Mal de Debarquement Syndrome: A Retrospective Online Questionnaire on the Influences of Gonadal Hormones in Relation to Onset and Symptom Fluctuation

Viviana Mucci, Josephine M Canceri, Rachael Brown, Mingjia Dai, Sergei B Yakushin, Shaun Watson, Angelique Van Ombergen, Yves Jacquemyn, Paul Fahey, Paul H Van de Heyning, Floris Wuyts, Cherylea J Browne, Viviana Mucci, Josephine M Canceri, Rachael Brown, Mingjia Dai, Sergei B Yakushin, Shaun Watson, Angelique Van Ombergen, Yves Jacquemyn, Paul Fahey, Paul H Van de Heyning, Floris Wuyts, Cherylea J Browne

Abstract

Introduction: Mal de Debarquement Syndrome (MdDS) is a condition characterized by a persistent perception of self-motion, in most cases triggered from exposure to passive motion (e.g., boat travel, a car ride, flights). Patients whose onset was triggered in this way are categorized as Motion-Triggered (MT) subtype or onset group. However, the same syndrome can occur spontaneously or after non-motion events, such as childbirth, high stress, surgery, etc. Patients who were triggered in this way are categorized as being of the Spontaneous/Other (SO) subtype or onset group. The underlying pathophysiology of MdDS is unknown and there has been some speculation that the two onset groups are separate entities. However, despite the differences in onset between the subtypes, symptoms are parallel and a significant female predominance has been shown. To date, the role of gonadal hormones in MdDS pathophysiology has not been investigated. This study aimed to evaluate the hormonal profile of MdDS patients, the presence of hormonal conditions, the influence of hormones on symptomatology and to assess possible hormonal differences between onset groups. In addition, the prevalence of migraine and motion sickness and their relation to MdDS were assessed.

Method: Retrospective online surveys were performed in 370 MdDS patients from both onset groups. Data were analyzed using Fisher's exact test or Fisher-Freeman-Hanlon exact test. When possible, data were compared with normative statistical data from the wider literature.

Results: From the data collected, it was evident that naturally cycling female respondents from the MT group were significantly more likely to report an aggravation of MdDS symptoms during menses and mid-cycle (p < 0.001). A few preliminary differences between the onset groups were highlighted such as in regular menstrual cycling (p = 0.028), reporting menses during onset (p < 0.016), and migraine susceptibility after onset (p = 0.044).

Conclusion: These results demonstrate a potential relation between hormone fluctuations and symptom aggravation in the MT group. This study is an important first step to suggest a hormonal involvement in the pathophysiology of MdDS and provides a base for further hormonal investigation. Future prospective studies should expand upon these results and explore the implications for treatment.

Keywords: Mal de Debarquement syndrome; Mal de Debarquement syndrome hormonal profiles; balance disorder; estrogen withdrawal; gonadal hormones; symptom fluctuations.

Figures

Figure 1
Figure 1
Symptom aggravation during menses (M—black bars) and mid-cycle around ovulation (O—gray bars) in Spontaneous/Other (SO) group expressed as the percentage of respondents. No statistically significant difference was observed among the SO group reporting an aggravation of symptoms during menses or ovulation.
Figure 2
Figure 2
Fluctuations of estrogen, progesterone and luteinizing hormone during a typical 28-day menstrual cycle. Abbreviations: EST, estrogen; PROG, progesterone; LH, luteinizing hormone.

References

    1. Van Ombergen A, Van Rompaey V, Meas LK, Van de Heyning PH, Wuyts FL. Mal de Debarquement syndrome: a systematic review. J Neurol (2016) 263(5):843–54.10.1007/s00415-015-7962-6
    1. Van Ombergen A, Wuyts FL, Cha YH. Letter to the editor: comment and erratum to “Mal de Debarquement syndrome: a systematic review”. J Neurol (2016) 263(5):855–60.10.1007/s00415-016-8102-7
    1. Cha YH. Mal de Debarquement syndrome: new insights. Ann N Y Acad Sci (2016) 1343(1):63–8.10.1111/nyas.12701
    1. Mucci V, Canceri JM, Brown R, Dai M, Yakushin SB, Watson S, et al. Mal de Debarquement syndrome: a survey on subtypes, misdiagnoses, onset and associated psychological features. J Neurol (2018) 265(3):486–99.10.1007/s00415-017-8725-3
    1. Mucci V, Cha YH, Wuyts FL, Van Ombergen A. Perspective: stepping stones to unraveling the pathophysiology of Mal de Debarquement syndrome with neuroimaging. Front Neurol (2018) 9:42.10.3389/fneur.2018.00042
    1. Dai M, Cohen B, Smouha E, Cho C. Readaptation of the vestibulo-ocular reflex relieves the Mal De Debarquement syndrome. Front Neurol (2014) 5:124.10.3389/fneur.2014.00124
    1. Dai M, Cohen B, Cho C, Shin S, Yakushin SB. Treatment of the Mal de Debarquement syndrome: a 1-year follow-up. Front Neurol (2017) 8:175.10.3389/fneur.2017.00175
    1. Cha YH, Brodsky J, Ishiyama G, Sabatti C, Baloh RW. Clinical features and associated syndromes of Mal de Debarquement. J Neurol (2008) 255(7):1038–44.10.1007/s00415-008-0837-3
    1. Brown JJ, Baloh RW. Persistent Mal de Debarquement syndrome: a motion-induced subjective disorder of balance. Am J Otolaryngol (1987) 8(4):219–22.
    1. Cha YH. Mal de Debarquement. Semin Neurol (2009) 29(5):520–7.10.1055/s-0029-1241038
    1. Hain TC, Hanna PA, Rheinberger MA. Mal de Debarquement. Arch Otolaryngol Head Neck Surg (1999) 125(6):615–20.10.1001/archotol.125.6.615
    1. Hain TC, Cherchi M. Mal de Debarquement syndrome. Handb Clin Neurol (2016) 137:391–5.10.1016/B978-0-444-63437-5.00028-5
    1. Poromaa S, Gingnell M. Menstrual cycle influence on cognitive function and emotion processing—from a reproductive perspective. Front Neurosci (2014) 8(24):380.10.3389/fnins.2014.00380
    1. Andrews JC, Gregory AA, Honrubia V. The exacerbation of symptoms in Meniere’s disease during the premenstrual period. Arch Otolaryngol Head Neck Surg (1992) 118(1):74–8.10.1001/archotol.1992.01880010078020
    1. Elkind-hirsch KE, Stoner WR, Stach BA, Jerger JF. Estrogen influences auditory brainstem responses during the normal menstrual cycle. Hear Res (1992) 60(2):143–8.10.1016/0378-5955(92)90016-G
    1. Eviatar A, Goodhill V. Dizziness as related to menstrual cycles and hormonal contraceptives. Arch Otolaryngol (1969) 90(3):301–6.10.1001/archotol.1969.00770030303010
    1. Korsunska LL, Meshcheryakova AV. The epidemiology of vestibular dysfunction in women with perimenopausal period. Crimean J Exp Clin Med (2013) 3 N(1–2):14–7.
    1. Lempert T, Neuhauser H. Epidemiology of vertigo, migraine and vestibular migraine. J Neurol (2009) 256(3):333–8.10.1007/s00415-009-0149-2
    1. Cha YH, Cui Y. Rocking dizziness and headache: a two-way street. Cephalalgia (2013) 33(14):1160–9.10.1177/0333102413487999
    1. Sacco S, Ricci S, Degan D, Carolei A. Migraine in women: the role of hormones and their impact on vascular diseases. J Headache Pain (2012) 13(3):177–89.10.1007/s10194-012-0424-y
    1. Tepper SJ. Perimenstrual migraines: are they different from migraines in general? Curr Pain Headache Rep (2008) 12(6):463–7.10.1007/s11916-008-0078-2
    1. Macgregor EA. Female sex hormones and migraine. Rev Neurol (Paris) (2005) 161(6–7):677–8.10.1016/S0035-3787(05)85114-8
    1. Park JH, Viirre E. Vestibular migraine may be an important cause of dizziness/vertigo in perimenopausal period. Med Hypotheses (2010) 75(5):409–14.10.1016/j.mehy.2009.04.054
    1. Cuomo-granston A, Drummond PD. Progress in neurobiology migraine and motion sickness: what is the link? Prog Neurobiol (2010) 91(4):300–12.10.1016/j.pneurobio.2010.04.001
    1. Golding JF. Predicting individual differences in motion sickness susceptibility by questionnaire. Pers Individ Dif (2006) 41(2):237–48.10.1016/j.paid.2006.01.012
    1. Grunfeld E, Gresty MA. Relationship between motion sickness, migraine and menstruation in crew members of a “round the world” Yacht race. Brain Res Bull (1999) 47(5):433–6.10.1016/S0361-9230(98)00099-9
    1. Balaban CD, Yates BJ. What is nausea? A historical analysis of changing views. Auton Neurosci (2017) 202:5–17.10.1016/j.autneu.2016.07.003
    1. Mcewen BS, Alves SE. Estrogen actions in the central nervous system. Endocr Rev (1999) 20(3):279–307.10.1210/edrv.20.3.0365
    1. Sherman S. Defining the menopausal transition. Am J Med (2005) 118(12B):3–7.10.1016/j.amjmed.2005.11.002
    1. O’Connor PJ. Normative data: their definition, interpretation, and importance for primary care physicians. Fam Med (1990) 22(4):307–11.
    1. Burch RC, Loder S, Loder E, Smitherman TA. The prevalence and burden of migraine and severe headache in the United States: updated statistics from Government Health Surveillance Studies. Headache (2015) 55(1):21–34.10.1111/head.12482
    1. Canaris GJ, Manowitz NR, Mayor G, Ridgway EC. The colorado thyroid disease prevalence study. Arch Intern Med (2000) 160(4):526–34.10.1001/archinte.160.4.526
    1. Ding T, Hardiman PJ, Petersen J, Wang F-F, Qu F, Baio G. The prevalence of polycystic ovary syndrome in reproductive-aged women of different ethnicity: a systematic review and meta-analysis. Oncotarget (2017) 8(56):96351–8.10.18632/oncotarget.19180
    1. Enewold L, Brinton LA, McGlynn KA, Zahm SH, Potter JF, Zhu K. Oral contraceptive use among women in the military and the general U.S. Population 1. J Womens Health (Larchmt) (2010) 19(5):839–45.10.1089/jwh.2009.1706
    1. Hersh AL, Stefanick ML, Stafford RS. National use of postmenopausal hormone therapy. Annual trends and response to recent evidence. JAMA (2004) 291(1):47–53.10.1001/jama.291.1.47
    1. Katol I, Toniolo P, Koenig KL, Shore RE, Zeleniuch-jacquotte A, Akhmedkhanov A, et al. Epidemiologic correlates with menstrual cycle length in middle aged women. Eur J Epidemiol (2016) 15(9):809–14.10.1023/A:1007669430686
    1. Sherman BM, Korenman SG. Hormonal characteristics. J Clin Invest (1975) 55(4):699–706.10.1172/JCI107979
    1. Reed BG, Carr BR. The normal menstrual cycle and the control of ovulation In: De Groot LJ, Chrousos G, Dungan K, editors. Endotext [Internet]. South Dartmouth, MA: Inc. (2000). Available from:
    1. Macgregor EA. Menstrual migraine: a clinical review. J Fam Plann Reprod Health Care (2007) 33(1):36–47.10.1783/147118907779399684
    1. Chung S-H, Kim T-H, Lee H-H, Lee A, Jeon D-S, Park J, et al. Premenstrual syndrome and premenstrual dysphoric disorder in perimenopausal women. J Menopausal Med (2014) 20(2):69–74.10.6118/jmm.2014.20.2.69
    1. Fridén C, Hirschberg AL, Saartok T, Bäckström T, Leanderson J, Renström P. The influence of premenstrual symptoms on postural balance and kinesthesia during the menstrual cycle. Gynecol Endocrinol (2003) 17(6):433–9.10.1080/09513590312331290358
    1. Ishii C, Nishino LK, De Campos CA. Vestibular characterization in the menstrual cycle. Braz J Otorhinolaryngol (2009) 75(3):375–80.10.1590/S1808-86942009000300012
    1. Gillies GE, McArthur S. Estrogen actions in the brain and the basis for differential action in men and women: a case for sex-specific medicines. Pharmacol Rev (2010) 62(2):155–98.10.1124/pr.109.002071
    1. Freeman EW. Pharmacological aspects: treatment of depression associated with the menstrual cycle: premenstrual dysphoria, postpartum depression, and the perimenopause. Dialogues Clin Neurosci (2002) 4(2):177–91.
    1. Santin AP, Weber Furlanetto T. Role of estrogen in thyroid function and growth regulation. J Thyroid Res (2011) 2011(875125):7.10.4061/2011/875125
    1. Woolley CS. Effects of estrogen in the CNS. Curr Opin Neurobiol (1999) 9(3):349–54.10.1016/S0959-4388(99)80051-8
    1. Al-Mana D, Ceranic B, Djahanbakhch O, Luxon LM. Hormones and the auditory system: a review of physiology and pathophysiology. Neuroscience (2008) 153(4):881–900.10.1016/j.neuroscience.2008.02.077
    1. Bondt T, De Belder F, Vanhevel F, Jacquemyn Y, Parizel PM. Prefrontal GABA concentration changes in women—influence of menstrual cycle phase, hormonal contraceptive use, and correlation with premenstrual symptoms. Brain Res (2015) 1597:129–38.10.1016/j.brainres.2014.11.051
    1. Halbreich U, Petty F, Yonkers K, Kramer GL, Rush AJ, Bibi KW. Low plasma gamma-aminobutyric acid levels during the late luteal phase of women with premenstrual dysphoric disorder. Am J Psychiatry (1996) 153(5):718–20.10.1176/ajp.153.5.718
    1. Nuss P. Anxiety disorders and GABA neurotransmission: a disturbance of modulation. Neuropsychiatr Dis Treat (2015) 11:165–75.10.2147/NDT.S58841
    1. Burger H, Woods NF, Dennerstein L, Leventhal Alexander J, Kotz K, Richardson G. Nomenclature and endocrinology of menopause and perimenopause. Expert Rev Neurother (2007) 11(7):35–43.10.1586/14737175.7.11s.S35
    1. Li S, Lanuza D, Gulanick M, Penckofer S, Holm K. Perimenopause: the transition into menopause. Health Care Women Int (1996) 17(4):293–306.10.1080/07399339609516246
    1. Su HI, Freeman EW. Hormone changes associated with the menopausal transition. Minerva Ginecol (2009) 61(6):483–9.
    1. Barth C, Steele CJ, Mueller K, Rekkas VP, Arélin K, Pampel A, et al. In-vivo dynamics of the human hippocampus across the menstrual cycle. Sci Rep (2016) 6:32833.10.1038/srep32833
    1. Allsworth JE, Clarke J, Peipert JF, Hebert MR, Cooper A, Boardman LA. The influence of stress on the menstrual cycle among newly incarcerated women. Womens Health Issues (2008) 17(4):202–9.10.1016/j.whi.2007.02.002
    1. Polson DW, Adams J, Wadsworth J, Franks S. Polycystic ovaries – a common finding in normal women. Lancet (1988) 1(8590):870–2.10.1016/S0140-6736(88)91612-1
    1. Celec P, Ostatníková D, Hodosy J. On the effects of testosterone on brain behavioral functions. Front Neurosci (2015) 9:12.10.3389/fnins.2015.00012
    1. Laughlin GA, Barrett-connor E, Kritz-silverstein D, Kritz-Silverstein D, von Mühlen D. Hysterectomy, oophorectomy, and endogenous sex hormone levels in older women: the Rancho Bernardo Study. J Clin Endocrinol Metab (2000) 85(2):645–51.10.1210/jcem.85.2.6405
    1. Jailer JW, Longson D. Hormonal changes during pregnancy. Surg Clin North Am (1957) 37(2):341–52.10.1016/S0039-6109(16)35130-1
    1. Møller UK, Streym S, Mosekilde L, Heickendorff L, Flyvbjerg A, Frystyk J, et al. Changes in calcitropic hormones, bone markers and insulin-like growth factor I (IGF-I) during pregnancy and postpartum: a controlled cohort study. Osteoporos Int (2013) 24(4):1307–20.10.1007/s00198-012-2062-2
    1. Saran S, Gupta BS, Philip R, Singh KS, Bende SA, Agroiya P, et al. Effect of hypothyroidism on female reproductive hormones. Indian J Endocrinol Metab (2016) 20(1):108–13.10.4103/2230-8210.172245
    1. Santosh UP, Sudhakar R. Incidence of hypothyroidism in Meniere’s disease. J Clin Diagn Res (2016) 10(5):6–8.10.7860/JCDR/2016/17587.7759
    1. Neuhauser HK, von Brevern M, Radtke A, Lezius F, Feldmann M, Ziese T, et al. Epidemiology of vestibular vertigo a neurotologic survey of the general population. Neurology (2005) 65(6):898–904.10.1212/01.wnl.0000175987.59991.3d
    1. Edlow AG, Bartz D. Hormonal contraceptive options for women with headache: a review of the evidence. Rev Obstet Gynecol (2010) 3(2):55–65.
    1. Osta RE, Almont T, Diligent C, Hubert N, Eschwège P, Hubert J. Anabolic steroids abuse and male infertility. Basic Clin Androl (2016) 26(2):2.10.1186/s12610-016-0029-4
    1. Jia H, Sullivan CT, McCoy SC, Yarrow JF, Morrow M, Borst SE. Review of health risks of low testosterone and testosterone administration. World J Clin Cases (2015) 3(4):338–44.10.12998/wjcc.v3.i4.338
    1. Furman JM, Marcus DA, Balaban CD. Migrainous vertigo: development of a pathogenetic model and structured diagnostic interview. Curr Opin Neurol (2003) 16(1):5–13.10.1097/00019052-200302000-00002
    1. Jepsen P, Johnsen SP, Gillman MW. Interpretation of observational studies. Heart (2004) 90(8):956–60.10.1136/hrt.2003.017269
    1. Bain J. The many faces of testosterone. Clin Interv Aging (2007) 2(4):567–76.10.2147/CIA.S1417

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