|Year : 2019 | Volume
| Issue : 1 | Page : 18-22
Menstrual cycle effects on otolith-ocular reflex pathway
Sujeet Kumar Sinha, Manisha Sahu
Department of Audiology, All India Institute of Speech and Hearing, Mysore, Karnataka, India
|Date of Submission||15-Mar-2018|
|Date of Decision||02-Jun-2018|
|Date of Acceptance||27-Feb-2019|
|Date of Web Publication||28-Jun-2019|
Sujeet Kumar Sinha
Department of Audiology, All India Institute of Speech and Hearing, Mysore - 570 006, Karnataka
Source of Support: None, Conflict of Interest: None
Introduction: Studies have shown morphological changes in the vestibule leading to alter the physiological changes during menstruation. And during the cycle, the level of hormones differs during different phases of the cycle. Hence, it is important to study the hormonal influences in the otolith-ocular pathways of females as the ocular vestibular evoked myogenic potentials (oVEMP) results might be interpreted wrongly if the different phase of the menstrual cycle affects the oVEMP results. The aim of the present study was to measure the changes in latency and amplitude of oVEMP test during three phases of the mensuration cycle. Materials and Methods: Twenty healthy females volunteers participated for the study and their otolith-ocular system was evaluated using oVEMP in three phases of the same cycle, i.e., menstruation phase (day 1–4), ovulation phase (day 12–17), and luteal phase (day 22–28). Results: oVEMP was present for all the participants in all the three phase of the menstrual cycle. For the obtained nonnormal data, nonparametric Freidman's Chi-square test was administered. The results showed no significant difference in latency or amplitude parameters of oVEMP across three recordings in participants, indicating that there was no significant effect of hormonal changes on oVEMPs recordings in females. Conclusions: It can be concluded that while assessing the vestibular system through an electrophysiological test like oVEMP, will not render differences in females based on their phases of menstruation cycles.
Keywords: Hormonal influences, menstruation cycle, oVEMP, vestibular system
|How to cite this article:|
Sinha SK, Sahu M. Menstrual cycle effects on otolith-ocular reflex pathway. J Indian Speech Language Hearing Assoc 2019;33:18-22
|How to cite this URL:|
Sinha SK, Sahu M. Menstrual cycle effects on otolith-ocular reflex pathway. J Indian Speech Language Hearing Assoc [serial online] 2019 [cited 2019 Sep 19];33:18-22. Available from: http://www.jisha.org/text.asp?2019/33/1/18/261753
| Introduction|| |
A fluctuation in the level of gonadal hormones leads to various changes in the human body. In females, the menstrual cycle is the regular natural changes that occurs in the uterus and ovaries that make pregnancy possible. And during the cycle, levels of hormones differ during different phases of the cycle. Objectively, the spatial ability of women during menstrual phase had higher scores when compared with mid-luteal phase. Furthermore, the menstrual cycle phases have stronger effects on hypothalamus–pituitary–adrenal axis which are involved in several behavioral, circulatory, endocrine, and immune disorders.
The effect of ovarian steroid hormones over cortical excitability has also been established. Not only at the cortical levels, but also the hormonal fluctuations increases laxity at the level of muscles and ligaments too. Assessing olfactory sensitivity, blood pressure, heart rate, body temperature, nasal airflow, and respiration rate, during different phases of menstruation cycle has also shown fluctuation in scores, over different phases. Variations in visual and olfactory thresholds, during the cycle, have also been reported in literature. Where sensitivity to painful stimuli has seen to be lowered during premenstrual phase of the cycle. Whereas, while assessing vocal perturbations, magnitude of vocal perturbation was notably different from other phases of cycle, for most of the females. These findings indicate changes in motor and sensory processes involved in laryngeal control.
Walpurger et al. reported, that early components of ERP in women in the luteal phase have diminished cortical arousal responses indicating an attenuated orienting response. These changes were significantly correlated with estradiol as well as progesterone levels. Whereas, the later ERP components, the N2 latency was shorter during menses as compared to the other two phases. In sum, this study documents changes in auditory ERPs across the menstrual cycle with the most prominent changes occurring during the luteal phase. Latency of P300 during the ovulatory period was observed to be more than rest two phases. In the same study, authors also recorded ABR in different phases of menstrual cycle and reported that the amplitude of waves I and III was found to be less during menses along with decreased wave V latency and III-V interpeak latency.
A plethora of studies has reported abnormal vestibular test findings during the different phases of the menstrual cycle. Ishi et al. reported significant differences before and after menstrual period in the calibration latency in the right eye, saccadic Movements precision in the left eye, and an abnormal directional preponderance in all their female participants. The abnormal findings in different tests of electronystagmography (ENG) suggest changes in the vestibular system during the menstrual cycle in females. Abdel Nabi et al. reported spontaneous nystagmus in four female participants, positional direction fixed nystagmus in six female participants, abnormal caloric test findings in nine female participants (four with the presence of directional preponderance, three with canal paresis, and two with both) 1 week before the menstrual phase. These changes in inner ear may be present due to the risen estrogen, progesterone, and aldosterone level followed by retention of salt and water during the premenstrual period, affecting inner ear metabolism.
Studies have also shown that during menstruation, female sex hormones alter the vestibule morphologically by changing the endolymphatic pressure and blood viscosity. Furthermore, few females have reported giddiness and vertigo during premenstruation, mainly in the luteal phase. While measuring visual-vestibular interactions, it was found that menstrual phase had no significant effect on optokinetic functions but, it did significantly affect lateral sway, indicating hormonal influences on the vestibular system. The above-mentioned studies have reported differences in the ENG recordings, during different phases of the menstrual cycle. However, the ENG test assesses the function of the semi-circular canals only. Since the vestibular system consists of multiple structures including utricle and saccule, it would be interesting to see whether similar effects are seen in the utricle also.
Hence, the objective of the present study was to assess the latency and amplitude parameters of oVEMP during the three phases of the menstrual cycle in young females.
| Methods|| |
Twenty adult females (40 ears) within the age range of 18–23 years with the mean age being 20 years participated for the study. All the participants had a regular menstrual cycle without any complications or disorders related to menstruation. The help of a gynecologist was taken to ensure the regular menstrual cycle in all the participants. All the participants had bilateral normal hearing sensitivity and absence of middle ear pathology. None of the participants had any neurological problems or presence or history of any vestibular disorders. All the participants were informed about the purpose of the study, and an informed consent was obtained from all the participants.
A two-channel Inventis piano diagnostic audiometer with the transducers TDH-39 headphone (Telephonic 815 broad hollow road, Farmingdale, New York 11735) and B-71 bone vibrator (Radioear, KIMMETRICS, Smithberger, MD 21783) were used to measure air conduction and bone conduction threshold, respectively. Grason Stadler Inc., Tympstar system (GSI VAISYS Healthcare, Wisconsin, USA) was used to measure middle ear function. Otoacoustic emission was measured using ILOv6 software (Otodynamics Ltd., UK). Vestibular evoked myogenic potentials were recorded using Bio-logic navigator pro auditory evoked potential unit, with an insert ER-3A earphone (EtymoticResarch, Inc., Elk Grove Village, II, USA).
For each of the participants, tests were carried out at three different phases during the menstrual cycle. The first phase was recorded between 1st and 4th day (menstruation phase), second recording was taken between 12th and 17th day (ovulation phase) following to it the last recording was taken between 22nd and 28th day (luteal phase).
Pure tone audiometry
Participant's pure tone thresholds were obtained using modified Hughson-Westlake Method, for the octave frequencies between 250 Hz and 8000 Hz for air conduction threshold and 250 Hz to 4000 Hz for bone conduction threshold.
Immittance audiometry was carried out to obtain tympanogram using 226 Hz probe tone, and pressure was altered from −400 to +200 dapa. Acoustic reflexes were measured to obtain the reflex thresholds for 500, 1000, and 2000 Hz and 4000 Hz frequencies.
Ocular-vestibular myogenic potential
The electrophysiological test, oVEMP was recorded for all the subjects with 500 Hz tone burst stimuli (Blackman window) using Bio-logic navigator pro auditory evoked potential unit, since this stimulus gives better amplitude compared to clicks. Gold-plated electrodes were used to record the responses. Noninverting electrode was placed at approximately 1 cm inferior to the lower eyelids and inverting electrodes were placed inferior to noninverting electrode and the ground electrode was placed at high forehead. Facial skin was cleaned before the placement of electrode using NuPrep skin abrasive. Electrode impedance was checked to ensure that the absolute impedance of each electrode site was within 5kohms and the inter-electrode impedance was within 2kohms. The responses were filtered from 1 Hz to 1000 Hz with the analysis time kept as 64 ms with the pre-stimulus of 10 ms. A total of 150 stimuli were presented at a repetition rate of 5.1/s in rarefaction polarity with an intensity of 95 dBnHL. Here, the responses were recorded in the contralateral mode, where the electrodes are placed contralateral to the stimulus presented. During the recording, individuals were instructed to stare straight ahead and then to look up as high as they can at a fixed point, since oVEMP recording was done in an upper gaze direction to activate the inferior oblique through contraction by looking up. The upward gaze for all the participant was fixed at 30° angle. Individuals were seated in an upright position. Upper gaze monitoring was assured. Responses were analyzed based on the stimulus ear, i.e., right ear recording had stimulus in the right ear and recording on the left eye muscles since the oVEMP is an excitatory response that we record from the extraocular muscle which is contralateral response.
| Results|| |
The latency of n1, p1, and n2 waveform peaks were analyzed along with the amplitude of n1-p1 and p1-n2 waveform for all the participants. Recordings were done in three different phases during the menstrual cycle, and oVEMPs were present in all the participants for all the three recordings.
[Figure 1]a,[Figure 1]b,[Figure 1]c,[Figure 1]d,[Figure 1]e,[Figure 1]f shows the individual and grand averaged waveform of oVEMPs recorded for the first phase, second phase, and third phase respectively for right and left ear.
|Figure 1: The individual and grand averaged oVEMP recorded waveforms of 20 individuals. All the waveforms are shown with the 10 ms prestimulus. (a) The right ear waveforms recorded during the follicular phase of the menstrual cycle and (b) the same phase of menstrual cycle recorded waveforms of left ear. (c and d) The recorded waveforms of right and left ear, respectively during the luteal phase; (e and f) the recorded waveforms of right and left ear during the menstrual phase of the menstrual cycle|
Click here to view
The latency of n1, p1, and n2 wave peaks and amplitude of n1-p1 and p1-n2 wave complex for all three recordings was noted. The mean and the standard deviation were calculated using descriptive statistics for latency of p1, n1, and p2 paks and amplitude of n1-p1 and p1-n2 complex. The mean and the standard deviation for the same are given in [Table 1].
|Table 1: Mean and standard deviation for latency and amplitude parameters of ocular vestibular evoked myogenic potentials|
Click here to view
It can be seen from [Table 1] that the mean amplitude of n1-p1 and p1-n2 complex was more in right ear for the second recording as compared to the first and third, whereas right ear mean amplitude of n1-p1 and p1-n2 complex was lesser for the first recording compared with the other two recordings. It can also be seen from [Table 1] that there was not much difefrences for the latencies values between the three recordings.
Shapiro–Wilk test of normality was carried out, and a nonnormal distribution of data was found (P < 0.05). Hence, a nonparametric Friedman's Chi-square test of differences among three recordings for different oVEMPs parameters was administered. Chi-square value rendered by the Friedman's Chi-square test for n1 latency of right ear was1.947 which was not significant (P > 0.05) and Chi-square value rendered for n1 latency of left ear was0.986 which was also statistically not significant (P > 0.05). Chi-square values obtained for p1-latency using Freidman's Chi-square test in right and left ear were 0.105 and 0.720 which shows both ears p1 latency was not significant (P > 0.05). Chi-square test rendered Chi-square value of 0.329 for n2 latency of the right ear which was not significant (P > 0.05) and Chi-square value of 1.368 was obtained for n2 latency of left ear which was also not significant (P > 0.05).
Chi-square test rendered Chi-square value of 2.632 for right ear for n1-p1 amplitude which was not significant (P > 0.05) and Chi-square value obtained for n1-p1amplitude for left ear was 0.421 which was also statistically not significant (P > 0.05). Chi-square value obtained by the Chi-square test for p1n2 amplitude for right ear was 1.520 which was not significant (P > 0.05). Chi-square value of 0.000 was rendered by the Chi-square test for p1-n2 amplitude for left ear which was not significant (P > 0.005). To summarize, there was no significant difference in latency or amplitude parameters of oVEMP across three recordings in participants, indicating that there was no significant effect of hormonal changes on oVEMPs recordings in females.
| Discussion|| |
The current clinical vestibular evaluation method oVEMP helps us understand the integrity of utricle and superior vestibular nerve. Thus understanding the results in the context of hormonal fluctuations during the menstrual cycle and its effect on vestibular functioning is important for differential diagnosis of the vestibular disorders. In spite of well-known effects of hormonal fluctuations in inner ear physiology, the present study indicates no difference in oVEMP in three phases of the menstrual cycle. The present study compared the ocular vestibular evoked myogenic responses in the three phases of menstruation which consists of menstrual phase (1st–4th day), ovulation phase (12th–17th day) and luteal phase (22nd–28th day) by utilizing oVEMP and revealed not so significant differences in latency or the amplitude parameters of oVEMP.
The results of the present study do not support the findings of the studies which evaluated the auditory system and have found various effects of changes in the hormonal levels. Researchers have shown changes in audiological findings such as reduced auditory sensitivity during the first phase of menstruation, increased latencies for click-evoked auditory brainstem responses during mid-cycle, enhanced amplitude, and reduced latencies in speech-evoked auditory brainstem responses in the first phase and mid-luteal phase of menstruation. Therefore, it was expected to observe similar altered responses in vestibular findings too as the vestibular system and the auditory system share the same common cavity.
However, in other studies related to the vestibular system, they have shown that the postural stability of the females is affected during the different phases of the menstruation cycle., Darlington et al. demonstrated that hormonal changes taking place during menstrual cycle do not have a significant effect on optokinetic function. However, the hormonal influences during menstrual cycle do affect the postural ability in lateral sway and not the anterior-posterior sway. The variation in the lateral sway does not appear to be directly related to the vestibular system rather arising from multiple other sources. Hence, we hypothesize that hormonal changes occurring during the menstrual cycle may not influence the ocular vestibular evoked myogenic potentials test findings in female participants during different phases of menstrual cycle.
The absence of cyclical amplitude or latency changes in oVEMP over the course of the menstrual cycle may seem surprising. Studies of puretone thresholds, auditory brainstem responses, and spontaneous otoacoustic emissions have demonstrated a change during a different phase of the menstrual cycles.,,,, The authors of these studies have not explained the basis of the change in different test results during the different phase of the menstrual cycle; however, it has been correlated with changing hormone level. It is also known that the I–V interwave interval of auditory brainstem responses is significantly shorter during midcycle in normal-cycling females.,,, Thus, one can expect similar changes in latency and amplitude in oVEMP also in normal cycling females.
The inner ear contains both cochlea and vestibular system and both the systems share a common cavity and endolymph. Hence, any change in fluid system during the menstrual cycle will affect both the cochlear and vestibular functions. However, there are studies, to prove that the potentials which are generated from the cochlea especially otoacoustic emissions (both TEOAE and DPOAE) remain unchanged during the different phase of the menstrual cycle.,, Thus, one can expect that although there might be changes in the endolymph during the different phases of the menstrual cycle, but the changes may not be large enough to bring about a change in the latency or amplitude of oVEMP.
| Conclusions|| |
In our present study, there was no significant difference seen in latencies of oVEMP peaks n1, p1 and n2. Neither did any variation in peak to peak amplitude of n1-p1 complex and p1-n2 complex was observed across the three phases of menstruation. Even though gender differences is one of the major concerns in the interpretation of auditory evoked potentials and auditory evoked vestibular potentials, hormonal differences due to menstruation show no variations. Hence, it can be concluded that while assessing the vestibular system through an electrophysiological test like oVEMP, will not render differences in females based on their phases of menstruation cycles.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Silverthorn DU, Ober WC, Garrison CW, Silverthorn AC, Johnson BR. Human Physiology: An Integrated Approach. San Francisco, CA, USA: Pearson/Benjamin Cummings; 2009.
Hausmann M, Slabbekoorn D, Van Goozen SH, Cohen-Kettenis PT, Güntürkün O. Sex hormones affect spatial abilities during the menstrual cycle. Behav Neurosci 2000;114:1245-50.
Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH. Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom Med 1999;61:154-62.
Eiling E, Bryant AL, Petersen W, Murphy A, Hohmann E. Effects of menstrual-cycle hormone fluctuations on musculotendinous stiffness and knee joint laxity. Knee Surg Sports Traumatol Arthrosc 2007;15:126-32.
Doty RL, Snyder PJ, Huggins GR, Lowry LD. Endocrine, cardiovascular, and psychological correlated of olfactory sensitivity changes during the human menstrual cycle. J Comp Physiol Psychol 1981;95:45-60.
Parlee MB. Menstrual rhythms in sensory processes: A review of fluctuations in vision, olfaction, audition, taste, and touch. Psychol Bull 1983;93:539-48.
Higgins MB, Saxman JH. Variations in vocal frequency perturbation across the menstrual cycle. J Voice 1989;3:233-43.
Walpurger V, Pietrowsky R, Kirschbaum C, Wolf OT. Effects of the menstrual cycle on auditory event-related potentials. Horm Behav 2004;46:600-6.
Tasman A, Hahn T, Maiste A. Menstrual cycle synchronized changes in brain stem auditory evoked potentials and visual evoked potentials. Biol Psychiatry 1999;45:1516-9.
Ishii C, Nishino LK, Campos CA. Vestibular characterization in the menstrual cycle. Braz J Otorhinolaryngol 2009;75:375-80.
Abdel Nabi EA, Motawee E, Lasheen N, Taha A. A study of vertigo and dizziness in the premenstrual period. J Laryngol Otol 1984;98:273-5.
Darlington CL, Ross A, King J, Smith PF. Menstrual cycle effects on postural stability but not optokinetic function. Neurosci Lett 2001;307:147-50.
Carhart R, Jerger J. Preferred method for clinical determination of pure-tone thresholds. J Speech Hear Disord 1959;24:330-45.
Souaid JP, Rappaport JM. Fluctuating sensorineural hearing loss associated with the menstrual cycle. J Otolaryngol 2001;30:246-50.
Avizheh S, Akbari M, Fatahi J, Pourbakht A, Jalaie S, Sheikholeslami K. Auditory brainstem responses during menstrual cycle and pregnancy. Aud Vestib Res 2015;24:217-23.
Prabhu P, Banerjee N, Anil A, Abdulla A. Role of sex hormones produced during menstrual cycle on brainstem encoding of speech stimulus. Eur Arch Otorhinolaryngol 2016;273:3647-50.
Shahin A, Ulas YH, Deniz E. Effects of menstrual periods on postural stability in eumenorrheic female group. Sci Res Essays 2012;7:3053-7.
Miller NH, Gould WJ. Fluctuating sensorineural hearing impairment associated with the menstrual cycle. J Aud Res 1967;7:373-85.
Picton TW, Stapells DR, Campbell KB. Auditory evoked potentials from the human cochlea and brainstem. J Otolaryngol Suppl 1981;9:1-41.
Davis MJ, Ahroon WA. Fluctuations in susceptibility to noise-induced temporary threshold shift as influenced by the menstrual cycle. J Aud Res 1982;22:173-87.
Dehan CP, Jerger J. Analysis of gender differences in the auditory brainstem response. Laryngoscope 1990;100:18-24.
Baker MA, Weiler EM. Sex of listener and hormonal correlates of auditory thresholds. Br J Audiol 1977;11:65-8.
Elkind-Hirsch KE, Stoner WR, Stach BA, Jerger JF. Estrogen influences auditory brainstem responses during the normal menstrual cycle. Hear Res 1992;60:143-8.
Elkind-Hirsch KE, Wallace E, Malinak LR, Jerger JJ. Sex hormones regulate ABR latency. Otolaryngol Head Neck Surg 1994;110:46-52.
Yellin MW, Stillman RD. Otoacoustic emissions in normal-cycling females. J Am Acad Audiol 1999;10:400-8.
Arruda PO, Silva IM. Study of otoacoustic emissions during the female hormonal cycle. Braz J Otorhinolaryngol 2008;74:106-11.
Yadav A, Tandon OP, Vaney N. Long latency auditory evoked responses in ovulatory and anovulatory menstrual cycle. Indian J Physiol Pharmacol 2003;47:179-84.