525590

research-article2014

AORXXX10.1177/0003489414525590Annals of Otology, Rhinology & LaryngologyStevens and Hullar

Article

Improvement in Sensorineural Hearing Loss During Pregnancy

Annals of Otology, Rhinology & Laryngology 2014, Vol. 123(9) 614­–618 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0003489414525590 aor.sagepub.com

Madelyn N. Stevens, BA1 and Timothy E. Hullar, MD1

Abstract Objective: Hearing loss is known to occur in some pregnant women, but improvement in sensorineural thresholds has not been audiometrically characterized. Here, we describe a patient with a history of Ménière’s disease and vestibular migraine who experienced temporary recovery of her hearing during pregnancy. Methods: Audiograms were obtained from a 31-year-old female over the course of 2 successive pregnancies. Results: Audiograms revealed a substantial improvement in hearing by the third trimester during each pregnancy, with a rapid return to baseline thresholds after delivery. Conclusion: This case is unique in documenting improvements in hearing thresholds during pregnancy and substantiates the effects of hormonal changes on hearing thresholds in humans. It raises the intriguing possibility of hormonal therapy as a treatment for sensorineural hearing loss in specific clinical situations. Keywords audiogram, auditory, hearing, hormone, Ménière’s, migraine, pregnancy, threshold, vestibular

Several reports have indicated that hearing acuity can worsen during pregnancy, but improvements in hearing among pregnant women have not previously been characterized audiometrically.1-3 Here, we describe a patient with Ménière’s disease and migraine-associated vertigo who had temporary but significant hearing improvement during each of her 2 pregnancies. A 31-year-old nulligravida presented with a 7-month history of asymmetric sensorineural hearing loss with episodic fullness, tinnitus, and vertigo 1 to 2 times per week, satisfying the criteria for definite Ménière’s disease.4 Her auditory symptoms were worse on the left side. More recently, her auditory symptoms had stabilized but she continued to have dizzy spells, associated with migraine headaches, at about the same frequency. These worsened with caffeine intake and menses and were accompanied by left-sided tinnitus, scotomata, imbalance, phonophobia, photophobia, and nausea, meeting the criteria for definite migraine-associated vertigo.5 Her medications included triamterene/hydrochlorothiazide 37.5/25 mg qd, diazepam 2 mg tid, and paroxetine 20 mg qd. Prior to presentation, for her migraines she had begun topiramate 100 mg qd and sumatriptan 100 mg prn without side effects. She wore hearing aids and followed a low-salt diet. She became pregnant and stopped all medications except paroxetine. She noted an increase in her symptoms of migraine-associated dizziness after stopping her topiramate yet felt that they were still less than before she began the

medication. Starting about the third month of gestation, her hearing on the right side markedly improved (G1P0, 5-31 weeks, Figure 1). This improvement was significant enough that she ceased using her hearing aid on that side. Within weeks of delivery, her right-sided hearing decreased rapidly. This did not improve with a course of prednisone and she resumed wearing her right hearing aid. Her migraine symptoms subsequently worsened to a frequency of twice per week, leading her to resume use of topiramate and prn sumatriptan, but she did not restart her diuretic. She subsequently switched from topiramate to amitriptyline, which gave her better control of her migraines. She became pregnant a second time approximately 2 years after delivering her first child. She again reported substantial subjective improvement in hearing on the right side at about the end of the first trimester and stopped using her hearing aid on that side. This improvement was confirmed with an audiogram at 24 weeks of gestation (G1P1, 21 months postpartum to G2P1, 24 weeks gestation, Figure 1). 1

Department of Otolaryngology–Head and Neck Surgery, Washington University School of Medicine, St. Louis, Missouri, USA Corresponding Author: Timothy E. Hullar, MD, Department of Otolaryngology–Head and Neck Surgery, Washington University School of Medicine, 660 South Euclid Avenue #8115, St. Louis, MO 63110, USA. Email: [email protected]

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Figure 1.  Pure-tone audiograms obtained during each of 2 successive pregnancies in a patient with Ménière’s disease. G (gravida): number of pregnancies; P (para): number of deliveries. Word recognition score (right ear/left ear, %): G1P0, 5 weeks gestation: 92/80; G1P0, 31 weeks gestation: 96/80; G1P1, 8 weeks postpartum: 96/72; G1P1, 21 months postpartum: 88/58; G1P2, 24 weeks gestation: 96/56; G2P2, 8 weeks postpartum: 84/72.

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She did not stop her amitriptyline and suffered only 1 migraine during this pregnancy. Within the first 5 days after a full-term delivery, however, she again noted a precipitous decline in her hearing on the right and resumed use of her hearing aid on that side. Her hearing has remained poor but stable since then. The frequency of her migraines also increased after delivery, but this resolved when she restarted her amitriptyline. Although her pure-tone thresholds varied significantly with pregnancy, her word recognition scores remained good throughout her clinical course.

Discussion We audiometrically documented spontaneous improvement in hearing during each of 2 successive pregnancies, with an almost immediate return to poor thresholds following delivery, in a woman meeting clinical criteria for Ménière’s disease and vestibular-associated migraine. This observation may shed light on the underlying causes and possible treatment of sensorineural hearing loss, particularly in the setting of patients with symptoms of endolymphatic hydrops and migraine. Several studies have indicated a relationship of hormonal levels, particularly estrogen, to hearing acuity.3 Otoacoustic emissions and auditory brainstem responses indicate a small increase in hearing sensitivity around ovulation, when estrogen levels are elevated.6 Hearing can worsen around menses7,8 and after menopause, when estrogen levels are depressed.9 Some studies have found that postmenopausal women taking estrogen replacement therapy have somewhat better hearing thresholds, particularly at high frequencies, than those who do not.10,11 Patients with Turner’s syndrome, who have deficiencies of estrogen production, have poorer auditory sensitivity than normal subjects.12 Estrogen appears to have an otoprotective effect against both noise trauma and aging.13,14 These observations suggest that higher estrogen levels may be associated with better hearing, although a more complicated pathway dependent on relative levels of several hormones such as antidiuretic hormone, thyroid hormone, and progesterone, may also be responsible.11,15 Estrogen receptors are present in the inner and outer hair cells as well as spiral ganglion cells, providing a possible direct pathway explaining the effects of pregnancy on hearing in the patient described here.13 Other possible mechanisms include fluid shifts and immunomodulation. Estrogen has profound effects on fluid regulation through its effects on arginine vasopressin (AVP), the renin-angiotensin-aldosterone system, and atrial natriuretic peptide.16,17 The inner ear contains aquaporin receptors, the target of AVP, which could allow estrogen to affect the severity of endolymphatic hydrops.18

Pregnancy also influences the function of the immune system in order for the mother’s body to tolerate the semiallogeneic fetus. Complex pathways contribute to a downregulation of the immune system, with estrogen specifically involved in inhibiting B-cell hematopoiesis.19 Some evidence indicates that Ménière’s disease is responsive to treatment with immunosuppressive steroids, suggesting that immunomodulation induced by pregnancy might be another contributor to improvement of hearing in our patient.20 Our patient’s case history comprises a single-subject crossover trial, repeated twice with similar results, offering strong evidence that the relationship of her pregnancies to her hearing improvements is not coincidental. Her audiometric results shown here correspond well to a previous report describing a subjective improvement of Ménière’s symptoms while pregnant.15 (One other report described severe nausea and vertigo during the first trimester of 2 successive pregnancies in a woman with Ménière’s, but no episodic changes in hearing were reported and hyperemesis gravidarum is a competing explanation for her symptoms.21) Her clinical course suggests that she initially had Ménière’s in the left ear, which had then become “burned out” with symptoms still occurring about twice per week on the right. This greater initial degree of hearing loss on the left may be the explanation for why its thresholds did not improve with pregnancy. Changes in our patient’s medical regimen are unlikely to be a good alternate explanation for her variation in hearing thresholds, as during both pregnancies, her hearing improved only after the first trimester (long after stopping her medications) and worsened after delivery but before she resumed her usual medications. Indeed, there is little evidence that a thiazide diuretic or anticonvulsant such as she was taking can directly affect hearing.22,23 Our patient’s initial symptoms of episodic tinnitus, vertigo, and hearing loss were typical of Ménière’s disease, but later, her hearing loss became stable and her episodes were limited to vertigo associated with her migraines (with hearing changing only over a long time course when it improved with pregnancy). Ménière’s and migraine-associated vertigo have similar symptoms, and about a quarter of patients meet clinical criteria for both diagnoses, as seen in our patient here.24 Our patient’s changes in hearing with pregnancy might plausibly be related to either condition. Symptoms of Ménière’s worsen during the late luteal phase as estrogen levels are dropping, just as occurred in our patient at the end of her pregnancies.15,25 Conversely, symptoms of Ménière’s disease can improve with glucocorticoid administration, an effect that may be mediated by the same receptors as sex steroids such as estrogen.20,26 In patients with migraine, drops in estrogen levels during the late luteal phase have been implicated in worsening symptoms while elevated levels of estrogen tend to reduce the frequency and severity of migraines during pregnancy.27,28

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Stevens and Hullar The association of hearing improvement with pregnancy in this patient supports the intriguing possibility of treating hearing loss in some patients with Ménière’s or migraineassociated vertigo by managing their levels of sex steroids. This has previously been tried using oral contraceptive pills, with varying success.15 Case reports have also suggested that treatment with gonadotropin-releasing hormone analogs such as leuprolide and nafarelin, which cause several weeks of increased estrogen secretion (“flare effect”) before eventually downregulating sex steroid secretion, may also be effective.29,30 Authors’ Note Both authors participated in conception, data collection, data analysis, and writing of the article and both reviewed and approved it for submission.

Acknowledgments We gratefully acknowledge the assistance of Kelle Moley, MD, Department of Obstetrics and Gynecology, Washington University School of Medicine.

Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Supported in part by grant NIH NIDCD T35 008675.

References 1. Sennaroglu G, Belgin E. Audiological findings in pregnancy. J Laryngol Otol. 2001;115(8):617-621. 2. Schmidt PM, Flores Fda T, Rossi AG, Silveira AF. Hearing and vestibular complaints during pregnancy. Braz J Otorhinolaryngol. 2010;76(1):29-33. 3. 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. doi:10.1016/j.neuroscience.2008.02.077. 4. Monsell EM, Balkany TA, Gates GA, Goldenberg RA, Meyerhoff WL, House JW. Committee on Hearing and Equilibrium guidelines for the diagnosis and evaluation of therapy in Meniere’s disease. Otolaryngol Head Neck Surg. 1995;113:181-185. 5. Radtke A, Neuhauser H, von Brevern M, Hottenrott T, Lempert T. Vestibular migraine—validity of clinical diagnostic criteria. Cephalalgia. 2011;31(8):906-913. doi:10.1177/0333102411405228. 6. Al-Mana D, Ceranic B, Djahanbakhch O, Luxon LM. Alteration in auditory function during the ovarian cycle. Hear Res. 2010;268(1-2):114-122. doi:10.1016/j. heares.2010.05.007.

7. Miller M, Gould W. Fluctuating sensorineural hearing impairment associated with the menstrual cycle. J Aud Res. 1967;7(4):373-385. 8. Souaid JP, Rappaport JM. Fluctuating sensorineural hearing loss associated with the menstrual cycle. J Otolaryngol. 2001;30(4):246-250. 9. Hederstierna C, Hultcrantz M, Collins A, Rosenhall U. The menopause triggers hearing decline in healthy women. Hear Res. 2010;259(1-2):31-35. doi:10.1016/j.heares.2009.09.009. 10. Kilicdag EB, Yavuz H, Bagis T, Tarim E, Erkan AN, Kazanci F. Effects of estrogen therapy on hearing in postmenopausal women. Am J Obstet Gynecol. 2004;190(1):77-82. doi:10.1016/j.ajog.2003.06.001. 11. Guimaraes P, Frisina ST, Mapes F, Tadros SF, Frisina DR, Frisina RD. Progestin negatively affects hearing in aged women. Proc Natl Acad Sci U S A. 2006;103(38):1424614249. doi:10.1073/pnas.0606891103. 12. Hederstierna C, Hultcrantz M, Rosenhall U. Estrogen and hearing from a clinical point of view; characteristics of auditory function in women with Turner syndrome. Hear Res. 2009;252(1-2):3-8. doi:10.1016/j.heares.2008.11.006. 13. Meltser I, Tahera Y, Simpson E, et al. Estrogen receptor beta protects against acoustic trauma in mice. J Clin Invest. 2008;118(4):1563-1570. doi:10.1172/JCI32796. 14. Nolan LS, Maier H, Hermans-Borgmeyer I, et al. Estrogenrelated receptor gamma and hearing function: evidence of a role in humans and mice. Neurobiol Aging. 2013;34(8):2077. e1-9. doi:10.1016/j.neurobiolaging.2013.02.009. 15. Andrews JC, Honrubia V. Premenstrual exacerbation of Meniere’s disease revisited. Otolaryngol Clin North Am. 2010;43(5):1029-1040. doi:10.1016/j.otc.2010.05.012. 16. Stachenfeld NS, Keefe DL. Estrogen effects on osmotic regulation of AVP and fluid balance. Am J Physiol Endocrinol Metab. 2002;283(4):E711-E721. doi:10.1152/ ajpendo.00192.2002. 17. Stachenfeld NS, Keefe DL, Palter SF. Estrogen and progesterone effects on transcapillary fluid dynamics. Am J Physiol Regul Integr Comp Physiol. 2001;281(4):R1319-R1329. 18. Eckhard A, Gleiser C, Arnold H, et al. Water channel proteins in the inner ear and their link to hearing impairment and deafness. Mol Aspects Med. 2012;33(5-6):612-637. doi:10.1016/j. mam.2012.06.004. 19. Arck PC, Hecher K. Fetomaternal immune cross-talk and its consequences for maternal and offspring’s health. Nat Med. 2013;19(5):548-556. doi:10.1038/nm.3160. 20. Phillips JS, Westerberg B. Intratympanic steroids for Meniere’s disease or syndrome. Cochrane Database Syst Rev. 2011;(7):CD008514. doi:10.1002/14651858.CD008514.pub2. 21. Uchide K, Suzuki N, Takiguchi T, Terada S, Inoue M. The possible effect of pregnancy on Meniere’s disease. ORL J Otorhinolaryngol Relat Spec. 1997;59(5):292-295. 22. van Deelen GW, Huizing EH. Use of a diuretic (Dyazide®) in the treatment of Meniere’s disease. ORL J Otorhinolaryngol Relat Spec. 1986;48:287-292. 23. Radtke A, von Brevern M, Neuhauser H, Hottenrott T, Lempert T. Vestibular migraine: long-term followup of clinical symptoms and vestibulo-cochlear findings. Neurology. 2012;79(15):1607-1614. doi:10.1212/ WNL.0b013e31826e264f.

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24. Neff BA, Staab JP, Eggers SD, et al. Auditory and vestibular symptoms and chronic subjective dizziness in patients with Meniere’s disease, vestibular migraine, and Meniere’s disease with concomitant vestibular migraine. Otol Neurotol. 2012;33(7):1235-1244. doi:10.1097/MAO.0b013e31825d644a. 25. Morse GG, House JW. Changes in Meniere’s disease responses as a function of the menstrual cycle. Nurs Res. 2001;50(5):286-292. 26. Bourke CH, Harrell CS, Neigh GN. Stress-induced sex differences: adaptations mediated by the glucocorticoid receptor. Horm Behav. 2012;62(3):210-218. doi:10.1016/j. yhbeh.2012.02.024.

27. Tozer BS, Boatwright EA, David PS, et al. Prevention of migraine in women throughout the life span. Mayo Clin Proc. 2006;81(8):1086-1091; quiz 92. doi:10.4065/81.8.1086. 28. Digre KB. Headaches during pregnancy. Clin Obstet Gynecol. 2013;56(2):317-329. doi:10.1097/GRF.0b013e31828f25e6. 29. Price TM, Allen TC, Bowyer DL, Watson TA. Ablation of luteal phase symptoms of Meniere’s disease with leuprolide. Arch Otolaryngol Head Neck Surg. 1994;120(2):209-211. 30. Andreyko JL, Jaffe RB. Use of a gonadotropin-releasing hormone agonist analogue for treatment of cyclic auditory dysfunction. Obstet Gynecol. 1989;74(3, pt 2):506-509.

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Improvement in sensorineural hearing loss during pregnancy.

Hearing loss is known to occur in some pregnant women, but improvement in sensorineural thresholds has not been audiometrically characterized. Here, w...
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