ORIGINAL RESEARCH published: 30 June 2021 doi: 10.3389/fpsyt.2021.638949 Sounds of Silence in Times of COVID-19: Distress and Loss of Cardiac Coherence in People With Misophonia Caused by Real, Imagined or Evoked Triggering Sounds Antonia Ferrer-Torres 1,2* and Lydia Giménez-Llort 1,2,3 1 Centro Médico Psicológico L’Alfatier, Barcelona, Spain, 2 Department of Psychiatry and Forensic Medicine, Faculty of Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain, 3 Institut de Neurociències, Universitat Autònoma de Barcelona, Barcelona, Spain The extreme, unprecedented situations in the current COVID-19 pandemic are risk factors for psychosocial stress for the entire population. However, strict confinement had Edited by: a particular impact on people suffering from misophonia and their families. Misophonia Umberto Volpe, Marche Polytechnic University, Italy is a condition in which hearing certain sounds triggers intense anger, disgust and even Reviewed by: severe autonomic nervous system responses. This prospective cohort study examined Hamdi Chtourou, the impact of strict confinement (Spain, March 14–June 21, 2020) on a sample of 24 University of Sfax, Tunisia people (16 women and eight men) who had been diagnosed with moderate to extreme Jennifer Jo Brout, International Misophonia Research misophonia and were regularly attending a medical psychology center in Barcelona. Network (IMRN), United States The 3-month period of confinement caused general emotional maladjustment, distress, *Correspondence: and a transitory crisis. Long-term biomonitoring of their heart variability rate (HRV) Antonia Ferrer-Torres cmedicopsicologico@alfatier.es enabled to identify a significant increase in physiological arousal after the confinement period, which had already been recorded in a loss of cardiac coherence under basal Specialty section: rest/relaxation conditions. Certain auditory stimuli triggered adverse responses, lowered This article was submitted to Public Mental Health, HRV scores, and an increased stress level and heart rate. Loss of cardiac coherence a section of the journal in their responses to these auditory stimuli (triggering mouth, nose and other sounds), Frontiers in Psychiatry as well as to non-triggering mouth, nose and other sounds was increased when Received: 07 December 2020 compared to two assessments performed during the previous year. Despite the limited Accepted: 25 May 2021 Published: 30 June 2021 sample size, sex differences were observed in the incidence. Loss of cardiac coherence Citation: worsened with the severity of the misophonia. Most importantly, imagined or evoked Ferrer-Torres A and Giménez-Llort L triggering sounds, as well as real ones, were enough to cause the aversive responses, (2021) Sounds of Silence in Times of COVID-19: Distress and Loss of as displayed by the increased loss of cardiac coherence with respect to the at-rest Cardiac Coherence in People With basal level. A semi-structured interview revealed the exceptional nature of the situations, Misophonia Caused by Real, Imagined increased hyper-sensorial sensitivity, fear of being infected with or dying from COVID-19, or Evoked Triggering Sounds. Front. Psychiatry 12:638949. the patients’ coping strategies, and the difficulties and constraints they faced. Finally, doi: 10.3389/fpsyt.2021.638949 the article gives recommendations for better management of misophonia. Improved Frontiers in Psychiatry | www.frontiersin.org 1 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement knowledge of this disorder would help address the current lack of health and social care, hopefully preventing this shortfall’s impact on social and affective relationships, which are particulary important for well-being now and in the coming periods of physical distancing measures. Keywords: misophonia, distress, loss, cardiac coherence, heart rate variability, COVID-19, confinement INTRODUCTION in the misophonic population is depression (13), which was diagnosed in 22% of a sample of 50 people suffering from COVID-19, Confinement and Secondary misophonia (14) and in 9.61% of a sample of 52 (8). Both Impact of COVID-19 Pandemic studies revealed a positive correlation between depression Since the WHO declared the COVID-19 outbreak a pandemic and the severity of misophonia symptoms. Rouw and on March 11, 2020 (1) an increasing number of scientific reports Erfanian (15) also found that post-traumatic stress disorder have documented the psychological affects upon the population. (PSTD) was one of the most common diagnoses in people These have been attributed to confinement, as well as the direct with misophonia. and indirect effects of the illness itself (2, 3). Added to this are the loss of loved ones and associated grieving processes, as well as the impacts of a sudden health and socioeconomic crisis of Mapping Neuronal Basis of Misophonia unprecedented magnitude. Neuroimaging research has revealed that there might be a Even before the COVID-19 pandemic, studies warned that neural basis to misophonia (16, 17). Individuals with misophonia confinement responding to outbreaks of viral diseases such as have been shown to have greater activity in the anterior SARS and H1N1 flu produced negative psychological effects insular cortex in response to signals that trigger misophonia (3). However, Spain had no choice but to implement strict than in response to non-triggering or universally unpleasant confinement measures to put a halt to the dramatic spread of signals, compared to the control group (18). The existence of the disease through its population and to prevent its health greater functional connectivity in the misophonic group between system reaching saturation point. In Spain, a strict lockdown the anterior insular cortex and the ventromedial prefrontal of 47 million people was put into place from March 14 to cortex, posteromedial cortex, hippocampus, and amygdala June 21, 2020, and limited the free movement of citizens to indicates that there are neuronal bases for the heightened, essential acts such as the acquisition of food and medicine or emotional response to triggering stimuli. Schröder et al. (12) going to medical centers or the workplace, resulting in the demonstrated networks’ prominent involvement in misophonia confinement of the population in their places of residence. The and that the right anterior cingulate cortex and the right emergence of anxiety, depression, insomnia, denial, anguish and insula are activated to a greater extent in people with the fear was particularly common, as was the aggravation of existing condition (12). conditions (4). The Spanish scientific-technical guidelines for managing COVID-19 included a section that detailed how the pandemic had contributed to the mental health crisis. The HRV and Cardiac Coherence as Objective document paid particular attention to health professionals and Physiological Measures of Misophonia hospitalized patients, people with pre-existing mental illness, At a physiological level, people with misophonia show higher and individuals in difficult situations caused by isolation and skin conductance responses to auditory stimuli that are triggering the economic crisis. The international scientific community for them, compared to healthy controls (19). This increase in has described this phenomenon as “the untold toll” – the conductance was thought to reflect an autonomous physical effects of the pandemic on patients without COVID-19 (5) component in the misophonic reaction. Also, heart rate and can be also referred as secondary impact of COVID- variability (HRV) describing the physiological phenomenon 19 pandemic. of variation in heartrate in the beat-to-beat time interval between consecutive heartbeats (20–25) is considered an effective Misophonia and Co-morbid Disorders instrument that is able to quantitatively assess the response of At present, misophonia is not included within the International the autonomic nervous system (ANS) to certain situations (26). Classification of Diseases (ICD-11) and does not appear in HRV analysis is therefore recognized in clinical settings as a the Diagnostic and Statistical Manual of Mental Disorders powerful indicator of the relationship between psychological and (DSM-5). However, several studies have indicated that physiological processes (27). As some scholars have pointed out, misophonia is a disorder associated with a wide variety of HRV is accepted to be a cost-effective method with a high level psychiatric symptoms (6–9), including anxiety that acts as of validity and reliability, regardless of any cardiovascular disease a channel for anger (10, 11). Furthermore, according to the patient may have (28). It has been used in several studies to studies by Schröder et al. (12), people with misophonia investigate the reactivity of the ANS to sounds (29, 30). Also, a report suffering a significantly higher percentage of anxiety number of interventions aimed to improve health and wellbeing symptoms than control groups. Another recurrent disorder though the adjustment of ANS balance train patients to achieve Frontiers in Psychiatry | www.frontiersin.org 2 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement “cardiac coherence,” the coupling and synchronization of the were previously conducted outside of it. Additionally, the crisis rhythm of breathing to the rhythm of the heart [i.e., (21, 31–35)]. situation has made it impossible for families and individuals to go through necessary adaptation processes, generating intra-family Misophonia Emotional, Behavioral, and social stress. Due to a lack of knowledge and information, Physical, and Physiological Components misophonic patients have not been taken into account at the When exposed to auditory stimuli, which may also be termed socio-sanitary or legal levels. This lack of assistance results from “triggering sounds,” people who suffer from misophonia the fact that the disorder is unfamiliar to a significant number of experience intense and unpleasant emotional, behavioral, psychological health professionals and a large proportion of the physical and physiological reactions. Thus, responses to population: even those who suffer from it. triggering sounds or “misophonic responses” are usually: emotional (anxiety, anger, disgust, extreme irritation, the feeling Current Study on the Secondary Impact of of losing emotional control, the feeling of being overloaded by Strict Confinement During COVID-19 stimuli); behavioral (feeling the need to flee or escape from the place where the sounds are being produced); physical (pressure Pandemic on Patients With Misophonia in the chest); or physiological (increased heart rate), in addition The objective of this prospective study was to determine the to many others (19, 36, 37). The most common somatic reactions impact of strict confinement on the HRV of misophonic patients in these patients are pressure in the chest, tension in the arms, in Spain, using a longitudinal design. For that purpose, a pre- head, or the whole body, and increased heart rate, increased post analysis of the HRV assessment was conducted in people body temperature, physical pain, or breathing difficulties (19). diagnosed with misophonia who were regularly attending a People with misophonia tend to avoid social situations or medical psychology center in Barcelona. The study hypothesized anticipate triggering stimuli, which leads to a deterioration that, during confinement, the following HRV-related changes of their social and functional life. Characterizing the complex would be observed: [1] there would be a worsening in neural underpinnings of misophonia and the interplay of neural responsiveness to auditory triggers, with respect to two preceding systems (38) to develop the behavioral, cognitive and emotional basal periods; [2] a stressful period of confinement would responses to misophonic triggers is among the key aspects increase heart rate variability in patients with misophonia, and considered in the road map for advancing in the scientific [3] not only real but imagined or evoked triggers would result research agenda in this new field (36). in a loss of cardiac coherence. Finally [4], it was hypothesized that the semi-structured interviews on their fears (the fear or Misophonia Common Triggers being infected or dying), relationships and emotional states, Sounds such as chewing, lip-smacking or breathing are among in conjunction with their self-assessments, would confirm the those that most frequently provoke intense anger and physical increased impact or perception of stressful events, while also arousal (19). According to Jager et al. (39), the most disturbing revealing their coping strategies. sounds are eating (96%), followed by nasal or respiratory sounds (85%), these being the two key groups used to diagnose MATERIALS AND METHODS misophonia. In addition to these two groups, other triggering stimuli, such as sounds made by other humans, animals, objects, Participants and the environment can be added. Concurrently, visual or The prospective study started on June 29th, 2019 with a cohort movement triggers are also noted. of 24 individuals (16 women and eight men), who were regular patients at a medical psychology center in the city of Barcelona. Misophonia and Secondary Impact of None of them had initially requested a specific consultation for COVID-19 Pandemic treatment for misophonia. These patients were later diagnosed Jastreboff first described this phenomenon in 2001 (40). Since with misophonia at the center using a recent scale: Amsterdam then, scientific studies of misophonia, while still scarce, have Misophonia Scale [A-MISO-S, Schröder et al. (41)]. increased in number [i.e., (14, 18, 19, 36, 39, 41–44)]. Misophonia Patients first came to the center in the belief that they had has only been discovered recently, yet it is a fairly common other conditions. In fact, 99% (one woman/24 patients) of condition. A study conducted with college psychology students them were completely unaware that they were suffering from reported that 19.9% had clinically significant misophonia misophonia. After initial diagnosis and subsequent check-ups, symptoms (10). Further work research of this research team we tested these regular patients for misophonia. The cases found 6% incidence among Chinese university students. Besides, identified as misophonic after June 2019 were selected for this their work provided further evidence on misophonia symptoms study. The inclusion criteria were as follows: Over 18 years of being associated with noteworthy impairment, as well as age; Having agreed to participate in the study; Having spent general sensory sensitivities, obsessive-compulsive, anxiety, and the national strict confinement period at home, following it depressive symptoms (43). During confinement, interpersonal according to the rules; Being a regular patient of the center; and social conflicts have also increased (2, 45–47). Factors Having been diagnosed with misophonia after June 2019; At least such as the reorganization of domestic space, the intrusion mouth and nasal sounds having been identified as triggering of virtual spaces into family life and multitasking, have made stimuli in the patient’s diagnosis; Having a minimum of four the home into a space in which activities take place that triggering stimuli. Frontiers in Psychiatry | www.frontiersin.org 3 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement Exclusion Criteria were: History of phonophobia, mild); level 2 (10–14, moderate); level 3 (15–19, severe); level 4 hyperacusis, tinnitus, tympanic membrane perforation or (20–24, extreme). temporomandibular disorders (TMDs); Having any degree of hearing impairment, from mild to severe, following the Physiological Measurements Bureau International d‘Audio-Phonologie (BIAP) criteria, which In order to measure the impact that confinement, the degree indicates mild hearing loss starting at 20dB; Have received a of balance-imbalance of the ANS was assessed. The patient’s treatment for misophonia. psychophysiological response was recorded by measuring HRV (ms) during exposure to certain auditory stimuli and in a state of rest or relaxation. The emWave R technology (emWave R EVALUATION TOOLS Desktop and emWave R PSR; HeartMath Institute, California, USA), a software that allows heart behavior patterns to be Diagnosis of Misophonia observed and measured on a computer, tablet, or cell-phone During the diagnostic phase, the Amsterdam Misophonia Scale screen in real time, was used. The software is a heart-rate (A-MISO-S) was used to assess whether patients were suffering coherence trainer, designed to assess, prevent, control and reverse from misophonia (41). For the only purpose of this study, in the effects of stress. Figure 1 provides an example of an HRV order to facilitate data collection and analysis, the five levels read-out upon exposure to a sound, the results remaining of this numerical scale (41) were labeled as follows: level 0, without the normal range (48). As indicated, each of the sounds not misophonic (for a score of 0–4, subclinical); level 1 (5–9, was evaluated through time domain analysis, using a statistical FIGURE 1 | Longitudinal monitoring of HRV in people with misophonia at three different stages. Results are expressed as medians of HRV (ms). The 25, 50, and 75th percentiles are detailed in the Supplementary Table in Supplementary Material Pre-confinement- First assessment (Pre-C1), Pre-confinement Second Assessment (Pre-C2), Post-confinement First (Post-C1), Second (Post-C2), and Third (Post-C3) Assessments. Sound on and sound off as depicted inside and between the bars, respectively. Black bars: HRV during the 10 min of relaxation, X: without sound stimuli. Gray bars: Sounds self-reported (SR) as neutral: Mouth sound 1, mouth sound 2, nose sound 1, nose sound 2, another sound 1, another sound 2. Trigger sounds: Magenta bars, mouth sound A; Purple: nose sound A, Pink: another sound A. Imagined sounds: Soft Magenta bars, imagined mouth sound A; Soft purple, imagined nose sound A; soft pink, imagined nose sound A. Normal cardiac coherence (50 < HRV < 100); in red, cardiac coherence out of range (<50). Statistics: ***p < 0.0001 Wilcoxon’s rank-sum test, as compared to “Basal level, Relaxation 10 min” of the first assessment. Frontiers in Psychiatry | www.frontiersin.org 4 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement method sourced from the Task Force of The European Society The Personalized Sound Bank (PSB) of Cardiology and The North American Society of Pacing and The PSB consisted of a personalized sound file for each patient Electrophysiology (49). This is currently one of the most widely and it was set up by a sound technician using a sound meter, a used methods. computer, headphones, the list of triggering sounds mentioned by the patient, and the interview notes. PSBs were created as follows: Patients had to record the Procedure situations and stimuli that triggered misophonia in their daily life The protocol was designed to assess HRV in three different stages: for 1 month. This record had to be brief, and the patient had [1] basal level – after obtaining the misophonia diagnosis (2019); to rate the trigger of misophonia from 0 to 10, differentiating [2] second assessment for a retest- after completing the first their physical reaction from the emotional one. At the end half of the program, and [3] post-confinement - at the end of of the month of recording, an interview was conducted in June 2021 after having been through the period of confinement which the patient handed over and explained the list of responding to the COVID-19 pandemic (March 14 to June 21, situations. From this list, the sounds corresponding to the 2020). patient’s description in the interview were selected from the 15 On each day of assessment, the participants were asked to have sound banks. had a light meal in the two hours before the test, but not to have Three alternative sounds were recorded that matched the ingested alcohol, coffee, tea, chocolate or any other stimulants. patient’s description. A pre-assessment of triggering sounds was They were informed about the duration of the study, what it carried out, where patients were asked to confirm whether the was about, and the number of sounds they would be exposed selected sounds resembled those they had described by them in to, but at no stage did they know what auditory stimulus would their month-long record. After exposure to the sound, the patient be presented to them. The assessments were conducted in a had to choose one of the following options: soundproof room, with dim light. During assessment sessions, no interruptions were allowed and the patient was physically isolated [1] It does not resemble the recorded sound at all; [2] It from the rest of the center. somewhat resembles the recorded sound; [3] Yes, this is the In the three assessments, prior to the exposure to the sounds, sound; [4] This is the exact sound situation experienced. the patient was asked to perform a relaxation exercise for 10 min, The sound was only accepted when the patient validated it followed by sound exposure for 5 min. Between each period with answer 3 or 4. If the patient agreed, the sound was of sound exposure, during the intertrial time of 5 min, a rest/ recorded as definitive. If the patient rejected the sound, it was relaxation was again performed. canceled and a new one was presented for the same task. For The exposures were as follows: each situation, three alternative sounds had been filed, using identical triggers described by the patient. All the sounds were Pre-confinement First assessment (Pre-C1) – The patient normalized so that they did not exceed 70dB, as measured with was exposed to non-triggering sounds (understood as those a sound meter. PBS were stored in a computer, from where sounds the participant had not identified as triggering they were used as outputs for the second assessment of the misophonia at the time of diagnosis), two sounds related to post-confinement stage. eating, two nasal sounds and two other sounds. All these sounds had been randomly selected by the psychologist administering the test. Self-Reporting Pre-confinement Second assessment (Pre-C2) – The patient After the confinement period and having conducted the was exposed to a total of three sounds they had identified as third and final HRV assessment (post-confinement stage), triggering misophonia: one chewing food, one nasal, and one a semi-structured interview was carried out with each miscellaneous. These sounds had been selected in advance by patient. Factors related to interpersonal relationships, the psychologist administering the test. In this assessment, the emotions and other areas connected to misophonia were sounds were taken from each participant’s Personalized Sound investigated by conducting a semi-structured interview, as Bank (PSB). The procedure for creating the PSB is explained detailed in Table 2. The descriptive analysis determined at the end of this section. A total of 15 sound banks were used. patients’ sociodemographic characteristics and the reasons Post-confinement (PC) – Consisted in three assessments: why they believed they had modified their behavior (Post-C1) exposure to non-triggering sounds, in which the during confinement. procedure completed in the first assessment was repeated, but using only three sounds identified as non-triggering Data and Statistical Analysis – 1 chewing food, 1 nasal and 1 miscellaneous; (Post- The statistical analysis derived from the HeartMath tool C2) exposure to second assessment triggering sounds, the was performed using IBM SPSS-software (version 25), second assessment being repeated in the same way; and through which both descriptive and inferential procedures (Post-C3) imagined triggering sounds used in the second were carried out. Statistical analysis of HRV was carried assessment, in which the patient was asked to imagine or out by means of Wilcoxon signed rank tests for non- recall the three triggering sounds used in the preceding parametric statistical analysis since the variables did not assessment of this stage. There was no sound exposure during follow a normal distribution and there was no homogeneity this assessment. of variances. Frontiers in Psychiatry | www.frontiersin.org 5 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement TABLE 1 | Demographics and misophonia diagnoses. Post-confinement Figure 2 illustrates HRV responses at the post-confinement stage Total Women Men and according to participants’ level of misophonia, as diagnosed (n = 24) (n = 16) (n = 8) using the A-MISO-S test. The responses are shown for non- Age (years) 45.75 ± 11.12 47.63 ± 11.83 42.0 ± 9.07 triggering auditory stimuli, the triggering auditory stimuli, and Marital status the imagined/evoked stimuli. Married 11 8 3 The same trend as in Figure 3 can be observed – the higher the Single 7 4 3 degree of misophonia, the lower the HRV score, as shown in the Divorcee 4 3 1 following figures. Assessment 1: M+ [2], 132.66; M+ [3], 85.94; Widow 1 1 0 M+ [4], 16.98. Assessment 2: M+ [2], 117.91; M+ [3], 79.44; M+ Level of education [4], 11.78. Assessment 3: M+ [2], 124.64; M+ [3], 87.06; M+ [4], 16.05. Primary 0 0 0 High school 12 6 6 University 12 10 2 Self-Reporting Misophonia (M+) Table 2 shows the self-reported results, constructed on the Level 2, moderate (M+ 10–14) 10 6 4 basis of a semi-structured interview carried out with the Level 3, severe (M+ 15–19) 10 7 3 patients after confinement. It includes their own evaluation Level 4, extreme (M+ 20–24) 4 3 1 of their interpersonal relationships and their ideas about why Assessed using the Amsterdam Misophonia Scale (A-MISO-S, 27). The levels were their emotional and relational states worsened. This general adapted by the authors for the only purpose to facilitate analysis in the present work. deterioration was defined by 100% of the patients as a “crisis.” They believed it to be a transitory crisis which would end once confinement and the pandemic ended. Despite distinct marital RESULTS status, none of participants were living alone during the strict confinement, nor confronted it in their own room but in a Demographics house or apartment. It can be seen that 79.17% of the patients The demographics of the sample of 24 participants, with a sex described a worsening in the relationship with their partner, ratio of 2:1 women to men, are depicted in Table 1. and 87.50% mentioned a deterioration in their relationships with the community. All of the patients showed emotional Longitudinal Monitoring of HRV deterioration. In 87.50% of the cases, patients believed the cause Figure 1 shows the results of participants diagnosed with to be the situation of confinement; the same percentage alluded misophonia in the three stages: basal level, retest and post- to overstimulation from sounds both within the family and in confinement assessments. For the basal level and retest the neighborhood. Having to live with move movement and the assessments, the HRV measurements in a state of relaxation resulting sounds, both in the morning and at night, was cited by (black bars) produced a score within the normal range (>50). 83.33% of the participants. All of the patients described having In contrast, during the post-confinement assessment, the three experienced increased hypersensitivity in general, including to scores for the relaxation period (black bar at PC1, PC2, and sounds and movements. Feeling more hypersensitive and hyper- PC3) progressively decreased. Significantly, in all the post- vigilant at bedtime was mentioned by 83.33%, due to noises confinement assessments, including those referring to the 10 min produced in the neighborhood, or by family members and pets: of relaxation, the scores were HRV < 50, outside the normality both in their own and neighbors’ homes. Fear of being infected range (Wilcoxon rank test, p < 0.001 vs. basal level). by COVID-19 was cited by 62.50% and the same percentage said that their ailments and discomfort increased, due to the change in routine and lack of physical exercise, as other authors have also HRV According to the Different Levels of observed (50). Misophonia In the following paragraphs, we provide a detailed overview Second Assessment of the patients’ open-ended comments about their strategies for Figure 3 depicts HRV responses to three non-triggering auditory coping with stress, and other reflections on their fears and the stimuli at the second assessment, according to participants’ level confinement period. The patients recognized that the frequency of misophonia (moderate, severe or extreme), as diagnosed using with which they experienced the variables related to hyper- the A-MISO-S test. A negative relationship can be observed vigilance and hyper-sensibility, described in Table 2, increased between the degree of misophonia and the results obtained by as the days of confinement passed. They claimed to have exposure to non-triggering sounds: the higher the degree of greater resilience to triggering stimuli (movements and sounds), misophonia, the lower the HRV score (misophonia-2: 20.32; thanks to having previously completed training in self-control misophonia-3: 12.0; misophonia-4: 10.5). The same relationship techniques, including breathing, visualization, and relaxation also appears in the relaxation or resting stage assessments: in this exercises. Most of them agreed that being well-practiced in these state of rest or relaxation, the HRV value progressively decreases, techniques could improve their capacity for self-control and their the more severe the misophonia. ability to manage triggering stimuli and/or adverse situations. Frontiers in Psychiatry | www.frontiersin.org 6 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement FIGURE 2 | Monitoring of HRV in people with misophonia during the second assessment, according to the severity of the disorder. Results are expressed as medians of HRV (ms). The 25, 50, and 75th percentiles are detailed in the Supplementary Table in Supplementary Material. Bar codes as in Figure 1. Moderate M+ (Level 2, n = 10), severe M+ (Level 3, n = 10), and extreme M+ (Level 4, n = 4) exposed to non-triggering auditory stimuli (mouth, nose, other). Misophonia was assessed using the Amsterdam Misophonia Scale [A-MISO-S, (41)] and the levels of misophonia were adapted by the authors for the only purpose to facilitate analysis in the present work. They also placed great value on having scheduled activities suitability or effectiveness of the intervention, since we must that they had to carry out on a daily basis: the medical psychology bear in mind that the threshold stress levels of a person with center had asked them to perform the activities, and monitored misophonia are those experienced by any other person in a this throughout the confinement period. These activities had confinement situation. Living with constant auditory stimuli or been designed on a completely individual basis, according to how disturbing sounds, without being able to control, avoid, run away the patients’ condition progressed. from or manage them is to live in a state of permanent stress. In To tackle information overload regarding COVID-19, deaths, addition, misophonic patients receive a lack of empathy usually and the risk of contagion, measures were taken such as limiting due to ignorance – from his or her family, society, and even the information and performing therapeutic writing exercises to health system. control fears and anxiety. Other measures taken to address Participants also described how, once they had entered a this and other issues, were performing daily physical exercise, stressful situation or felt unstable, they were unable to return adjusting chronobiological factors – sleep-wake cycles and meal to a state of normality by performing self-control exercises, times – and practicing various self-control exercises. especially if triggering stimuli occurred during the day and The patients told researchers how forced confinement was night. They thought that practicing self-control exercises could implemented in an excessively sudden manner, which made be somewhat more effective after “venting.” This was achieved it difficult for them to prepare therapeutic strategies that through behavior such as getting angry, yelling, singing, running, would enable them to deal with the situation, and left them hitting an object, playing music, or putting on any device at unprepared on a psychological, physical and organizational level. a very high volume. After this “shock,” some patients found it They considered these factors to have aggravated the effects of helpful to: isolate themselves from others (if they were able); do confinement and made their subsequent recovery less effective. self-control exercises; put herbal heat packs (or pads) on their All the strategies employed by misophonic patients during ears, covering both ears entirely; listen to relaxing music; do this period could be useful for anyone experiencing a situation gentle physical exercise, or have a very hot shower or bath. These of confinement. However, this should not detract from the observations, made during the semi-structured interview, tally Frontiers in Psychiatry | www.frontiersin.org 7 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement FIGURE 3 | Monitoring of HRV in people with misophonia during the three assessments conducted at the post-confinement stage, according to the disorder’s severity. Results are expressed as medians of HRV (ms). The 25, 50, and 75th percentiles are detailed in the Supplementary Table in Supplementary Material. Bar codes as in Figure 1. Moderate M+ (Level 2, n = 10), severe M+ (Level 3, n = 10) and extreme M+ (Level 4, n = 4) exposed to non-triggering auditory stimuli (mouth, nose other), triggering auditory stimuli (mouth, nasal, other), and imagined/evoked triggers (mouth, nose, other). Misophonia was assessed using the Amsterdam Misophonia Scale [A-MISO-S, (41)] and the levels of misophonia were adapted by the authors for the only purpose to facilitate analysis in the present work. with the notes and statements that the patients made during the physiological arousal. Triggering auditory stimuli caused aversive post-confinement HRV assessment. responses, lowering HRV scores and thus increasing the stress level and heart rate, with a sustained loss of cardiac coherence. More importantly, not only real but imagined or remembered DISCUSSION stimuli were able to cause these effects, despite the fact that there was no audio reproduction. This study examined the secondary impact of situations related Some interesting results were obtained for the relaxation or to COVID-19 and the strict confinement measures implemented rest stage, in which patients spent 10 min performing a relaxation in Spain upon the fears, relationships, and emotional states of a exercise that they practiced every day at home. In the first stage, group of people with misophonia, who were regularly attending which established the basal level, and in the second assessment, a medical psychology center in Barcelona. Most importantly, it the HRV scores were within the normal range of > 50. These explored whether HRV was useful as a physiological indicator results show that the patients, at that moment, presented a of their distress, this also being compared to their basal levels, normal level of HRV in the absence of stress. However, during recorded during the preceding year. The difference between the the post-confinement assessments, there was a drop in HRV at number of male and female subjects in the sample, observed the resting stage, which was maintained in all three assessments. in our preceding work (51), was also confirmed. Our results In the first post-confinement assessment, where the patients show that the three-month confinement period caused these performed 10 min of relaxation and had not yet been exposed patients general emotional distress and a significant increase in to any sound, they did not manage to raise their HRV level to Frontiers in Psychiatry | www.frontiersin.org 8 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement TABLE 2 | Self-reporting on confinement: Transitory crises, deterioration of they would be exposed to. The patients lived in a state of relationships and emotions, and causes. hypervigilance resulting from the constant auditory stimuli that Total Women Men were present during confinement, which they experienced as a (%) (n = 16) (n = 8) threat and therefore caused them stress (52, 53). LeDoux posed the hypothesis of increased activity in the amygdala (54, 55) and Transitory crisis 100.0 16 8 the superior temporal cortex being related to maintaining greater Relationships attention to sounds (56, 57). With the partner worsened 79.27 14 5 Another factor that supports this interpretation is the With a neighbor worsened 87.5 15 6 progressive decrease in scores in all the assessments, recovery With the family worsened 25.0 4 2 not having been possible, despite patients having taken 5 min Emotional state of rest and carrying out a relaxation exercise that they knew Worsened 100.0 16 8 and had practiced before. Added to this was the cumulative Symptoms that I already had have worsened 41.7 8 2 effect that occurred in all the assessments, especially at the post- New symptoms have appeared 12.5 2 1 confinement stage. According to Schröder et al. (58), repeated Causes exposure to triggering stimuli may increase the severity of Increased general hypersensitivity 100.0 16 8 reactions. The data in this study demonstrate this cumulative Increased hypersensitivity to sounds and 100.0 16 8 effect, caused by the succession of sounds, and show that the movements time provided for recovery was not enough. The participants Overstimulation caused by sounds in the 87.5 14 7 themselves made the case for another solution: most of them family and the neighborhood mentioned a need to get out of the room, run, move, yell, The confinement situation 87.5 14 7 scream, talk or do any activity that involved physical movement Movements and multisensory stimuli during 83.3 14 6 and verbal expression. The relaxation exercise, after exposure to the day and at night sound, was an impediment rather than a help. However, before Increased hypersensitivity due to sleep 83.3 14 6 any auditory exposure, relaxation exercises did reduce the effect disorders, caused by neighborhood of triggering sounds or prevent these effects from occurring sounds as quickly. Increased hypersensitivity due to sleep 83.3 14 6 A decrease in the HRV score for the second of the post- disorders, caused by family and pet sounds confinement assessments was to be expected, since this one Increased hypersensitivity due to changes in 62.5 10 5 exposed the patient to the triggering auditory stimuli that he routine and a lack of physical exercise or she had predetermined before confinement and during the Fear of getting infected with COVID-19 and 62.5 10 5 second assessment in the program. However, it is worth noting dying how these scores compare to the following assessment, the third in the post-confinement stage. In this last assessment (post- confinement 3), the patients were asked to remember or imagine the triggering sounds they had heard in the previous assessment a normal state. The same occurred in the next two relaxation (post-confinement 2). Therefore, in this last assessment, the stages, within the same post-confinement assessment period. sounds were not audible. Comparing both groups, a recovery These results suggest that the patients had been experiencing in HRV scores can be observed in the third post-confinement a stressful situation during confinement to which they were assessment. The patients therefore experienced less stress in this not exposed at the time of the previous assessments (basal final assessment. The conclusion we may draw is that triggering level and second assessment), as they themselves confirmed in sounds, even if they are not those heard by patients in their the interview carried out once the study was completed, after daily lives, having been extracted from a database, generate confinement had ended. greater distress than the imagined sounds. Although more in- It can be seen that patients’ evaluations of auditory stimuli depth study is required, considering this observation is of special in the basal-level assessment were somewhat higher than their interest for misophonia treatment. evaluations of the same stimuli during the second assessment. In both the second assessment and the post-confinement In other words, the patients presented a higher level of stress stage, there was a negative relationship between HRV scores in the second assessment than in the basal level. The same and the severity of misophonia. The more severe the degree of was true for the results of the first of the post-confinement misophonia, the lower the HRV score. Moreover, this occurred assessments, in comparison to the previous assessments (second during periods of relaxation and when exposed to auditory assessment and the basal level). It can be inferred from this stimuli, which confirms that when a patient has a higher level that the results obtained in these post-confinement assessments of misophonia, both hypervigilance and stress levels are more are due to the alertness or hypervigilance that the patient was pronounced. Here it is important to clarify that misophonia was experiencing confinement. While the patients had not defined the assessed using the Amsterdam Misophonia Scale [A-MISO-S, auditory stimuli presented to them in the basal level assessment (41)] and the ‘levels of misophonia’ used in the present work were as triggering sounds, the participants were aware of the procedure defined by the authors for the only purpose to facilitate analysis they were about to go through, but not the type of sounds in categories. Frontiers in Psychiatry | www.frontiersin.org 9 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement As expected, in the semi-structured interview, all participants techniques, and controlled breathing. Other interventions that self-reported a deterioration in their emotional status and can help include: experiencing a transitory crisis. They all attributed these changes [4] Fitting bedtime and the time for restorative sleep to the to a general sense of hypersensitivity, as well as hypersensitivity. circadian rhythm. Avoiding long naps and heavy meals close Feeling particularly sensitive, due to the change in their routines to bedtime. Alcoholic or caffeinated drinks, or any other and a lack of physical activity, were also cited as causes of stimulants, should also be avoided. their worsening psychological health. The fear of getting infected [5] Doing physical exercise daily, as well as having designated with COVID-19 and dying was also mentioned by 10 out of 16 objectives to meet and scheduled activities to perform. women, and five out of eight men. According to a previous article [6] When sounds are unavoidable, it is helpful to have a published by the authors (51), once the lockdown was finished, repertoire of prepared strategies to help muffle them, such most misophonia patients attending the medical center reported as: white noise, listening to music on headphones, noise- to practicing self-confinement, their main reason for doing so canceling headphones. In these situations, and to relax, it is being the fear of being infected with or dying from COVID-19. effective to place a soft heat pack on the auditory pinna. Conflicts with participants’ partners, and especially with their neighbors, were caused by the noise they made throughout the day and part of the night. The long, strict confinement period CONCLUSIONS made this a recurrent situation that was impossible to avoid. This caused a crisis on the personal and interpersonal levels, as The extreme, unprecedented situations (the fear/risk of death and it affected their relationships with their neighbors and partners. confinement) caused by the current COVID-19 pandemic have Patients described the crisis as transient because they directly threatened to worsen the symptoms of misophonia sufferers and, related it to the situation of confinement and the fact that it was consequently, their physical and psychological health. The results difficult to manage the problems. However, the lack of empathy of this study, obtained from a sample of people with moderate for people with misophonia – sometimes due to ignorance, to extreme misophonia who underwent the strict confinement but mostly due to a lack of consideration – was another imposed in Spain, confirm the usefulness of home-monitored aggravating factor in this crisis. A recent study (12) showed there HVR to identify a worsening responsiveness to auditory triggers, to be neuronal correlates of misophonia that are triggered by with respect to two previous basal periods. The loss of cardiac audiovisual stimuli, resulting in a conditioned response involving coherence was greater for patients with more severe misophonia. anger and increased physical arousal. Thus, increased activation Additionally, imagined or evoked triggering sounds, as well as of the right insula, anterior cingulate cortex and superior real ones, resulted in a loss of cardiac coherence. At the same temporal cortex was observed in their patients. According to time, the deterioration in patients’ interpersonal relationships, the authors, given that these areas are involved in the moral especially with partners and neighbors, requires more initiatives evaluation of stimuli (59, 60), patients with misophonia may at a clinical level but also at a societal level. Finally, participants have perceived these stimuli as personal harassment, triggering handled their worsening situations with several coping strategies subsequent anger. With respect to our study, in the ongoing and by considering the crisis a transitory one that was associated COVID-19 pandemic, fear of the disease and death, as well with the severe conditions of confinement. Raising awareness as present and future uncertainty (this paper and 32) occur about this disorder would help address the current lack of in contrasting situations: being exposed to inescapable sounds health and social care and hopefully prevent the impact of this inside the home, and the silence of empty cities and streets. shortfall, currently evidenced in a deterioration in social and The sensorimotor gating process may have come up against affective relationships. an unprecedented neurophysiological sensorial imbalance that, in turn, may have enhanced individuals’ physiological arousal, DATA AVAILABILITY STATEMENT heightening their perception of the sounds around them and their interpretation of these sounds as aversive stimuli. The raw data supporting the conclusions of this article will be In the context of an extreme situation such as confinement, made available by the authors, without undue reservation. the most desirable strategy would be to take preventive measures, so that people with misophonia do not develop behaviors and ETHICS STATEMENT emotional states that are undesirable, both for themselves and the people with whom they live. Based on results of this study, The studies involving human participants were reviewed and we have produced a series of guidelines and recommendations, approved by L’Alfatier Medical Center. The patients/participants which are detailed below. provided their written informed consent to participate in [1] Awareness needs to be raised about the problem and what this study. its triggers are. [2] The awareness of family members or the people with AUTHOR CONTRIBUTIONS whom patients live also needs to be raised. [3] Prior to being exposed to any extreme situation, such as AF-T: interviews, data collection and analysis, and manuscript confinement, the person suffering from misophonia should draft. All authors contributed equally to the concept, design, and have learned and internalized relaxation exercises, self-control scientific discussion, as well as manuscript writing and approval. Frontiers in Psychiatry | www.frontiersin.org 10 June 2021 | Volume 12 | Article 638949 Ferrer-Torres and Giménez-Llort Misophonia in COVID-19 Confinement ACKNOWLEDGMENTS SUPPLEMENTARY MATERIAL We are grateful to the participants for their trust and The Supplementary Material for this article can be found their willingness to contribute to fighting COVID-19 through online at: https://www.frontiersin.org/articles/10.3389/fpsyt. scientific research. 2021.638949/full#supplementary-material REFERENCES 19. Edelstein M, Brang D, Rouw R, Ramachandran VS. Misophonia: physiological investigations and case descriptions. 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Practical recommendations for maintaining active lifestyle during the distributed under the terms of the Creative Commons Attribution License (CC BY). COVID-19 pandemic: a systematic literature review. Int J Environ Res Public The use, distribution or reproduction in other forums is permitted, provided the Health. (2020) 17:6265. doi: 10.3390/ijerph17176265 original author(s) and the copyright owner(s) are credited and that the original 51. Ferrer-Torres A, Giménez-Llort L. Confinement and the hatred of sound in publication in this journal is cited, in accordance with accepted academic practice. times of COVID-19: a Molotov cocktail for people with misophonia. Front. No use, distribution or reproduction is permitted which does not comply with these Psychiatry. (2021) 12:627044. doi: 10.3389/fpsyt.2021.627044 terms. Frontiers in Psychiatry | www.frontiersin.org 12 June 2021 | Volume 12 | Article 638949