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Figure.  Overall Framework of Auditory Paradigms and Stimuli Parameters
Overall Framework of Auditory Paradigms and Stimuli Parameters
Table 1.  Auditory Contributions to Postural Control in Healthy Adults
Auditory Contributions to Postural Control in Healthy Adults
Table 2.  Auditory Contributions to Postural Control in Clinical Populations
Auditory Contributions to Postural Control in Clinical Populations
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Maheu  M, Sharp  A, Landry  SP, Champoux  F.  Sensory reweighting after loss of auditory cues in healthy adults.  Gait Posture. 2017;53:151-154. doi:10.1016/j.gaitpost.2017.01.015PubMedGoogle ScholarCrossref
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Maheu  M, Behtani  L, Nooristani  M,  et al.  Vestibular function modulates the benefit of hearing aids in people with hearing loss during static postural control.  Ear Hear. 2019;40(6):1418-1424. doi:10.1097/AUD.0000000000000720PubMedGoogle ScholarCrossref
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Ross  JM, Balasubramaniam  R.  Auditory white noise reduces postural fluctuations even in the absence of vision.  Exp Brain Res. 2015;233(8):2357-2363. doi:10.1007/s00221-015-4304-yPubMedGoogle ScholarCrossref
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Ross  JM, Will  OJ, McGann  Z, Balasubramaniam  R.  Auditory white noise reduces age-related fluctuations in balance.  Neurosci Lett. 2016;630:216-221. doi:10.1016/j.neulet.2016.07.060PubMedGoogle ScholarCrossref
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Easton  RD, Greene  AJ, DiZio  P, Lackner  JR.  Auditory cues for orientation and postural control in sighted and congenitally blind people.  Exp Brain Res. 1998;118(4):541-550. doi:10.1007/s002210050310PubMedGoogle ScholarCrossref
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Raper  SA, Soames  RW.  The influence of stationary auditory fields on postural sway behaviour in man.  Eur J Appl Physiol Occup Physiol. 1991;63(5):363-367. doi:10.1007/BF00364463PubMedGoogle ScholarCrossref
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Mainenti  MRM, De Oliveira  LF, De Melo Tavares De Lima  MA, Nadal  J.  Stabilometric signal analysis in tests with sound stimuli.  Exp Brain Res. 2007;181(2):229-236. doi:10.1007/s00221-007-0921-4PubMedGoogle ScholarCrossref
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Sioud  R, Khalifa  R, Houel  N.  Auditory cues behind congenitally blind subjects improve their balance control in bipedal upright posture.  Gait Posture. 2019;70:175-178. doi:10.1016/j.gaitpost.2019.03.004PubMedGoogle ScholarCrossref
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Gago  MF, Fernandes  V, Ferreira  J,  et al.  Role of the visual and auditory systems in postural stability in Alzheimer’s disease.  J Alzheimers Dis. 2015;46(2):441-449. doi:10.3233/JAD-150131PubMedGoogle ScholarCrossref
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Siedlecka  B, Sobera  M, Sikora  A, Drzewowska  I.  The influence of sounds on posture control.  Acta Bioeng Biomech. 2015;17(3):96-102.PubMedGoogle Scholar
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Soames  RW, Raper  SA.  The influence of moving auditory fields on postural sway behaviour in man.  Eur J Appl Physiol Occup Physiol. 1992;65(3):241-245. doi:10.1007/BF00705088PubMedGoogle ScholarCrossref
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Agaeva  MY, Altman  YA.  Effect of a sound stimulus on postural reactions.  Hum Physiol. 2005;31(5):511-514. doi:10.1007/s10747-005-0090-4Google ScholarCrossref
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Gandemer  L, Parseihian  G, Kronland-Martinet  R, Bourdin  C.  The influence of horizontally rotating sound on standing balance.  Exp Brain Res. 2014;232(12):3813-3820. doi:10.1007/s00221-014-4066-yPubMedGoogle ScholarCrossref
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Deviterne  D, Gauchard  GC, Jamet  M, Vançon  G, Perrin  PP.  Added cognitive load through rotary auditory stimulation can improve the quality of postural control in the elderly.  Brain Res Bull. 2005;64(6):487-492. doi:10.1016/j.brainresbull.2004.10.007PubMedGoogle ScholarCrossref
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Tanaka  T, Kojima  S, Takeda  H, Ino  S, Ifukube  T.  The influence of moving auditory stimuli on standing balance in healthy young adults and the elderly.  Ergonomics. 2001;44(15):1403-1412. doi:10.1080/00140130110110601PubMedGoogle ScholarCrossref
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Guigou  C, Toupet  M, Delemps  B, Heuschen  S, Aho  S, Bozorg Grayeli  A.  Effect of rotating auditory scene on postural control in normal subjects, patients with bilateral vestibulopathy, unilateral, or bilateral cochlear implants.  Front Neurol. 2018;9:972. doi:10.3389/fneur.2018.00972PubMedGoogle ScholarCrossref
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Rumalla  K, Karim  AM, Hullar  TE.  The effect of hearing aids on postural stability.  Laryngoscope. 2015;125(3):720-723. doi:10.1002/lary.24974PubMedGoogle ScholarCrossref
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Goodworth  AD, Mellodge  P, Peterka  RJ.  Stance width changes how sensory feedback is used for multisegmental balance control.  J Neurophysiol. 2014;112(3):525-542. doi:10.1152/jn.00490.2013PubMedGoogle ScholarCrossref
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Shumway-Cook  A, Horak  FB.  Assessing the influence of sensory interaction of balance. Suggestion from the field.  Phys Ther. 1986;66(10):1548-1550. doi:10.1093/ptj/66.10.1548PubMedGoogle ScholarCrossref
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Karim  AM, Rumalla  K, King  LA, Hullar  TE.  The effect of spatial auditory landmarks on ambulation.  Gait Posture. 2018;60:171-174. doi:10.1016/j.gaitpost.2017.12.003PubMedGoogle ScholarCrossref
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Lubetzky-Vilnai  A, McCoy  SW, Price  R, Ciol  MA.  Young adults largely depend on vision for postural control when standing on a BOSU ball but not on foam.  J Strength Cond Res. 2015;29(10):2907-2918. doi:10.1519/JSC.0000000000000935PubMedGoogle ScholarCrossref
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    Review
    March 12, 2020

    Auditory Input and Postural Control in Adults: A Narrative Review

    Author Affiliations
    • 1Steinhardt School of Culture, Education and Human Development, Department of Physical Therapy, New York University, New York
    • 2Steinhardt School of Culture, Education and Human Development, Department of Music and Performing Arts Professions, New York University, New York
    • 3Vestibular Rehabilitation, New York Eye and Ear Infirmary of Mount Sinai, New York
    • 4Department of Otolaryngology–Head and Neck Surgery, New York Eye and Ear Infirmary of Mount Sinai, New York
    JAMA Otolaryngol Head Neck Surg. Published online March 12, 2020. doi:10.1001/jamaoto.2020.0032
    Abstract

    Importance  An increase in the number of mechanistic studies targeting the association between sound and balance has been observed in recent years, but their results appear equivocal.

    Observations  A search of PubMed and the Cochrane Database of Systematic Reviews for English-language studies on auditory input and postural control published from database inception through October 31, 2019, yielded 28 articles for review. These articles included 18 (64%) studies of healthy adults, 1 (4%) of participants with Alzheimer disease, 2 (7%) of participants with congenital blindness, 3 (11%) of participants with vestibular loss, and 4 (14%) of participants with diverse levels of hearing loss. Studies varied by the type of audio stimuli (natural vs generated sounds), apparatus (speakers vs headphones), and movement of sounds (eg, stationary, rotational). Most balance measurements involved standing on the floor or foam with eyes open or closed during which sway amount or velocity was quantified. Stationary broadband sounds, including white or environmental noise, may improve balance, but the results regarding stationary pure tone were inconclusive. The implication of moving sounds varied by apparatus (typically destabilizing when headphones were used) and sensory loss (more destabilizing with vestibular or hearing loss but perhaps less with a unilateral cochlear implant).

    Conclusions and Relevance  Findings from this review suggest that stationary broadband noise can serve as an auditory anchor for balance primarily when projected via speakers and when the balance task is challenging. More research is needed that includes individuals with sensory loss and that tests paradigms using dynamic, ecologically valid sounds; clinicians should also consider auditory cues and the presence of hearing loss in balance and fall-risk assessments.

    Introduction

    Falls are the leading cause of fatal injuries in the United States, and they have important implications for quality of life.1 Previous studies have suggested that hearing loss is associated with reduced balance performance in adults2 with3 or without dizziness and could be a potentially modifiable risk factor for falls.4,5 Decreasing fall risk in individuals with hearing loss requires a better understanding of the mechanism underlying this association. Liu et al6 proposed that the association between hearing loss and balance problems may be mediated by an underlying subthreshold vestibular dysfunction even without vestibular symptoms. Other studies have suggested that auditory cues are needed for environmental awareness and that individuals with hearing loss develop substitution strategies,7,8 in which individuals depend on other sensory input (vision, vestibular, or somatosensory) or cognitive resources to maintain their balance.9

    Do auditory cues participate in the sensory integration process for postural control? In recent years, we have observed an increase in the number of mechanistic studies attempting to explain a possible independent association between sounds and postural control. Studies in this area spread across diverse research fields, including acoustics and psychoacoustics, audiology, otology and neurotology, movement sciences, psychology, and physical therapy. In this narrative review, we (1) define the terms used to describe the auditory aspects of postural control and sound paradigms, (2) describe the method used to study the association between auditory input and postural control, (3) summarize the findings regarding the implications of auditory input for standing postural control in healthy adults and individuals with sensory loss (such as vestibular or hearing loss), (4) propose a mechanism by which auditory cues are used for balance, and (5) provide recommendations for future research.

    Methods

    We searched PubMed and the Cochrane Database of Systematic Reviews for English-language studies published from database inception through October 31, 2019; the search strategy is outlined in eAppendix 1 in the Supplement. We also manually searched the bibliography lists of all included articles. Eligible studies included adults (aged 18 years or older) and tested the association of auditory perturbations with standing balance. We excluded studies that tested dynamic tasks (eg, stepping or gait), had training components, or used sounds as biofeedback or dual task.

    We could not include several other auditory paradigms that appeared in the literature, such as the implication of groove, timbre, or reverberation because each was studied in only 1 article. We also excluded studies that investigated responses to music because moving with music may be associated with affect or emotional expression, and this psychological urge to move may confound the results.

    To create a common language with which to discuss the disparate experimental paradigms related to sound and posture, we defined terms describing sound stimuli, hardware, and paradigms (eAppendix 2 in the Supplement).10-12 Balance paradigms and outcomes were also defined (eAppendix 3 in the Supplement). The Figure provides a conceptual framework of auditory stimuli variables used in previous research.

    Observations

    In total, we reviewed 28 articles. These articles included 18 (64%) studies involving healthy adults, 1 (4%) had participants with Alzheimer disease, 2 (7%) included participants with congenital blindness, 3 (11%) involved participants with vestibular loss, and 4 (14%) had participants with diverse levels of hearing loss.

    Healthy Adults

    Results from the healthy adult population are summarized by auditory paradigm in Table 1. Reduction, no difference, and increase in sway were all observed with sound attenuation.13-15 A fixed, nonmoving broadband noise (white or pink) was consistently found to reduce sway.16-21 The more sway the participants had originally, the more sway reduction they experienced.16

    The results regarding pure tone or narrowband static sound were inconclusive.22-27 Static prerecorded natural sounds appeared to reduce postural sway. Gandemer et al28 concluded that the richer the auditory environment, the more individuals can integrate sound information to decrease their postural sway. Sounds moving front to back or side to side were found to increase sway.29 Sounds moving along a 180-degree arc were found to increase sway (compared with silence) in 1 study30 but to reduce sway (compared with blocking sounds) in another study.13 Other studies reported reduction, no change, or increase in postural sway with rotating sounds.31-35 Guigou et al35 postulated that, in monaural hearing, the rotation of the sound was not perceived, and thus sound had a stabilizing role like a stationary sound.

    Table 1 lists other studies on frequency modulation36,37 or unpleasant sounds.38 In healthy adults, several studies found no association between sound loudness27,39,40 or sound pressure level36 and postural sway. Siedlecka et al27 found that sway area was reduced with extreme loudness only in high-frequency trials.

    Hearing Loss and Vestibular Dysfunction

    Four studies included individuals with diverse levels of hearing loss13,19,35,41 (Table 2). Three of the 4 studies suggested that sounds may be used to improve balance in individuals with hearing loss if the participants can hear the sounds.

    Three studies included adults with various levels of vestibular dysfunction.13,19,35 All 3 studies found that the associations of sounds with postural control (ie, stabilizing with static sounds or destabilizing with moving or blocked sounds) were magnified in adults with vestibular dysfunction. It appeared that adults with vestibular dysfunction may use an auditory substitution strategy42,43 similar to that seen with visual and somatosensory substitution. The change was larger in individuals with unilateral vestibular dysfunction than in healthy adults (Table 1).13

    Congenital Blindness and Alzheimer Disease

    Single-frequency sounds were used in 2 studies that compared postural control in individuals with congenital blindness and control participants.22,25 Both studies reported that auditory cues can be used to improve postural control in individuals with congenital blindness. No significant reduction was observed with 1 speaker placed in front of participants’ heads or with a head-mounted sonar.22

    One study showed that suppressing background noise was beneficial for postural control in individuals with Alzheimer disease.26 Gago et al26 concluded that audition, although less important than vision, also played a role in the process of multisensory integration for postural control by the central nervous system. Although the results were similar in individuals with Alzheimer disease and in control participants, this finding could be particularly important for patients with Alzheimer disease who may substitute for cognitive decline by sensory dependence.

    Discussion
    Suggested Mechanism of Auditory Input in Balance

    The 28 studies included in this review were generally guided by the weighting and reweighting theory of sensory integration for postural control. This theory suggests that individuals prioritize sensory information differently on the basis of the sources of sensory input available and the challenge induced by the task.44,45 It is well established that postural control requires ongoing integration of visual, vestibular, and somatosensory information, but the studies reviewed herein suggest that, overall, auditory input also has implications for postural sway in standing.23 Nevertheless, auditory cues appear to have a minor association with postural control compared with visual, somatosensory, and vestibular information. In studies involving healthy control participants, the findings were variable (ie, increased, reduced, or no change in sway with different sounds). The role of auditory cues seems to become more important in the presence of inherent sensory loss (such as those with vestibular dysfunction or visual impairment) or paradigm-induced sensory loss (ie, standing on foam with eyes closed). The increase in sensory reliance was not seen for the change in somatosensory input (standing on floor and/or foam).18,19 Discrepancies in studies with healthy young adults may reflect the inherent redundancy of a healthy system. In individuals with multiple possible strategies to generate a stable stance, auditory cues may not be essential for balancing during standing.

    One proposed theory regarding the integration of sound into postural control is that of auditory anchorage.28,35 According to this theory, stationary sound sources provide spatial information that helps the brain structure a spatial image of the environment. The brain then uses that information for stabilization. This concept has parallels in other research involving visual integration for balance. Previous research has consistently shown that a visual anchor decreases postural sway,46 compared with no vision or a moving visual stimulus. The use of an auditory anchor is supported by studies demonstrating that stationary sound sources and addition of sound sources helped reduce sway,16,22,28 whereas sound attenuation increased sway.14 A stationary source of sound, however, does not guarantee reduction in sway. Reduced sway with stationary sounds has been reported for broadband noise (eg, white noise), but the studies were inconclusive regarding pure tones.23 Compared with pure tones, broadband noise is richer (ie, combines all frequencies, has greater ecological validity and increased familiarity, or is more authentic and occurs in nature). In localization studies, participants typically localized white noise better than pure tones.12 Any or all of these characteristics of the sound could allow it to function as an auditory landmark. In addition, stationary white noise was primarily tested via speakers. Karim et al47 suggested that a stationary white noise source had to be earth-referenced rather than head-referenced (speakers rather than headphones) to improve performance on a dynamic task. Ross and Balasubramaniam,20 however, observed some reduction of sway with white noise presented by headphones.

    Overall, previous studies have suggested that healthy young adults are more likely to use auditory cues for balance in paradigms with reduced sensory input, such as standing with eyes closed or standing on a compliant surface. This finding was not the case with standing on foam among healthy young adults,28 but foam was a factor in the integration of auditory cues in individuals with vestibular and hearing loss.19 In addition, the combination of blocking vision and standing on foam increased the importance of sounds for balance in healthy older adults.34 It is possible that the foam was not challenging enough to induce sensory reweighting in healthy young adults48 compared with those with sensory loss.

    The auditory landmark theory suggests that the sudden perturbation30 or jumping from one side to the other29 of the sound source will interfere with the hearing spatial map, leading to destabilization (ie, increased postural sway). However, this theory does not explain the reduction in sway associated with rotating sounds. It is possible that continuous, regular movement of sounds from an array of speakers can also be used to improve postural sway. Gandemer et al31 proposed that the rotation provides additional sensory input to supply and enrich the spatial map. This process seemed to happen when auditory cues of white noise were projected from an array of speakers rather than headphones. Such a setup allows for localization of the sound using differences in the temporal and intensity characteristics of the sound. Another possibility is that participants reweighted the fast-rotating sounds and used the stable ground to reduce their sway. Studies with different setups such as headphones, however, did not observe the same phenomena.35 Reduction in sway is not expected with moving visual stimuli or support surfaces. Peterka44 found that increased sway in healthy adults was associated with an increase in the amplitude of the visual and surface movements until those movements were too large to follow and thus no longer induced an increased sway. This behavior coincided with reweighting of unreliable sensory cues. Even in the case of such normal reweighting, however, the overall amount of sway with a moving visual stimulus or surface was higher than that of the static conditions. Therefore, the possibility that rotating sounds can facilitate stability suggests a different mechanism for sounds vs vision integration for postural control. This possibility needs to be further studied within naturally moving sounds, such as a train or a bus, combined with visual cues that are static or dynamic.

    An alternative theory for the association of sound with posture pertains to the role of attention in sensory integration for balance. In addition to the array of speakers and broadband sounds that could provide spatial cues, the study by Gandemer et al31 also involved a cognitive task that was compatible with the movement of the sounds; participants were asked to count the number of laps the sound completed. It is possible that the cognitive load through the secondary task was associated with reduced sway and not the auditory input by itself. Supporting the importance of attention, other studies in healthy adults suggested that sounds can be integrated only if they are attended to, a claim that is not typically made for visual, somatosensory, and vestibular information. The reason may be that the association between sounds and postural control is weaker than that between visual, somatosensory, and vestibular when all sensory systems are intact. This possibility has led several authors28,33 to propose that the reduction in sway is attributable to the concurrent cognitive task rather than the sounds themselves. Future studies should test this theory within challenging balance tasks and among individuals with sensory loss for whom the ability to switch focus of attention may be more limited.

    Directions for Future Research
    Study Populations

    Future study populations should include individuals with sensory loss. Inclusion criteria should be well defined and cohesive in terms of the degree of hearing loss, vestibular loss, or a combination, such that a comparison between normal aging and aging with sensory loss can be made. When the role of sound in posture among people with specific levels of hearing loss has been clarified, studies should assess whether hearing rehabilitative strategies (ie, hearing aids, cochlear implants) can change sensory integration and thereby affect balance performance.

    Auditory Paradigm

    Future studies should include prerecorded sounds of real-life situations. Current studies categorize sounds into either stationary or moving, but this division does not necessarily apply to natural or realistic sounds that involve stationary and moving components. In addition, it appears from previous studies that salience of the sounds is important. To our knowledge, the study of natural sounds within proper contexts has not been comprehensively addressed in the literature and may further shed light on the underlying mechanism of increased fall risk in individuals with hearing loss in real-life environments. The use of headphones for providing 3-dimensional information should be further tested owing to the clinical implications and simpler setup of headphones vs speakers.

    Balance Paradigm

    Future studies on sound and posture in adults should include an adequate level of balance challenge. If the task is challenging enough, perhaps we will observe integration of auditory cues regardless of the level of attention. In addition, most of the studies in this review investigated the importance of sounds for postural control when visual cues were completely removed. Studying the simultaneous integration of diverse visual stimuli and generated or natural sounds may promote understanding of how sighted individuals may be using sounds for balance in real-life situations. Virtual reality technology presents an opportunity to develop immersive balance paradigms that are ecologically valid. Testing sound integration during dynamic balance and gait tasks will also enhance the ecological validity of the findings because most falls happen during movement.

    Limitations

    This narrative review has several limitations. Despite the large number of studies published on this topic since 1990, combining the results into a cohesive conclusion proved challenging. The auditory paradigms varied among studies, and inconsistent results were occasionally found among studies that applied a similar testing paradigm. This review synthesized studies on standing balance. We did not include auditory paradigms that appeared only once in the literature or had an emotional component such as music.

    Conclusions

    Stationary broadband sound (white noise or environmental sounds) may serve as an auditory anchor for balance primarily when projected through speakers and when the balance task is challenging. A stationary pure tone was not associated with changes in sway. Moving sounds were typically associated with increased sway when projected through headphones. In individuals with vestibular or hearing loss, but not in those with a unilateral cochlear implant, moving sounds appeared to be more destabilizing than in healthy controls. Auditory cues and the presence of hearing loss should be considered in balance and fall risk assessments.

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    Article Information

    Accepted for Publication: January 9, 2020.

    Corresponding Author: Anat V. Lubetzky, PT, PhD, Steinhardt School of Culture, Education and Human Development, Department of Physical Therapy, New York University, 380 Second Ave, 4th Floor, New York, NY 10010 (anat@nyu.edu).

    Published Online: March 12, 2020. doi:10.1001/jamaoto.2020.0032

    Author Contributions: Drs Lubetzky and Cosetti had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

    Concept and design: Lubetzky, Gospodarek, Kelly, Roginska, Cosetti.

    Acquisition, analysis, or interpretation of data: Lubetzky, Gospodarek, Arie, Kelly, Cosetti.

    Drafting of the manuscript: Lubetzky, Gospodarek, Arie, Kelly, Cosetti.

    Critical revision of the manuscript for important intellectual content: Lubetzky, Kelly, Roginska, Cosetti.

    Administrative, technical, or material support: Lubetzky, Kelly, Roginska.

    Supervision: Roginska.

    Other—summarized most of the articles in the paper: Arie.

    Conflict of Interest Disclosures: Dr Cosetti reported unpaid participation in research on cochlear implants and other implantable devices manufactured by Advanced Bionics, Cochlear Americas, MED-El, and Oticon Medical outside the submitted work. No other disclosures were reported.

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