
73 motion sickness, even during highly sickening sea flict between expected versus actual interactions 114
74 conditions [5]. Modern interest in the mechanisms, among visual, vestibular, and somatosensory inputs 115
75 treatment, and prevention of motion sickness grew [6, 18]. This conflict can be due to dissonance among 116
Y.-H. Cha et al. / Motion sickness diagnostic criteria 3
117 different sensory modalities, intra-vestibular mis- nausea and vomiting without conferring any func- 169
118 match between canal and otolith inputs, mismatch tional benefit to the individual [27, 28]. 170
f
125 autonomic pathways by physical or apparent motion Members of the Classification Committee of the 173
roo
126 to which the human nervous system is unable to or Bárány Society (CCBS) met in Berlin, Germany in 174
127 has not had sufficient time to adapt [23, 24]. These March 2017 and proposed the creation of a subcom- 175
128 theories predict that motion sickness will diminish mittee to develop criteria for motion sickness for 176
129 with repeated exposure if the challenging motions the International Classification of Vestibular Disor- 177
130 are sufficiently within one’s adaptive capacity and the ders (ICVD). They selected a Chairperson (YHC) 178
rP
131 internal model of expected sensory input recalibrates. to choose subcommittee members who represented a 179
132 The toxin hypothesis of motion sickness is a vari- broad range of subspeciality expertise and who came 180
133 ant of the sensory conflict theory which attempts to from three different continents. Subcommittee com- 181
134 explain the evolutionary origins of the characteristic munication occurred through email and subsequent 182
tho
135 symptoms of motion sickness (e.g., nausea, vomit- meetings. The CCBS met again to discuss its progress 183
136 ing) rather than the immediate cause of the motion before the 30th Bárány Society meeting in Uppsala, 184
137 sickness reaction during a given stimulus [25]. This Sweden in June 2018, and in Berlin, Germany in 185
138 hypothesis postulates that motion-induced vomiting November 2019. Diagnostic criteria were developed 186
139 is an accidental, modern (transportation-related) by- through discussions among subcommittee members. 187
Au
140 product of an ancient evolutionarily protective respo- Draft criteria were presented to the CCBS in Novem- 188
141 nse to the neural effects of various toxins which are ber 2019 and then modified based on comments. A 189
142 often associated with distortions of sensory input. revised draft was made available for comment by the 190
143 Thus, sensory integration disturbances and neural eff- Bárány Society membership in January 2020. Fur- 191
144 ects are produced by modern motion which are simi- ther comments and concerns were addressed before 192
145 193
147 even intoxicants such as fermented fruit) [17]. A sha- 2.2. Selection of symptoms for criteria 194
150 vation that individuals with high motion sickness sus- derived from a large body of studies that have cat- 196
151 ceptibility are more likely to suffer from nausea and egorized motion sickness symptoms and have con- 197
rre
152 vomiting from other causes, such as chemotherapy tributed to the development of well-validated motion 198
153 and actual toxins [26]. However, many tenets of the sickness metrics. The categorization of the symptoms 199
154 toxin hypothesis have been questioned and modified. of motion sickness and VIMS was initially driven 200
155 The direct evolutionary hypothesis posits that an- by military and space exploration needs to include 201
co
156 cient physical or apparent motions existed that could pre-vomiting symptoms. Vomiting, while objective, 202
157 have contributed directly to the evolution of aversive is usually a late sign of motion sickness and is 203
158 reactions, without the need for accidental co-opting impractical for assessing escalating severity of mot- 204
159 of a poison response via the neural effects of modern ion sickness and VIMS. The identification of ear- 205
Un
160 transportation [17]. Nevertheless, the direct poison- lier symptoms broadened the spectrum of severity 206
161 ing hypothesis posits that the body’s poison response of motion sickness and led to recognition of when 207
162 system shaped some of the signature motion sickness interventions were needed to stop the progression of 208
163 symptoms that emerged during the direct evolution of sickness. By the 1940s, some of the most common 209
164 aversive reaction to certain ancient motions. symptoms beyond obvious vomiting or retching were 210
165 Finally, the possibility has been raised that motion agreed upon by multiple authors (e.g., cold sweating, 211
166 sickness is simply an unfortunate structural conse- pallor), leading to a full diagnostic checklist contain- 212
167 quence of the proximity of anatomical pathways that ing multiple motion sickness symptoms developed by 213
168 mediate vestibular signals with those that mediate the 1960s [29–31]. 214
4 Y.-H. Cha et al. / Motion sickness diagnostic criteria
215 The three most influential multi-symptom motion urge to vomit, retching, actual vomiting, epigastric/ 262
216 sickness state questionnaires include: 1) the Sim- stomach discomfort/awareness, change in salivation 263
217 ulator Sickness Questionnaire/Motion Sickness and/or appetite, burping, and a desire to move bowels. 264
218 Questionnaire (SSQ/MSQ) [12], 2) the Pensacola Thermoregulatory disruption can include sweating/ 265
219 Diagnostic Index (PDI) (most-cited in [32], and fully cold sweating, clamminess, flushing, warmth, and 266
220 matured in [31]), and 3) the Motion Sickness Assess- pallor. Alterations in arousal can include drowsiness, 267
221 ment Questionnaire (MSAQ) [33]. The complete 28- fatigue, tiredness, and difficulty concentrating. Dizzi- 268
222 item MSQ and the 16-items focused on simulator ness and/or vertigo can include these symptoms as 269
f
223 sickness that make up the SSQ portion have been well as disorientation, faintness, and visual motion 270
roo
224 cited more than any other motion sickness state que- illusions. Headache and/or ocular strain can include 271
225 stionnaires and are relevant to the development of head pain, head fullness, eyestrain, difficulty focus- 272
226 other motion sickness scales (e.g. MSAQ[33], Mis- ing, and blurred vision. Blurred vision can also occur 273
227 ery Scale [34]). In order to form a more manageable in the context of vertigo. The presence of a greater 274
228 and easily remembered set of criteria, however, the number of signs and/or symptoms allows greater 275
rP
229 major items of the MSQ/SSQ and the PDI have specificity that symptoms are due to motion sickness. 276
tho
233 duced the motion sickness/VIMS criteria below and ger motion sickness. While highly susceptible 279
234 detailed in Tables 1–3. people tend to be susceptible to multiple motion 280
235 3. Diagnostic criteria bility to others for an entire group of people. 283
Au
Examples of sickening motion stimuli include: 284
236 3.1. Motion sickness and visually induced a. Water transportation, e.g., ships, boats, ra- 285
diving 287
238 Motion sickness is diagnosed when the sickness b. Air transportation, e.g., airplanes, helico- 288
inducing stimulus is physical motion of the person; pters, hang-gliding, parasailing, skydiving,
d
239 289
240 visually induced motion sickness (VIMS) is diag- parabolic flight 290
cte
241 nosed when the stimulus is visual motion. An acute c. Land transportation, e.g., cars, trains, truc- 291
242 episode of motion sickness/VIMS is sickness induced ks, buses, off-road vehicles (including arm- 292
243 by physical motion/visual motion that meets Criteria ored vehicles), self-driving cars, and some 293
camels) 295
A. Physical motion of the person1 or visual mo-
rre
245
d. Amusement devices, e.g., amusement park 296
246 tion2 elicits sign(s) and/or symptom(s) in at
rides, playground motion devices, certain 297
247 least one of the following categories, experie-
swings or hammocks 298
248 nced at greater-than-minimal severity:
e. Swaying buildings, e.g., low frequency 299
249 1. Nausea and/or gastrointestinal disturbance3
co
253
vertical axis rotation (OVAR), horizontal 304
254 B. Sign(s)/Symptom(s) appear during motion and
or vertical low frequency linear oscillation, 305
255 build as exposure is prolonged8
and certain stimuli aboard human centri- 306
256 C. Sign(s)/Symptom(s) eventually stop after ces-
fuges 307
257 sation of motion9
g. Space travel, e.g., upon entering orbit or 308
258 D. Sign(s)/Symptom(s) are not better accounted
first returning to Earth 309
259 for by another disease or disorder10
2. Visual stimulation may be presented via vir- 310
260 COMMENTS:Nausea and/or gastrointestinal dis- tual/augmented reality devices, simulators, 311
261 turbance can include a feeling of sickness with an movies, computer monitors, dynamic video 312
Y.-H. Cha et al. / Motion sickness diagnostic criteria 5
313 games, or optokinetic drums. Even certain weighed heavily by clinicians but failing to 365
314 small mobile displays can be disturbing under recollect the presence of pallor is inconclusive. 366
315 certain conditions (e.g., display parallax whe- 5. Symptoms such as fatigue, drowsiness, or diff- 367
316 rein foreground and background move) or iculty concentrating are part of the full list of 28 368
317 when viewed while walking or riding in a vehi- SSQ/MSQ symptoms and are considered to be 369
318 cle. When visually-triggered motion sickness suggestive of the ‘sopite’ syndrome [39]. Sev- 370
319 also includes physical motion, e.g., motion- eral other symptoms related to poor mood or 371
320 based flight simulators, driving simulators, or reduced motivation have been inferred to be 372
f
321 ship simulators, the contributions of both forms sopite-related during prolonged motion tests 373
roo
322 of stimuli should be noted. [39], and symptoms such as fuzzy/foggy- 374
323 3. Many of these symptoms and others in the cri- headed, lazy/unmotivated, and relaxed have 375
324 teria have been formally defined [12, 17]. been endorsed by research participants recol- 376
325 Stomach awareness and discomfort are com- lecting situations involving mild motion [17, 377
326 mon early gastric manifestations of motion 40]. Fatigue due to motion sickness should be 378
rP
327 sickness. The unpleasant sensations can incl- distinguishable from sleep deprivation, phys- 379
328 ude the esophageal or epigastric areas. Nausea ical exhaustion, or other disorders causing 380
330 of vomiting is generally related to the severity 6. When due to motion sickness, these symptoms 382
tho
331 of nausea, vomiting may rarely occur at low should not be solely attributable to vestibu- 383
332 or negligible levels of nausea without much lar disorders, changes in atmospheric pressure, 384
333 warning in some situations, or in very suscep- postural hypotension, or visual cliffs [41]. Fee- 385
334 tible people [35]. Prolonged mild or moderate lings of vertigo or spinning can also be elicited 386
335 nausea can occasionally lead to an ‘avalanche’ without motion sickness during piloting an air- 387
Au
336 phenomenon in which symptoms rapidly esca- craft without good visual references or exp- 388
337 late to vomiting [36]. If vomiting occurs du- eriencing a visually induced illusion of self- 389
338 ring a severe stimulus, it generally happens motion. When an episode of vertigo leads to 390
339 within 60-minutes of the onset of other symp- overlapping symptoms with motion sickness, 391
340 toms, such as moderate or severe nausea [23, these symptoms are considered sequelae of the 392
37]. Vomiting is not as common with VIMS vertigo spell and not a separate motion sick-
d
341 393
342 as with physical motion, partially because ness syndrome. However, clinicians should be 394
cte
343 affected individuals can close their eyes before aware of differences between the ICVD and 395
344 symptoms become severe. Nausea and related the motion sickness literature, the latter of wh- 396
345 symptoms should be distinguishable by the ich established its symptom definitions prior to 397
346 clinician from primary gastric disorders and the ICVD. The ICVD defines dizziness as dis- 398
348 4. When due to motion sickness, sweating is gen- of motion [42], whereas in motion sickness 400
349 erally a ‘cold’ sweat that can accompany other research, dizziness is not always defined or has 401
350 autonomic signs and symptoms. The sweating a definition that does not exclude illusions of 402
351 is ‘cold’ because it occurs in the absence of a self-motion. Similarly, the ICVD defines ver- 403
co
352 rise in ambient temperature, not because it is tigo as, “a sensation of self-motion when no 404
353 always experienced as cold clamminess. In self-motion is occurring or the sensation of dis- 405
354 fact, it is often preceded by a sudden warm sen- torted self-motion during an otherwise normal 406
355 sation in the face, neck, and/or upper chest. head movement,” [42] whereas in motion sic- 407
Un
356 Sweating due to motion sickness in a warm kness research, vertigo usually means a loss of 408
357 environment should be distinguishable from orientation with respect to the vertical upright 409
358 ambient thermal causes (e.g., by suddenness [12]. The ICVD definition of internal vertigo 410
359 of onset). Pallor is almost always present in does not explicitly distinguish among illusions 411
360 some combination prior to vomiting [38]. How- of angular motion, linear motion, or tilt. App- 412
361 ever, an individual’s recollection concerning lying the ICVD definition of vertigo to the mot- 413
362 pallor depends upon others to mention it for ion sickness literature, vertigo certainly can be 414
363 the individual to observe it (e.g., in a mirror). induced by motion stimuli which elicit motion 415
364 Therefore, a recollection of pallor should be sickness. The most widely used laboratory 416
6 Y.-H. Cha et al. / Motion sickness diagnostic criteria
417 protocol for the controlled elicitation of se- should be distinguishable from visual overwork 469
418 vere motion sickness (Coriolis cross-coupling or ocular/visual disorders. Blurred vision may 470
419 during constant velocity rotation in the dark) also accompany vertigo, and not always imply 471
420 repeatedly elicits a temporary illusion of dis- ocular dysfunction, however. 472
421 torted self-tilt displacement (and an even gre- 8. Symptoms that start immediately with move- 473
422 ater illusion of self-velocity) during otherwise ment or are maximal at the onset of motion 474
423 normal head movements. Similarly, illusions should raise suspicion for a possible disorder 475
424 of velocity and displacement can be caused (vestibular for physical motion, ocular or vis- 476
f
425 by high-speed turns, low-frequency horizontal ual-vestibular for visual motion), an anxiety 477
roo
426 linear oscillation, viewing large optokinetic reaction, or an aversively conditioned response 478
427 fields, decelerating after non-pendular centri- wherein past motion sickness has led to classi- 479
428 fugation, various flight illusions (e.g., leans, cal conditioning to the sight and smell of the 480
429 somatogravic, G-excess), and terrestrial rea- situation. Strong stimuli in very susceptible 481
430 daptation following spaceflight, most of which individuals may induce symptoms with very lit- 482
rP
431 can cause motion sickness [41, 43]. For these tle temporal delay. Continued exposure within 483
432 reasons, it is best for clinicians not to assume the individual’s adaptive capacity may also lead 484
433 that a report of frank vertigo is evidence against to habituation and eventual reduction of sick- 485
tho
435 without vestibular pathology. 9. Although some symptoms of motion sickness 487
436 Visually induced dizziness (VID) is recognized or VIMS may persist after termination of the 488
437 as a sense of spatial disorientation caused by stimulus, the onset of sickness symptoms must 489
438 moving or visually complex stimuli and is time- occur during the motion stimulus and not begin 490
439 locked to the stimulus, ie. the onset is imm- exclusively after the stimulus has ended. This 491
Au
440 ediate with the onset of the visual stimulus. distinguishes motion sickness from mal de 492
441 Dizziness in VIMS is phenomenologically débarquement syndrome, which only begins 493
442 indistinguishable from VID, but the onset will once the motion has ended and lasts for at least 494
443 often be delayed and build in intensity with 48-hours [46]. 495
444 continued exposure. While whole-field motion 10. Motion sickness and VIMS may co-occur and 496
is known to readily elicit an illusion of self- symptom severity may be exacerbated by the
d
445 497
446 motion (called vection), this illusion is neither presence of ocular motility disorders, visual- 498
cte
447 necessary nor sufficient for VIMS to occur [17]. vestibular disorders, or vestibular disorders 499
448 Nevertheless, a large field moving in the roll such as vestibular migraine, vestibular neuri- 500
449 (x-axis) of the head can cause a compelling sen- tis, or persistent postural perceptual dizziness. 501
450 sation of self-motion consistent with vection In these situations, both a diagnosis of motion 502
509
460 be more common and occur more frequently (VIMSD) is diagnosed when the stimulus is visual 510
461 without nausea in VIMS than in motion sick- motion. MSD or VIMSD is diagnosed when Criteria 511
462 ness caused by physical motion. A secondary A through E are met: 512
463 symptom, head fullness, is relevant as well,
464 since it is a similar symptom that has emerged A. At least five episodes of motion sickness/VIMS 513
465 frequently in simulator or cybersickness stud- triggered by the same or similar motion 514
467 and visual blurring are particularly common sy- B. Sign(s)/Symptom(s) are reliably triggered by 516
468 mptoms of VIMS [7, 8]. Eye/visual symptoms the same or similar motion stimuli4 517
Y.-H. Cha et al. / Motion sickness diagnostic criteria 7
518 C. Sign(s)/Symptom(s) severity does (do) not sig- susceptibility, aversive conditioning, and the 568
519 nificantly decrease after repeated exposure to individual’s ability to adapt. The repeated trig- 569
520 the same or similar motion stimuli5 gering of sickness to the same stimulus signifies 570
521 D. Sign(s)/Symptom(s) lead to one or more of the an inability to habituate and is a core feature 571
522 following behavioral or emotional responses6 of MSD and VIMSD. An exception is made 572
523 a. Activity modification to abort sickness for stimuli that are extremely severe and infre- 573
525 b. Avoidance of the motion stimulus that trig- very rough sea conditions. 575
f
526 gers sickness 6. The usual behavioral response to motion sick- 576
roo
527 c. Aversive anticipatory emotions prior to ness or VIMS is to avoid the sickness-inducing 577
528 exposure to the motion stimulus motion stimulus or to shorten the duration of 578
529 E. Sign(s)/Symptom(s) are not better accounted exposure, when possible. When neither is pos- 579
530 for by another disease or disorder7 sible, negative anticipatory emotions or con- 580
rP
531
nausea) may occur prior to exposure to the 582
533 to four episodes have occurred. 7. An individual may be diagnosed with MSD, 584
534 2. On a population level and in the absence of cer- VIMSD, or both. 585
tho
535 tain disorders that impact vestibular function
536 (see Section 4.5) motion sickness susceptibility 3.3. Motion sickness susceptibility and severity 586
539 symptoms refer to the ≤ 12-year range or the last century has led to the development of a number of 588
Au
540 > 12-year range will help in accurate commu- severity and susceptibility scales. Several scales used 589
541 nication of current status and in determination for research purposes are presented, with common 590
542 of prognostic variables. Based on a simplified elements listed to show the overlap in queried symp- 591
543 scoring system of the MSSQ, the Pearson cor- toms (per Criteria 3.1 A) (Table 1 for multi-symptom 592
544 relation between recollected childhood (Part A) checklists of severity state [12, 31–33] [40], Table 2 593
and adult motion sickness susceptibility (Part for single-answer severity state questionnaires [49,
d
545 594
546 B) is r = 0.65 [47, 48]. 50] [51–53] and Table 3 for retrospective scales for 595
cte
548 3. Susceptibility to motion sickness or VIMS from used based on its specific advantages to the research 598
549 one type of stimulus may not predict reactions question or clinical application, e.g. the Motion Sick- 599
550 to other types of stimuli. Therefore, motion ness Susceptibility Questionnaire (MSSQ-Short) 600
rre
551 sickness and VIMS to each motion stimulus form to retrospectively estimate general motion sick- 601
552 (e.g., airplanes, automobiles, boats, virtual real- ness trait susceptibility [48], the first 16 items of the 602
553 ity systems, simulators) should be considered Simulator Susceptibility Questionnaire (SSQ) for 603
554 separately (see Notes 1&2, Section 3.1) estimating state VIMS, and the full list of 28 SSQ/ 604
co
555 4. The induction of motion sickness and VIMS can MSQ symptoms for estimating state motion sickness 605
557 tion, e.g., the individual may only feel sick on While motion sickness can be induced in nearly 607
558 small boats but not large ships, smaller propel- all people with a sufficiently strong stimulus, there 608
Un
559 lor aircraft but not large jetliners, etc. Similarly, are individuals at the extremes of the population dis- 609
560 the induction of VIMS may be specific to a tribution of susceptibility. The distribution curve of 610
561 particular head-mounted virtual reality display, recollections of past susceptibility is linear up to 611
562 simulator, or viewing screen. about the 75Th percentile of susceptibility and flattens 612
563 5. Susceptibility to motion sickness and VIMS out on the high end of scores, e.g., on the MSSQ-Short 613
564 usually declines with repeated exposures, with form, out of a total possible score of 54, a score of 614
565 the rate of adaptation being dependent upon 11 = 50th percentile, 19 = 75th percentile, 27 = 90th 615
566 many factors including the strength or pred- percentile, and 31 = 95th percentile, indicating that 616
567 ictability of the initial stimulus, inherent only a small proportion of people are severely 617
8
Table 1
Multi-Symptom Checklist Motion Sickness Severity Questionnaires
MAIN MULTISYMPTOM CHECKLISTS
Known as Pensacola Diagnostic Index/Pensacola Simulator Sickness Questionnaire/ Motion Sickness Assessment
Diagnostic Criteria/Modified Pensacola Motion Sickness Questionnaire [12] Questionnaire [33]
Diagnostic Criteria [31, 32, 40]
Shorthand PDI/PDC/MPDC SSQ/MSQ MSAQ
Year 1968/1970/2014 1993 2001
Main Stimuli Initially validated during: rotation room (free SSQ: initially validated in stationary
Un
Studied movement, Dial Test, automated Coriolis and moving flight simulators
cross-coupling), Active/voluntary
Coriolis cross-coupling
rre
virtual reality, etc. parabolic flight, virtual reality, etc.
Severity Level for Most symptoms originally scored none- None-slight-moderate-severe 1–9 (1 = not at all, 9 = severely)
Each Symptom minimal-minor-major.
cte
Multisymptom No formal subfactors, but the following Oculomotor (O) Gastrointestinal (G)
Cluster Names symptoms are grouped as one severity Disorientation (D) Central (C)
continuum in original PDI: epigastric Nausea (N) Peripheral (P)
awareness/discomfort, minimal, moderate,
Symptoms Queried
Nausea,
Gastrointestinal
major nausea, vomiting/retching
Nausea
d Below are 16 SSQ symptoms + 12
Au
more comprising the full SSQ/MSQ
Nausea (N,D) Nausea (G)
Queasy (G)
Distburbance Vomiting/Retching
rP
(assessed separately but neither counted as discomfort short of nausea)
towards severity score in original PDI) Decreased/Increased appetite (two items on
full MSQ)
roo
Burping (N)
Desite to move bowels (on full MSQ)
Increased Salivation Increased salivation (N)
Decreased salivation (on full MSQ)
f
Thermoregulatory Cold sweating Sweating (N) Sweaty (P)
Disruption Clammy/Cold sweat (P)
Flushing/warmth Hot/warm (P)
Pallor
(Continued)
Y.-H. Cha et al. / Motion sickness diagnostic criteria 9
f
Tired/fatigued (S)
Lightheaded (C)
626
roo
of normal susceptibility is not a strong predictor of
Spinning (C)
Faintlike (C)
627
Drowsy (S)
Dizzy (C)
rP
lar motor issues (e.g., eyestrain, blurred vision) and 632
tho
adults [7, 17, 57].
Visual illusions of movement (when not in
636
Au
Boredom (on full MSQ)
644
Fatigue (O)
646
653
Headache/
in Arousal
Dizziness/
Ocular
Un 2 = mild symptoms∗
3 = mild nausea
4 = mild to moderate nausea
2 = vague∗∗
3 = slight∗∗
4 = fairly∗∗
rre
other unspecified symptoms 8 = severe nausea
9 = retching
10 = vomiting
cte
∗∗
Individual Symptoms Dizziness, warmth, headache, No individual symptoms tracked,
Implicitly Contributing stomach awareness, sweating, but subjects instructed to focus on
to Overall Score other unspecified symptoms nausea, stomach problems,
d
and general discomfort
While ignoring other symptoms
(e.g., fatigue, dizziness, oculomotor)
Nausea,
Gastrointestinal
Distburbance
Nausea
Au Nausea
Retching
Vomiting
(Nausea)
tho
Salivation (Frank sickness)
(Stomach problems)
Stomach awareness Stomach awareness
Burping
Thermoregulatory
Disruption
Alterations rP Sweating
Warm
roo
in Arousal Tiredness
Yawning
Dizziness/Vertigo Dizziness
Headache/Ocular
Other
∗ NOTE:
Headache
Blurred vision
Uneasiness
f
General discomfort
Golding & Kerguelen used a 1–7 scale, Griffin et al. used a 0–6 scale.
Y.-H. Cha et al. / Motion sickness diagnostic criteria 11
Table 3
Retrospective Motion Sickness Trait Susceptibility Scales
Known as Pensacola Motion History Motion Sickness
Questionnaire [54] Susceptibility Questionnaire
(Long/Short)[47, 48]
Shorthand MHQ MSSQ; MSSQ-S;
(54 items; later shortened to 18)
Year 1990 1998/2006
Motion type queried Physical motion Physical motion
f
Components Part A Child (<12yrs)
roo
Part B Adult (last 10 yrs)
Queries incidence of 12 symptoms in 14 situations. Queries episodes of feeling sick or
The 12 symptoms include: vomiting, nausea, nauseated during each of 9 situations
stomach awareness, increased salivation, (Long version also queries
dizziness, drowsiness, sweating, pallor, vertigo, amount of exposure)
awareness of breathing, headache, or other.
rP
668 fulfilling obligations to family, employers, or social 25% in young adults; it is a frequent problem in 14% 702
669 contacts can have physical and mental health con- of adults younger than 30 years old and 7% of adults 703
670 sequences. Even in otherwise healthy individuals, 61 years old or older [72–74]. The prevalence of 704
671 motion sickness can reduce work or school produc- VIMS ranges widely depending on the stimulus type 705
tho
672 tivity and decrease social engagement through direct and the visual content, with rates varying from 1% 706
673 effects from being ill, avoidance of sickness-inducing [75] to 60% [76] to 80–95% [77, 78]. 707
678 dehydration or aspiration [39, 68]. Susceptibility to motion sickness changes with 710
679 Formal disability scales can be paired with existing age. Infants are resistant to motion sickness until 711
680 motion sickness or VIMS scales to quantify disabil- about age 2, at which point motion sickness sus- 712
681 ity due to MSD or VIMSD. As an example, the ceptibility rises between the ages of 7–12 years and 713
683 family, or social function on a 10-point scale along 72, 79]. Susceptibility gradually continues to decline 715
685 due to symptoms [69]. Alternatively, a basic impact of individuals [27]. An increase in susceptibility to 717
686 assessment that queries whether work, social, fam- VIMS as a factor of age has been well-documented, 718
687 ily, or travel difficulties are experienced (Yes or No) with older adults reporting more VIMS than younger 719
688 due to symptoms can be used as a quick assessment, adults [55, 80, 81]. Prevalence estimates should con- 720
rre
689 e.g., the Social Work Impact of Dizziness short form sider that people might self-restrict their behavior and 721
690 adapted for motion sickness [70, 71]. avoid situations that provoke motion sickness if they 722
691 Even if motion sickness or VIMS does not cre- are aware of their elevated susceptibility. 723
693 entity that deserves medical attention. In most cases 4.2.2. Sex 724
694 , education, exposure minimization, avoidance of The evidence of sex differences in motion sickness 725
695 exacerbating behaviors, short-term use of anti-motion is mixed. Only 50% of the studies in the litera- 726
696 sickness medications, or simple habituation exercises ture have found women to be significantly more 727
Un
697 beforehand may be employed to reduce morbidity. susceptible to motion sickness [17], with estimates 728
698 4. Motion sickness clinical features [47, 74, 82–86]. Sex differences in motion sickness 731
699 4.1. Prevalence controlled laboratory studies and more commonly 733
700 The prevalence of motion sickness in childhood authors positing a sex difference, the estimated effect 735
701 has been estimated at 35–43% prior to puberty and of sex is only about one-third that of age [87, 88]. 736
12 Y.-H. Cha et al. / Motion sickness diagnostic criteria
737 Secondary hormonal factors such as the use of oral UBE2E2, CBLN4, MUTED, LINGO2 and CPNE4 786
738 contraceptives, menstruation, pregnancy, and cortisol [74]. A genetic risk score using the number of risk 787
739 levels correlate with motion sickness susceptibility alleles found on each individual for these 35 vari- 788
740 in women, which further complicates the association ants could be used to anticipate motion sickness 789
741 [87, 89, 90]. susceptibility. These genes involve a wide variety of 790
742 Sex differences in VIMS have been observed in functions such as brain, eye, and ear development and 791
743 some studies [81, 91–93], but it remains unclear even insulin resistance. Some of these loci overlap 792
744 whether such observations are due to women being with genes in individuals who experience dizziness, 793
f
745 more open about reporting than men, are better at post-operative nausea and vomiting, altitude sick- 794
roo
746 introspecting than men, or have less experienced ness, morning sickness, indigestion to dairy, and 795
747 with motion than men, among several other con- headache after red wine [74]. 796
750 tual reality (VR) usage [94] while another study [95]
rP
751 concluded that VIMS sex differences in VR may be Other modifying factors may include baseline 798
752 accounted for by a non-sex-specific variable such as autonomic tone, glucose levels, and aerobic fitness 799
753 difficulty in fitting the VR properly to people with [100–102]. It is difficult to predict how these nu- 800
754 smaller interpupillary distance. A variety of other fac- merous factors, in combination, ultimately impact 801
tho
755 tors unrelated to sex can affect occurrence of VIMS, susceptibility in an individual, however. 802
761 4.2.3. Race and ethnicity ness, and headache [84, 103]. Motion sickness is 807
762 Studies that assessed motion sickness susceptibil- self-reported in at least 50% of migraine headache 808
763 ity by questionnaire, rotation of the body with head sufferers with motion sickness in childhood correlat- 809
pitching, and exposure to optokinetic drums have ing with eventual development of migraine headaches
d
764 810
765 reported heightened susceptibility in people of Asian in adolescence and adulthood [47, 104, 105]. These 811
cte
766 descent compared to European or African descent associations suggest that neural pathways for nausea 812
767 [82, 99]. These differences persist in American-born and emesis are particularly sensitive in individuals 813
768 children of Asian parents, supporting at least a partial with migraine [47]. Scalp tenderness and nausea dur- 814
769 heritable component to motion sickness susceptibil- ing optokinetic stimulation increase more for those 815
770 ity[99]. who experience migraine than for those who do not 816
rre
771 Further controlled studies of the ethnic, racial, or [106]. Motion sickness induced by OVAR is espe- 817
772 cultural components to motion sickness are needed. cially intense in individuals with migraine [45]. This 818
773 Generalizations concerning these features which type of motion sickness may be blunted by rizatrip- 819
774 could influence decisions about patient care or occu- tan, a migraine abortive medication [107, 108]. In 820
co
775 pational status should be treated with caution. contrast, VIMS does not appear to be mitigated by 821
776 4.3. Genetic migraine headaches experience both motion sickness 823
777 Heritability for motion sickness (in women) shows migraine, but the correlation between motion sick- 825
778 a 0.69 concordance in monozygotic twins and 0.44 ness and VIMS in this group is weak [110]. 826
781 A large genome-wide association study involving Loss of peripheral vestibular function significantly 828
782 80,494 individuals with carsickness found 35 sin- raises the threshold for motion sickness but the role 829
783 gle nucleotide variants at genome-wide significant of a functioning vestibulum for VIMS is less clear 830
784 levels. The top ten genes involved in these regions [45, 111–113]. Congruently, patients with chronic 831
785 included: PVRL3, GPD2, ACO1, AUTS2, GPR26, stable vestibular loss (unilateral and bilateral) report 832
Y.-H. Cha et al. / Motion sickness diagnostic criteria 13
833 less motion sickness on clinical motion sickness rat- not be the relevant marker of motion sickness suscep- 882
834 ings than healthy controls. In comparison, patients tibility, but rather the ability to modify the VOR in 883
835 with benign paroxysmal positional vertigo show a response to varying motion sickness-inducing stimuli 884
836 non-significant difference in motion sickness sus- [27, 88]. The relationship between motion sickness 885
837 ceptibility [79]. Patients with vestibular neuritis can susceptibility and adaptability of vestibular responses 886
838 experience either an increase or a decrease in motion has also been supported by lower cervical vestibular 887
839 sickness susceptibility after the onset of their disor- evoked myogenic potential (VEMPS) thresholds cor- 888
840 der, with increased susceptibility in uncompensated relating with the ability to habituate to seasickness; 889
f
841 cases [45, 57]. Two studies have shown that indi- this may be attributable to the wider potential range 890
roo
842 viduals with Ménière’s disease are more susceptible of adaptive responses to motion stimuli with lower 891
843 to motion sickness than healthy controls but are not VEMP thresholds [122]. 892
rP
847 and scores on a clinical motion sickness question-
848 naire. In contrast, patients with vestibular disorders Because motion sickness susceptibility in a healthy 894
849 without vestibular loss report higher degrees of mot- person generally declines with age, an adult present- 895
850 ion sickness than controls [45, 104]. About 10-min- ing with increasing susceptibility to motion should be 896
tho
851 utes of laboratory motion exposure has been shown evaluated for underlying causes of a lowered thresh- 897
852 to distinguish the susceptibility of individuals with old for motion sickness. This evaluation may include 898
853 different vestibular disorders (vestibular neuritis, an assessment for vestibular disorders, migraine, 899
854 bilateral vestibulopathy, vestibular migraine) [45]. endocrine abnormalities, ocular misalignment, and 900
855 5. Motion sickness laboratory examinations whole-body motion) should be suspected as being 903
856 Motion sickness may be induced in laboratory try and evaluated with vestibular laboratory testing, 905
857 settings with approximately 38% of the variabil- unless such discomfort is directly related to the after- 906
ity in motion sickness in operational settings being effects of prolonged adaptation to motion (e.g., return
d
858 907
859 explained by an individual’s response to provoca- to land after a voyage at sea). Similarly, abrupt 908
cte
860 tive laboratory motion tests [54]. Most of these changes in VIMS should prompt careful evaluations 909
861 established motion sickness tests are not used for for ocular and ocular motility problems. Clinicians 910
862 clinical diagnosis, however. Correlations between should be aware that head motion during certain 911
863 the MSSQ and laboratory-induced nausea by cross- types of uncompensated vestibular pathology or by 912
864 coupled stimulation have been reported to be between healthy persons during challenging motions or within 913
rre
865 0.14 and 0.58, with generally higher correlations seen unusual force environments (such as space) can each 914
866 for vertical translational oscillations than horizontal elicit similar symptoms of nausea, headache, dizzi- 915
867 oscillations [47]. Of the translational planes, motion ness, vertigo, oscillopsia, or visual blurring, so these 916
868 through the body-referenced X- or Y-axes (fore-aft or symptoms cannot be assumed to definitively dif- 917
co
869 side-to-side motion when upright, respectively) are ferentiate between vestibular pathology and motion 918
870 more provocative than the body-referenced Z-axis, sickness without further inquiry concerning when the 919
871 (up-down) but motion direction with respect to the symptoms appeared (e.g., relative to the last motion 920
872 gravity vector (e.g. vertical versus horizontal) is a experience), under what conditions they appeared 921
Un
873 less important factor [116]. (e.g., the type and duration of the motion experi- 922
874 An area of controversy is whether a smaller phase ence), and what additional symptoms were present 923
875 lead of the vestibulo-ocular reflex (VOR), which [43]. Finally, while a motion sickness disorder would 924
876 indicates enhanced velocity storage, is related patho- be more strongly suspected in a younger person scor- 925
877 physiologically to motion sickness susceptibility, as ing high on the MSSQ or a VIMS disorder in an 926
878 found in some laboratories [116–120] but not others older individual scoring high on the SSQ, individual 927
879 [88, 107]. The mixed findings may relate to the degree variability in motion sickness and VIMS susceptibil- 928
880 of habituation to the motion stimulus [121]. It has ity is high, so clinicians should be cautious not to 929
881 been proposed that the absolute value of the VOR may over-generalize from demographical findings.
14 Y.-H. Cha et al. / Motion sickness diagnostic criteria
930 7. Future directions protection under this title is not available for any work 977
f
Motion Sickness-A Plague at Sea and on Land, Also with 981
937 in determining this distinction in no small part lies in Military Impact, Front Neurol 8 (2017), 114.
roo
982
938 the large number of variables that contribute to inher- [2] E. Darwin, Zoonomia, or The Laws of Organic Life, Vol- 983
939 ent (trait) susceptibility, comorbidity, and variability ume I : Second Edition. Printed for J. Johnson, St. Paul’s 984
Church-Yard, London, (1796) 985
940 of the stimulus each person experiences. [3] J.A. Irwin, The pathology of sea sickness, The Lancet 118 986
941 A challenge in motion sickness and VIMS re- (1881), 907–909. 987
942 search has been the rapid technological advance- [4] W. James, The sense of dizziness in deaf-mutes, Am Ann 988
rP
943 ments in transportation and entertainment options Deaf 28 (1883), 102–117. 989
[5] R.S. Kennedy, A. Graybiel, R.C. McDonough and D. 990
944 that have created an environment of increasing Beckwith, Symptomatology under storm conditions in the 991
945 motion stimuli in both novelty and number [123]. North Atlantic in control subjects and in persons with bilat- 992
946 It remains to be determined whether human beings eral labyrinthine defects., Acta Oto-laryngol 66 (1968), 993
533–540.
tho
947 may be able to push current boundaries of motion 994
[6] J.T. Reason and J.J. Bland, Motion Sickness, London, New 995
948 tolerance through enhanced habituation exercises, York, San Francisco, 1975. 996
949 helpful Earth-referenced sensory cues, manipulation [7] B. Keshavarz, H. Hecht and B.D. Lawson, Visually- 997
950 of vestibular input, cognitive enhancement tech- induced motion sickness: Causes, characteristics, and 998
951 niques, pharmacological therapies, or noninvasive countermeasures. Handbook of virtual environments: 999
Design, implementation, and applications, 2nd Edition. 1000
Au
952 brain stimulation methods. Prediction of suscepti- New York, NY: CRC Press, an imprint of Taylor & Francis 1001
953 bility based on demographics, hormonal rhythms, Group, LLC. (2014), 647–698. 1002
954 genetics, and physiological status may lead to opt- [8] L.J. Hettinger and G.E. Riccio, Visually induced motion 1003
sickness in virtual environments, Presence-Teleop Virt 1 1004
955 imization of environments that reduce stimulus inten-
(1992), 306–310. 1005
956 sity and morbidity. Toward those ends, criteria for [9] R.W. Wood, The ‘Haunted Swing’ illusion, Psychol Rev 2 1006
motion sickness/VIMS and MSD/VIMSD have been
d
958 proposed here to promote clearer communication [10] G.M. Stratton, Some preliminary experiments on vision 1008
without inversion of the retinal image, Psychol Rev 3 1009
cte
959 among clinicians and investigators. These criteria are (1896), 611–617. 1010
960 expected to evolve as data on epidemiology, natural [11] G.M. Stratton, Vision without inversion of the retinal 1011
961 history, biomarkers, and assessments of future health image, Psychol Rev 4 (1897), 341–360. 1012
962 consequences are methodically acquired. [12] R. Kennedy, N. Lane, K. Berbaum and M. Lilienthal, Sim- 1013
ulator sickness questionnaire: An enhanced method for 1014
quantifying simulator sickness, Int J of Aviat Psychol 3
rre
1015
(1993), 203–220. 1016
[13] G.H. Crampton and F.A. Young, The differential effect of 1017
963 Acknowledgements and disclaimers a rotary visual field on susceptibles and nonsusceptibles 1018
to motion sickness, J Comp Physiol Psychol 46 (1953), 1019
451–453. 1020
co
964 The working meetings for the International Cl- [14] R. Kennedy, G. Allgood, B. Van Hoy and M. Lilienthal, 1021
965 assification of Vestibular Disorders (ICVD) are finan- Motion sickness symptoms and postural changes follow- 1022
966 cially supported by the International Bárány Society ing flights in motion-based flight trainers, J Low Freq 1023
Noise, Vib 6 (1987), 147–154. 1024
967 and by Neuro + e.V., Berlin, Germany, a non-profit [15] R.S. Kennedy, M.G. Lilienthal, K.S. Berbaum, D.R. Balt-
Un
1025
968 association for neurological research. We thank zley and M.E. McCauley, Simulator sickness in U.S. Navy 1026
969 members of the Bárány Society for reviewing the flight simulators, Aviat Space Envir Md 60 (1988), 10–16. 1027
970 manuscript prior to publication. The views in this [16] D.R. Baltzley, R.S. Kennedy, K.S. Berbaum, M.G. Lilien- 1028
thal and D.W. Gower, The time course of postflight 1029
971 manuscript are those of the authors and do not reflect simulator sickness symptoms, Aviat Space Envir Md 60 1030
972 the official policy or position of the Department of the (1989), 1043–1048. 1031
973 Navy, Department of Defense, nor the U.S. Govern- [17] B.D. Lawson, Motion sickness symptomatology and 1032
origins. Handbook of virtual environments: Design, imple- 1033
974 ment. This work was assisted by an employee of the
mentation, and applications, 2nd Edition. New York, NY: 1034
975 U.S. Government (Dr. Lawson) as part of his official CRC Press, an imprint of Taylor & Francis Group, LLC. 1035
976 duties. Title 17, U.S.C., §105 provides that ‘copyright (2014), 531–600. 1036
Y.-H. Cha et al. / Motion sickness diagnostic criteria 15
1037 [18] J.T. Reason, Motion sickness adaptation: A neural mis- [39] B.D. Lawson and A.M. Mead, The sopite syndrome revis- 1102
1038 match model, J R Soc Med 71 (1978), 819–829. ited: Drowsiness and mood changes during real or apparent 1103
1039 [19] J.F. Golding, Motion sickness susceptibility, Auton motion, Acta Astronaut 43 (1998), 181–192. 1104
1040 Neurosci-Basic 129 (2006), 67–76. [40] B.D. Lawson, Motion sickness scaling. Handbook of 1105
1041 [20] C.M. Oman, Motion sickness: A synthesis and evaluation virtual environments: Design, implementation, and appli- 1106
1042 of the sensory conflict theory, Can J Physiol Pharm 68 cations, 2nd Edition. New York, NY: CRC Press, an 1107
1043 (1990), 294–303. imprint of Taylor & Francis Group, LLC. (2014), 601–626. 1108
1044 [21] J.E. Bos and W. Bles, Modelling motion sickness and [41] B.D. Lawson and B.E. Riecke, The perception of body 1109
1045 subjective vertical mismatch detailed for vertical motions, motion, ed. Stanney K., Hale K., Handbook of Virtual 1110
1046 Brain Res Bull 47 (1998), 537–542. Environments: Design, Implementation, and Applications, 1111
f
1047 [22] F.E. Guedry and A.J. Benson, Coriolis cross-coupling CRC Press, New York, NY., 2014, 163–196. 1112
roo
1048 effects: disorienting and nauseogenic or not? Aviat Space [42] A. Bisdorff, M. Von Brevern, T. Lempert and D.E. 1113
1049 Envir Md 49 (1978), 29–35. Newman-Toker, Classification of vestibular symptoms: 1114
1050 [23] R. Kennedy, K. Stanney and W. Dunlap, Duration and towards an international classification of vestibular dis- 1115
1051 exposure to virtual environments: Sickness curves dur- orders, J Vestib Res 19 (2009), 1–13. 1116
1052 ing and across sessions, Presence-Teleop Virt 9 (2000), [43] B.D. Lawson, A.H. Rupert and B.J. McGrath, The 1117
1053 463–472. neurovestibular challenges of astronauts and balance 1118
rP
1054 [24] B.J. Yates, A.D. Miller and J.B. Lucot, Physiological basis patients: some past countermeasures and two alternative 1119
1055 and pharmacology of motion sickness: An update, Brain approaches to elicitation, assessment and mitigation, Front 1120
1056 Res Bull 47 (1998), 395–406. Sys Neurosci 10 (2016), 1–12. 1121
1057 [25] M. Treisman, Motion sickness: An evolutionary hypothe- [44] B.S.K. Cheung, I.P. Howard, J.M. Nedzelski and J.P. 1122
1058 sis, Science 197 (1977), 493–495. Landolt, Circularvection about earth-horizontal axes 1123
1059 [26] G.R. Morrow, The effect of a susceptibility to motion sick- in bilateral labyrinthine-defective subjects, Acta Oto- 1124
tho
1060 ness on the side effects of cancer chemotherapy, Cancer laryngol 108 (1989), 336–344. 1125
1061 55 (1985), 2766–2770. [45] F. Murdin, F. Chamberlain, S. Cheema, Q. Arshad, M.A. 1126
1062 [27] J.F. Golding, Motion sickness., Handb Clin Neurol 137 Gresty, J.F. Golding and A. Bronstein, Motion sickness in 1127
1063 (2016), 371–390. migraine and vestibular disorders, J Neurol Neurosur Ps 1128
1064 [28] C.M. Oman, Are evolutionary hypotheses for motion 86 (2015), 585–587. 1129
1065 sickness “just so” stories?, J Vestib Res 22 (2012), [46] Y.H. Cha, R.W. Baloh, C. Cho, M. Magnusson, J.-J. Song, 1130
Au
1066 117–127. M. Strupp, F. Wuyts and J.P. Staab, Mal de Debarquement 1131
1067 [29] D.B. Tyler and P. Bard, Motion sickness, Physiol Rev 29 Syndrome Diagnostic Criteria: Consensus Document of 1132
1068 (1949), 311–369. the Classification Committee of the Barany Society, J 1133
1069 [30] A. Graybiel, B. Clark and J.J. Zarriello, Observations on Vestib Res 30 (2020), 285–293. 1134
1070 human subjects living in a “slow rotation room” for periods [47] J.F. Golding, Motion sickness susceptibility questionnaire 1135
1071 of two days, Arch Neurol 3 (1960), 55–73. revised and its relationship to other forms of sickness, 1136
[31] E.F. Miller and A. Graybiel, A provocative test for grading Brain Res Bull 47 (1998), 507–516. 1137
d
1072
1073 susceptibility to motion sickness yielding a single numer- [48] J.F. Golding, Predicting individual differences in motion 1138
1074 ical score, Acta Otolaryngol Suppl 274 (1970), 1–20. sickness susceptibility by questionnaire, Pers Indiv Differ 1139
cte
1075 [32] A. Graybiel, C.D. Wood, E.F. Miller and D.B. Cramer, 41 (2006), 237–248. 1140
1076 Diagnostic criteria for grading the severity of acute motion [49] J.F. Golding and M. Kerguelen, A comparison of the 1141
1077 sickness, Aerosp Med 39 (1968), 453–455. nauseogenic potential of low-frequency vertical versus 1142
1078 [33] P.J. Gianaros, E.R. Muth, J.T. Mordkoff, M.E. Levine and horizontal linear oscillation, Aerosp Med Assoc 63 (1992), 1143
1079 R.M. Stern, A questionnaire for the assessment of the mul- 491–497. 1144
1080 tiple dimensions of motion sickness, Aviat Space Envir Md [50] M.J. Griffin and M.M. Newman, Visual field effects on 1145
rre
1081 72 (2001), 115–119. motion sickness in cars, Aviat Space Envir Md 75 (2004), 1146
1082 [34] J.E. Bos, S.N. MacKinnon and A. Patterson, Motion sick- 739–748. 1147
1083 ness symptoms in a ship motion simulator: effects of [51] J.E. Bos, S.N. MacKinnon and A. Patterson, Motion sick- 1148
1084 inside, outside, and no view, Aviat Space Envir Md 76 ness symptoms in a ship motion simulator: effects of 1149
1085 (2005), 1111–1118. inside, outside, and no view, Aviat Space Envir Md 76 1150
co
1086 [35] J.R. Lackner and A. Graybiel, Sudden emesis follow- (2005), 1111–1118. 1151
1087 ing parabolic flight maneuvers: implications for space [52] M.L. van Emmerik, S.C. de Vries and J.E. Bos, Internal 1152
1088 motion sickness, Aviat Space Envir Md 57 (1986), and external fields of view affect cybersickness., Displays 1153
1090 [36] J.T. Reason and A. Graybiel, Changes in subjective esti- [53] B. Keshavarz and H. Hecht, Validating an efficient method 1155
Un
1091 mates of well-being during the onset and remission of to quantify motion sickness, Hum Factors 53 (2011), 1156
1093 Room., Aerospace Med 41 (1970), 166–171. [54] R.S. Kennedy, W.P. Dunlap and F. J.E., Chapter 11: Pre- 1158
1094 [37] J.F. Golding, A.C. Paillard, H. Normand, S. Besnard and P. diction of motion sickness susceptibility, G. H. Crampton, 1159
1095 Denise, Prevalence, predictors, and prevention of motion Boca Raton, FL., 1990, 179–215. 1160
1096 sickness in zero-g parabolic flights, Aerosp Med Hum Perf [55] S. Lamb and K.C. Kwok, MSSQ-Short norms may under- 1161
1097 88 (2017), 3–9. estimate highly susceptible individuals: Updating the 1162
1098 [38] S.F. Wiker, R.S. Kennedy, M.E. McCauley and R.L. Pep- MSSQ-short norms, Hum Factors 57 (2015), 622–633. 1163
1099 per, Susceptibility to seasickness: influence of hull design [56] B. Keshavarz, R. Ramkhalawansingh, B. Haycock, S. Sha- 1164
1100 and steaming direction, Aviat Space Envir Md 50 (1979), hab and J.L. Campos, Comparing simulator sickness in 1165
1101 1046–1051. younger and older adults during simulated driving under 1166
16 Y.-H. Cha et al. / Motion sickness diagnostic criteria
1167 different multisensory conditions, Transport Res F-Traf performance in fixed and moving base driving simulators, 1232
1168 54 (2018), 47–62. Transport Res F-Traf 37 (2016), 78–96. 1233
1169 [57] R.S. Kennedy and J.E. Fowlkes, Simulator sickness [76] K.M. Stanney, R.S. Kennedy, J.M. Drexler and D.L. Harm, 1234
1170 is polygenic and polysymptomatic: Implications for Motion sickness and proprioceptive aftereffects follow- 1235
1171 research, Int J Aviat Psychol 2 (1992), 23–38. ing virtual environment exposure, Appl Ergon 30 (1999), 1236
1172 [58] J.F. Golding and M.A. Gresty, Pathophysiology and treat- 27–38. 1237
1173 ment of motion sickness, Curr Opin Neurol 28 (2015), [77] S. Cobb, S. Nichols, A. Ramsey and J. Wilson, Virtual 1238
1174 83–88. reality-induced symptoms and effects (VRISE), Presence- 1239
1175 [59] B. Keshavarz and H. Hecht, Pleasant music as a counter- Teleop Virt (1999), 169–186. 1240
1176 measure against visually induced motion sickness, Appl [78] K. Stanney and G. Salvendy, Aftereffects and sense 1241
f
1177 Ergon 45 (2014), 521–527. of presence in virtual environments: Formulation of a 1242
roo
1178 [60] F.D. Yen Pik Sang, J.F. Golding and M.A. Gresty, Sup- research and development agenda, Int J Hum Comput 1243
1179 pression of sickness by controlled breathing during mildly Interact 10 (1998), 135–187. 1244
1180 nauseogenic motion, Aviat Space Envir Md 74 (2003), [79] A.C. Paillard, G. Quarck, F. Paolino, P. Denise, M. Paolino, 1245
1181 998–1002. J.F. Golding and V. Ghulyan-Bedikian, Motion sickness 1246
1182 [61] D.B. Mowrey and D.E. Clayson, Motion sickness, ginger, susceptibility in healthy subjects and vestibular patients: 1247
1183 and psychophysics, Lancet 1 (1982), 655–657. Effects of gender, age and trait-anxiety, J Vestib Res 23 1248
rP
1184 [62] H.C. Lien, W.M. Sun, Y.H. Chen, H. Kim, W. Hasler and C. (2013), 203–209. 1249
1185 Owyang, Effects of ginger on motion sickness and gastric [80] J.O. Brooks, R.R. Goodenough, M.C. Crisler, N.D. Klein, 1250
1186 slow-wave dysrhythmias induced by circular vection, Am R.L. Alley and B.L. Koon, Simulator sickness during driv- 1251
1187 J Physiol-Gastr L 284 (2003), G481–489. ing simulation studies, Accident Anal Prev 42 (2010), 1252
1188 [63] P.L. Palatty, R. Haniadka, B. Valder, R. Arora and M.S. 788–796. 1253
1189 Baliga, Ginger in the prevention of nausea and vomiting: [81] N. Kawano, K. Iwamoto, K. Ebe, B. Aleksic, A. Noda and 1254
tho
1190 a review, Crit Rev Food Sci Nutr 53 (2013), 659–669. H. Umegaki, Slower adaptation to driving simulator and 1255
1191 [64] A. Alkaissi, T. Ledin, L.M. Odkvist and S. Kalman, P6 simulator sickness in older adults, Aging Clin Exp Res 24 1256
1192 acupressure increases tolerance to nauseogenic motion (2012), 285–289. 1257
1193 stimulation in women at high risk for PONV, Can J [82] S. Klosterhalfen, S. Kellermann, F. Pan, U. Stockhorst, 1258
1194 Anaesth 52 (2005), 703–709. G. Hall and P. Enck, Effects of ethnicity and gender 1259
1195 [65] K.E. Miller and E.R. Muth, Efficacy of acupressure and on motion sickness susceptibility, Aviat Space Envir Md 1260
Au
1196 acustimulation bands for the prevention of motion sick- (2005), 1051–1057. 1261
1197 ness, Aviat Space Envir Md 75 (2004), 227–234. [83] P.M. Gahlinger, Cabin location and the likelihood of 1262
1198 [66] A. Brainard and C. Gresham, Prevention and treatment of motion sickness in cruise ship passengers, J Travel Med 7 1263
1199 motion sickness, Am Fam Physician 90 (2014), 41–46. (2000), 120–124. 1264
1200 [67] A. Shupak and C.R. Gordon, Motion sickness: Advances [84] D.A. Marcus, J.M. Furman and C.D. Balaban, Motion 1265
1201 in pathogenesis, prediction, prevention, and treatment, sickness in migraine sufferers, Expert Opin Pharmaco 6 1266
1202 Aviat Space Envir Md 77 (2006), 1213–1223. (2005), 2691–2697. 1267
d
1203 [68] O. Samuel and D. Tal, Airsickness: Etiology, treatment, [85] A. Lawther and M.J. Griffin, A survey of the occurrence 1268
1204 and clinical importance-a review, Mil Med 180 (2015), of motion sickness amongst passengers at sea, Aviat Space 1269
cte
1211 Social life & Work Impact of Dizziness questionnaire Space Envir Md 76 (2005), 970–973. 1276
1212 (SWID), 7th Meeting of the British Society of Neuro- [88] J.F. Golding and M.A. Gresty, Motion sickness, Curr Opin 1277
1213 Otology, Leicester Tigers Rugby Stadium (2009). Neurol (2005), 29–34. 1278
1214 [71] A.M. Bronstein, J.F. Golding, M.A. Gresty, M. Mandalá, [89] R.L. Matchock, M.E. Levine, P.J. Gianaros and R.M. 1279
1215 D. Nuti, A. Shetye and Y. Silove, The Social Impact of Stern, Susceptibility to nausea and motion sickness as a 1280
co
1216 Dizziness in London and Siena, J Neurol 257 (2010), function of the menstrual cycle, Womens Health Iss 18 1281
1217 183–190. (2008), 328–335. 1282
1218 [72] C.M. Reavley, J.F. Golding, L.F. Cherkas, T.D. Spector and [90] K. Meissner, P. Enck, E.R. Muth, S. Kellermann and A. 1283
1219 A.J. MacGregor, Genetic influences on motion sickness Klosterhalfen, Cortisol levels predict motion sickness tol- 1284
1220 susceptibility in adult women: A classical twin study, Aviat erance in women but not in men, Physiol Behav 97 (2009), 1285
Un
1297 [94] D. Saredakis, A. Szpak, B. Birckhead, H.A.D. Keage, A. [109] J.M. Furman and D.A. Marcus, A pilot study of rizatriptan 1349
1298 Rizzo and T. Loetscher, Factors Associated With Virtual and visually-induced motion sickness in migraineurs, Int 1350
1299 Reality Sickness in Head-Mounted Displays: A System- J Med Sci 6 (2009), 212–217. 1351
1300 atic Review and Meta-Analysis, Front Hum Neurosci 14 [110] P.D. Drummond, Triggers of motion sickness in migraine 1352
1301 (2020), 96. sufferers, Headache 45 (2005), 653–656. 1353
1302 [95] K. Stanney, C. Fidopiastis and L. Foster, Virtual reality is [111] W.H. Johnson, F.A. Sunahara and J.P. Landolt, Importance 1354
1303 sexist: but it does not have to be, Frontiers in Robotics and of the vestibular system in visually induced nausea and 1355
1304 AI 7 (2020). self-vection, J Vestib Res 9 (1999), 83–87. 1356
1305 [96] H. Ujike, K. Ukai and K. Nihei, Survey on motion [112] B.S. Cheung, I.P. Howard and K.E. Money, Visually- 1357
1306 sickness-like symptoms provoked by viewing a video induced sickness in normal and bilaterally labyrinthine- 1358
f
1307 movie during junior high school class, Displays 29 (2008), defective subjects, Aviat Space Envir Md 62 (1991), 1359
roo
1308 81–89. 527–531. 1360
1309 [97] B. Keshavarz, A.C. Novak, L.J. Hettinger, T.A. Stoffre- [113] R.S. Kennedy, A. Graybiel, R.C. McDonough and F.D. 1361
1310 gen and J.L. Campos, Passive restraint reduces visually Beckwith, Symptomatology under storm conditions in the 1362
1311 induced motion sickness in older adults, J Exp Psychol north atlantic in control subjects and in persons with bilat- 1363
1312 Appl 23 (2017), 85–99. eral labyrinthine defects, Acta Otolaryngol 66 (1968), 1364
1313 [98] J. Bos, W. Bles and E. Groen, A theory on visually induced 533–540. 1365
rP
1314 motion sickness, Displays 29 (2008), 47–57. [114] J.F. Golding and M. Patel, Meniere’s, migraine, and 1366
1315 [99] R.M. Stern, S. Hu, S.H. Uijtdehaage, E.R. Muth, L.H. motion sickness Acta Otolaryngol 137 (2017), 495–502. 1367
1316 Xu and K.L. Koch, Asian hypersusceptibility to motion [115] J.D. Sharon and T.E. Hullar, Motion sensitivity and caloric 1368
1317 sickness, Hum Hered 46 (1996), 7–14. responsiveness in vestibular migraine and Meniere’s dis- 1369
1318 [100] B.S. Cheung, K.E. Money and I. Jacobs, Motion sickness ease, Laryngoscope 124 (2014), 969–973. 1370
1319 susceptibility and aerobic fitness: A longitudinal study, [116] J.F. Golding, H.M. Markey and J.R. Stott, The effects of 1371
tho
1320 Aviat Space Environ Med 61 (1990), 201–204. motion direction, body axis, and posture on motion sick- 1372
1321 [101] N. Rawat, C.W. Connor, J.A. Jones, I.B. Kozlovskaya and ness induced by low frequency linear oscillation, Aviat 1373
1322 P. Sullivan, The correlation between aerobic fitness and Space Envir Md 66 (1995), 1046–1051. 1374
1323 motion sickness susceptibility, Aviat Space Envir Md 73 [117] S.H. Jeong, S.Y. Oh, H.J. Kim, J.W. Koh and J.S. Kim, 1375
1324 (2002), 216–218. Vestibular dysfunction in migraine: Effects of associ- 1376
1325 [102] F.F. Mo, H.H. Qin, X.L. Wang, Z.L. Shen, Z. Xu and ated vertigo and motion sickness, J Neurol 257 (2010), 1377
Au
1326 K.H. Wang, Acute hyperglycemia is related to gastroin- 905–912. 1378
1327 testinal symptoms in motion sickness: An experimental [118] M. Dai, T. Raphan and B. Cohen, Prolonged reduction of 1379
1328 study, Physiol Behav 105 (2012), 394–401. motion sickness sensitivity by visual-vestibular interac- 1380
1329 [103] A. Cuomo-Granston and P.D. Drummond, Migraine and tion, Exp Brain Res 210 (2011), 503–513. 1381
1330 motion sickness: What is the link?, Prog Neurobiol 91 [119] M.E. Hoffer, K.R. Gottshall, R.D. Kopke, P. Weisskopf, 1382
1331 (2010), 300–312. R.J. Moore, K.A. Allen and D. Wester, Vestibular testing 1383
1332 [104] A.C. Paillard, G. Quarck, F. Paolino, P. Denise, M. Paolino, abnormalities in individuals with motion sickness, Otol 1384
d
1333 J.F. Golding and V. Ghulyan-Bedikian, Motion sickness Neurotol 24 (2003), 633–636. 1385
1334 susceptibility in healthy subjects and vestibular patients: [120] G. Clément and M.F. Reschke, Relationship between 1386
cte
1335 effects of gender, age and trait-anxiety, J Vestib Res 23 motion sickness susceptibility and vestibulo-ocular reflex 1387
1336 (2013), 203–209. gain and phase, J Vestib Res 28 (2018), 295–304. 1388
1337 [105] A. Kayan and J.D. Hood, Neuro-otological manifestations [121] A. Shupak, D. Kerem, C. Gordon, O. Spitzer, N. Mende- 1389
1338 of migraine Brain 107 (1984), 1123–1142. lowitz and Y. Melamed, Vestibulo-ocular reflex as a 1390
1339 [106] P.D. Drummond, Motion sickness and migraine: Optoki- parameter of seasickness susceptibility, Ann Otol Rhinolo 1391
1340 netic stimulation increases scalp tenderness, pain Laryngol 99 (1990), 131–136. 1392
rre
1341 sensitivity in the fingers and photophobia, Cephalalgia [122] D. Tal, D. Hershkovitz, G. Kaminski-Graif, G. Wiener, 1393
1342 22 (2002), 117–124. O. Samuel and A. Shupak, Vestibular evoked myogenic 1394
1343 [107] J.M. Furman, D.A. Marcus and C.D. Balaban, Riza- potentials and habituation to seasickness, Clin Neurophys- 1395
1344 triptan reduces vestibular-induced motion sickness in iol 124 (2013), 2445–2449. 1396
1345 migraineurs. J Headache Pain 12 (2011), 81–88. [123] T.A. Stoffregen, Y.C. Chen and F.C. Koslucher, Motion 1397
co
1346 [108] D.A. Marcus and J.M. Furman, Prevention of motion sick- control, motion sickness, and the postural dynamics of 1398
1347 ness with rizatriptan: A double-blind, placebo-controlled mobile devices Exp Brain Res 232 (2014), 1389–1397. 1399
1348 pilot study, Med Sci Monit 12 (2006), PI1-7.
Un