Received: 5 July 2021 Revised: 30 October 2021 Accepted: 3 November 2021 DOI: 10.1002/brb3.2440 ORIGINAL ARTICLE The impact of coronavirus disease 2019 on emotional and behavioral stress of informal family caregivers of individuals with stroke or traumatic brain injury at chronic phase living in a Mediterranean setting Alejandro Garcia-Rudolph1,2,3 Joan Sauri1,2,3 Alberto Garcia-Molina1,2,3 Blanca Cegarra1,2,3 Eloy Opisso1,2,3 Josep Maria Tormos1,2,3 Dietmar Frey4 Vince Istvan Madai4,5,6 Montserrat Bernabeu1,2,3 1 Universitat Autònoma de Barcelona, Bellaterra, Cerdanyola del Vallès, Spain Abstract 2 Fundació Institut d’Investigació en Ciències Introduction: Even in nonpandemic times, persons with disabilities experience emo- de la Salut Germans Trias i Pujol, Badalona, Spain tional and behavioral disturbances which are distressing for them and for their close 3 Institut Guttmann Hospital de persons. We aimed at comparing the levels of stress in emotional and behavioral Neurorehabilitacio, Badalona, Spain aspects, before and during coronavirus disease 2019 (COVID-19), as reported by infor- 4 CLAIM Charité Lab for AI in Medicine, mal family caregivers of individuals with chronic traumatic brain injury (TBI) or stroke Charité Universitätsmedizin Berlin, Berlin, Germany living in the community, considering two different stratifications of the recipients of 5 QUEST Center for Transforming Biomedical care (cause and injury severity). Research, Berlin Institute of Health (BIH), Methods: We conducted a STROBE-compliant prospective observational study ana- Berlin, Germany, Charité – Universitätsmedizin Berlin, Berlin, Germany lyzing informal caregivers of individuals with stroke (IC-STROKE) or traumatic brain 6 School of Computing and Digital Technology, injury (IC-TBI). Faculty of Computing, Engineering and the IC-STROKE and IC-TBI were assessed in-person before and during COVID-19 online, Built Environment, Birmingham City University, United Kingdom using the Head Injury Behavior Scale (HIBS). The HIBS comprises behavioral and emo- tional subtotals (10 items each) and a total-HIBS. Comparisons were performed using Correspondence Alejandro Garcia-Rudolph, Institut Guttmann, the McNemar’s test, Wilcoxon signed-rank test or t-test. Recipients of care were strat- Barcelona, Spain. ified according to their injury severity using the National Institutes of Health Stroke Email: alejandropablogarcia@gmail.com Scale (NIHSS) and the Glasgow Coma Scale (GCS). Funding information Results: One hundred twenty-two informal caregivers (62.3% IC-STROKE and 37.7% H2020 Personalised Medicine by Predictive Modeling in Stroke, Grant/Award Number: IC-TBI) were assessed online between June 2020 and April 2021 and compared to their 777107 own assessments performed in-person 1.74 ± 0.88 years before the COVID-19 lock- down. IC-STROKE significantly increased their level of stress during COVID-19 in five emo- tional items (impatience, frequent complaining, often disputes topics, mood change and overly sensitive) and in one behavioral item (overly dependent). IC-TBI stress level only increased in one behavioral item (impulsivity). This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2021 The Authors. Brain and Behavior published by Wiley Periodicals LLC Brain Behav. 2022;12:e2440. wileyonlinelibrary.com/journal/brb3 1 of 13 https://doi.org/10.1002/brb3.2440 2 of 13 GARCIA-RUDOLPH ET AL . By injury severity, (i) mild (14.7%) showed no significant differences in emotional and behavioral either total-HIBS (ii) moderate (28.7%) showed significant emotional differ- ences in two items (frequent complaining and mood change) and (iii) severe (56.6%) showed significant differences in emotional (often disputes topics) and behavioral (impulsivity) items. Conclusions: Our results suggest specific items in which informal caregivers could be supported considering cause or severity of the recipients of care. KEYWORDS behavioral, COVID-19, emotional, informal caregivers, stress, stroke, traumatic brain injury 1 INTRODUCTION Evidence suggests, even in nonpandemic times, that persons with disabilities experience emotional and behavioral disturbances which Informal care is considered a cornerstone of all long-term care provi- are distressing for both individuals with disabilities and their close per- sion systems in Europe (EU, 2018). It is also gaining increasing recog- sons (Kim, 2007). There are limited data on the impact or added burden nition in international policy circles as a key issue for future welfare of a pandemic (or other calamities) on informal caregivers of persons policy. Estimates suggest that as much as 80% of all long-term care in with TBI or stroke. Europe is provided by informal carers (Frontiera et al., 2019). In the TBI is a growing public health concern and represents the great- United States, approximately 43.5 million people are caregivers to a est contributor to disability globally among all trauma-related injuries family member with a disability or illness (Gottschalk et al., 2020). (Dewan et al., 2018). There is consensus over the fact that the disabil- Caregiving can affect a caregiver’s emotional well-being and their ity associated with TBI stems mainly from the cognitive, emotional, and social activities as they often feel that they are not prepared for their behavioral alterations that complicate its course (Jorege et al., 2015). role due to a wide variety of personal factors and lack of skills (Wood- Furthermore, it has been recognized that these disturbances tend to be ford et al., 2018). chronic, difficult to treat and, occasionally, progressive (Bavisetty et al., A first step to developing therapeutic interventions provided by clin- 2008). icians targeting caregiver preparedness is to better understand fac- Stroke is a major cause of long-term disability worldwide with tors which influence such burden levels. This might enable the devel- increasing number of young people being affected by stroke in low- opment of effective interventions to prepare and support caregivers in and middle-income countries (Katan et al., 2018). Behavioral distur- their role (Lieshout et al., 2020). A recent thematic analysis reporting bances have been reported as frequent complications in stroke sur- on informal caregivers of community dwelling people with traumatic vivors (Ferro et al., 2009). As reported in previous research, survivors brain injury (TBI) highlighted the health systems’ reliance on informal of TBI very often experience symptoms ranging from irritability to care and the importance of supporting them: Healthcare profession- aggressive outbursts (Dyer et al., 2006). als need to consider and respond to the impact that changing circum- Previous research remarked that increased severity of acquired stances have on the capacity of informal caregivers to manage their injury is related to higher levels of caregiver stress. For example, Doser workload (McIntyre et al., 2018). and Norub (2016) demonstrated over a long period (from 3 to 6 years) The coronavirus disease 2019 (COVID-19) began spreading in China that the main factor influencing the burden of spouse-caregivers was at the end of 2019 and, to date (October 2021) represents an interna- the severity of the injury of the patients. Considering a shorter period tional health emergency without precedents in terms of its health, eco- after injury (2 years) Laratta et al. (2020) recently identified injury nomic and organizational effects on people’s lives (WHO, 2021). severity being associated with a higher level of spouse-caregiver bur- Spain has been one of the most affected countries in the world in den. Similarly, the CONOCES study concluded that both the burden terms of relative and absolute number of diagnosed cases. On March borne by informal caregivers and the likelihood of them being at a 13, 2020 (legally effective on March 15), the government declared a high risk of burnout (at 3 and 12 months post event) were associated national state of alarm, with regulations targeted to facilitate diag- with the severity of the stroke (Oliva Moreno et al., 2018). Meanwhile nosis, ensure appropriate treatment of cases and reduce the spread complaints on behavioral issues (such as low self-activation, lack of of COVID-19, including measures of national lockdown, confinement initiative or apathy) have been previously reported in survivors of of the population and restricted mobility (Laxe et al., 2020). While stroke (Caeiro et al., 2013). these experiences have been felt globally, the COVID-19 pandemic has Consequently, we hypothesized that during COVID-19, specific introduced additional vulnerability and marginalization to those with emotional (e.g., anger, irritability and impatience) or behavioral (e.g., some type of functional impairment—people with disabilities, chronic lack of initiative and overly dependency) aspects could be identified as illness or frailty due to aging (Kang et al., 2020). sources of increased stress to caregivers when recipients of care are GARCIA-RUDOLPH ET AL . 3 of 13 stratified by cause or by injury severity. Such aspects may be taken as an cerning the care of the person with TBI or stroke, regardless of whether initial step for developing personalized therapeutic interventions pro- he/she lives with the latter and/or (ii) spends most of the time, daily or vided by clinical professionals (e.g., as online remote services) to infor- weekly, accompanying/looking after the person with TBI or stroke. The mal caregivers. informal caregiver might look after no more than one dependent per- Therefore, this study aims at comparing the levels of stress in a set son (De Arroyabe et al., 2013). of 10 emotional and 10 behavioral standardized items, as reported by Every eligible participant was contacted as part of the routine clin- informal family caregivers of people with chronic TBI or stroke living in ical follow-up. Consequently, participants completed the online mea- the community before and during the outbreak of COVID-19. We strat- sures analyzed in this study as part of a virtual visit involving other ified the participants in (i) informal caregivers of people with TBI (IC- assessments, not analyzed in this study. Such assessments include, for TBI) and informal caregivers of people with stroke (IC-STROKE) and (ii) example the Patient Competency Rating Scale (PCRS) to assess self- informal caregivers of mild, moderate or severe recipients of care. awareness following brain injury. Informal caregivers answered their follow-up online assessments within 10 days since contacted; therefore, all assessments were com- 2 MATERIALS AND METHODS pleted between June 2020 and April 2021. 2.1 Study design 2.3 Remote follow-up service and the Head We conducted a prospective observational study analyzing informal Injury Behavior Scale caregivers of individuals with acquired brain injury (TBI or stroke) at chronic phase, with more than 3 years since injury, who were living in The online assessments were implemented during the COVID-19 lock- the community. The individuals with stroke or TBI were selected from down in order to provide a remote follow-up service. Each partici- the electronical health records of Institut Guttmann- Neurorehabilita- pant received the online assessments by an SMS message sent to the tion hospital in Catalonia, Spain. participant’s mobile phone. This SMS was sent by the professional Before COVID-19, it was usual practice for patients and their infor- from the hospital’s Psychosocial Unit in charge of the online follow-up. mal caregivers to periodically (approximately every 18 months) visit The online assessments include the same questionnaires and measure- the hospital. Such in-person follow-up visits aimed to assess their medi- ments as when participants were assessed (before the COVID-19 out- cal and psychosocial status. During COVID-19, in-person follow-up vis- break) in-person during their follow-up visits. its were suspended and online assessments were implemented as part In this study, we focused on one of such measurements: the Head of the hospital’s remote services. Injury Behavior Scale (HIBS) (Godfrey et al., 2003). The Psychoso- Therefore, only informal caregivers of individuals with stroke or TBI cial Unit of the hospital routinely performs HIBS follow-up every registered in the hospital’s electronical health records with at least 3 years. one in-person visit to the hospital (before the COVID-19 outbreak) The HIBS was implemented to assess distress in caregivers of per- and who responded to the online assessment (during COVID- 19) were sons with acquired brain injury. It is a 20-item scale describing com- included in this study. Recruitment period for the online assessment mon psychological problems that occur following brain injury. For each was between June 2020 and April 2021. This study conforms to the of the items in the scale, the caregiver is asked, “Is the behavior a Strengthening the Reporting of Observational Studies in Epidemiology problem?” (yes/no) and “How much distress does this problem cause?.” (STROBE) Guidelines (STROBE, 2021). Distress ratings are recorded for the identified items using a four- point scale: 1 (no distress); 2 (mild distress); 3 (moderate distress) and 4 (severe distress). The HIBS includes two subscales: Emotional 2.2 Participants Regulation and Behavioral Regulation. The Emotional Regulation sub- scale assesses behaviors reflecting impaired emotional control and Eligible participants were informal caregivers of individuals with the occurring during interactions with caregivers (e.g., sudden/rapid mood diagnosis of stroke or TBI (at the moment of injury were aged ≥18), liv- changes, depression, anger and aggression). The Behavioral Regulation ing in the community with electronical health records including com- subscale assesses problems that carry less emotional valence for care- plete data. givers (e.g., lack of control over behavior, inappropriate behavior for Individuals with stroke or TBI were excluded for the following rea- social situations, lack of motivation, or lack of interest in doing things) sons: diagnosis of concomitant comorbidity (e.g., spinal cord injury, (Godfrey et al., 2003). brain tumors and anoxia) and a previous history of another disabling The HIBS has been previously used in assessing emotional and condition or not living in the community. behavioral problems in individuals with chronic TBI (Villalobos et al., To satisfy the informal caregiver criteria, the participant had to be a 2020) (Marsh et al., 2006) or stroke (Orfei et al., 2009). In this study, first-degree relative (parent, sibling or spouse) who had spent at least we used the version of the HIBS adapted to the Spanish language (De 12 months looking after the person with TBI or stroke and who had the Arroyabe et al., 2013). A description of the 20 HIBS items is presented following characteristics: (i) is responsible for and makes decisions con- in Table S1. 4 of 13 GARCIA-RUDOLPH ET AL . 2.4 Clinical and demographic variables TA B L E 1 Demographics and clinical characteristics of all individuals with stroke (n = 76) or traumatic brain injury (n = 46) included in the study Demographics (age, sex, years of education and marital status), as well as time since onset of the injury, were collected. Stroke severity of Total participants the injury was assessed within 24 h before acute phase discharge by Variables (N = 122) the National Institutes of Health Stroke Scale (NIHSS) and stratified Sex (%) as follows: mild (1–4), moderate (NIHSS 5–14) or severe (NIHSS ≥15) Male 71.3 (Williams et al., 2000). Female 28.7 The Glasgow Coma Scale (GCS) (Teasdale et al., 1974) was used to Age at the moment of the online 55.49 (11.82) assess TBI severity at admission and was stratified as mild (14–15), assessment, mean (SD) moderate (9–13) or severe (3-8) (Mena et al., 2011). All data were col- Age <65 at the moment of the online 78.7 lected from the hospital’ electronical health records of the individuals assessment (%) with TBI or stroke. Age ranges at the moment of the online assessment (%) 2.5 Statistical analyses 18–30 1.6 31–45 24.6 All statistical analyses were performed in R-v3.6.3 (64 bits) (The R 46–60 38.5 project, 2021), and level of significance was set at p = .05. Descriptive 61–75 32.0 statistics were used for demographic and clinical characteristics of indi- 76+ 3.3 viduals with stroke or TBI. Responses to HIBS were compared before Time (in days) since lockdown (March 191 (73) and during the COVID-19 outbreak and during it using the McNemar’s 14) to the online assessment, mean test for nominal data (2 × 2 contingency tables with a dichotomous (SD) trait, caused stress [yes, no]), the Wilcoxon ranked test or paired t-test Time (in years) since closest in-person 1.74 (0.88) when appropriate (HIBS total, emotional and behavior subtotals). The assessment to lockdown (March 14), mean (SD) Shapiro Wilk test was used to assess normality, Levene test for homo- geneity of variances and Cohen’s d to assess effects sizes (small effect Time (in years) since injury to online 8.47 (7.48) assessment, mean (SD) size [d = 0.1], medium [d = 0.3] and large effect size [d = 0.5]). Age at the moment of injury in years, 44.74 (14.47) mean (SD) 2.6 Ethical considerations Injury origin, n (%) Traumatic brain injury 46 (37.7%) The study follows the Declaration of Helsinki and was approved by the Stroke 76 (62.3%) Ethics Committee of Clinical Research of Institut Guttmann- Neurore- Type of stroke, n (%) habilitation hospital. The participants were anonymized and nonidenti- fiable. Hemorrhagic stroke 36 (29.5%) Ischemic stroke 40 (32.8%) 3 RESULTS Severity of stroke (NIHSS) (%) Mild 13.8 The initial number of eligible participants, considering the criteria Moderate 43.0 described in Section 2.2. was n = 191, four of them had difficulties Severe 43.2 in understanding or expressing in the Spanish language as detected Severity of traumatic brain injury by members of the research team, which prevented him/her from (GCS) (%) being able to collaborate. One hundred and eighty-seven participants Mild 15.6 received the SMS in their mobile phones, 24 (12.8%) were not a first- Moderate 11.1 degree relative (parent, sibling or spouse) who had spent at least Severe 73.3 12 months looking after the person with TBI or stroke, 3 (1.6%) were FIM in-person assessment, mean (SD) looking after more than one dependent person, 11 (5.8%) did not have Cognitive FIM 26.48 (8.82) an available Functional Independence Measure (FIM) in person assess- Motor FIM 61.32 (26.16) ment and 27 (14.4%) did not complete the online HIBS assessment. Consequently, a total of 122 informal caregivers participated in the Total FIM 87.81 (33.30) study, 76 (62.3%) were IC-STROKE and 46 (37.7%) were IC-TBI. Time in years since FIM in-person 0.81 (1.31) Table 1 presents the demographics and clinical characteristics of assessment to the online assessment, mean (SD) the individuals with TBI and stroke. The mean age at the moment of (Continues) GARCIA-RUDOLPH ET AL . 5 of 13 TA B L E 1 (Continued) online assessment was 55 (11) years, and 70% of the individuals were men. Total participants Variables (N = 122) In relation to the injury severity, 70% of the individuals with TBI Years of education at the moment of the were severe, and 86% of the individuals with stroke were moderate or online assessment (%) severe. The mean time since lockdown (March 14) to the online assess- Read and write (<2 years) 6.6 ment was 191 (73) days. The mean time since the closest in-person assessment to lockdown (March 14) was 1.74 (0.88) years. The mean Primary (2–5 years) 38.5 time since injury to online assessment was 8.47(7.48) years. Secondary (6–12 years) 29.5 Higher (>13 years) 25.4 Marital status. Married (%) 64.8 3.1 Stratification by IC-TBI or IC-STROKE Location where respondents were living at the moment of answering the We then compared the emotional regulation subtotal, the behavioral online assessment (%) regulation subtotal and the total HIBS score for IC-TBI (N = 46, 37.7%) Barcelona 72.8 and IC-STROKE (N = 76, 62.3%), as presented in Table 2. Girona 10.7 When considering emotional regulation subtotals, no significant dif- Tarragona 9.9 ferences were found in IC-TBI (p = .109), but differences were sig- Lérida 6.6 nificant for IC-STROKE (p = .001) and with the highest effect size Note: All characteristics are presented as percentages (%), unless otherwise d = −0.365 indicated. Meanwhile, the opposed is observed when considering behav- Abbreviations: FIM, Functional Independence Measure; NIHSS, National ioral regulation subtotals, no significant differences were found in institute of Health Stroke Scale; GCS, Glasgow Comma Scale. IC-STROKE (p = .072), but differences were significant for IC-TBI (p = .027). TA B L E 2 Paired comparisons for precoronavirus decease 2019 (COVID-19) assessments and during COVID-19 assessments for Head Injury Behavior Scale (HIBS) emotional, behavioral and total Wilcoxon Shapiro-Wilk Signed Wilcoxon SE CI mean normality rank test Signed rank Effect Stratification Subscale COVID-19 Median Mean (SD) Mean 0.95% test (p) (W) test (p) size (d) All (N = 122) Emotional Before 5.50 8.09 (8.47) 0.77 1.52 <.0001 1801 <.001 −0.317 During 9.00 11.25 (10.71) 0.97 1.92 <.0001 Behavioral Before 6.00 8.47 (8.37) 0.76 1.50 <.0001 2060 .004 −0.256 During 9.00 10.82 (9.44) 0.85 1.69 <.0001 Total Before 13.50 16.56 (15.42) 1.40 2.76 <.0001 1853.5 <.001 −0.323 During 18.00 22.07 (18.63) 1.69 3.34 <.0001 IC-TBI (N = 46) Emotional Before 9.00 10.00 (9.30) 1.37 2.76 <.0001 340 .109 −0.236 During 9.50 12.02 (10.36) 1.53 3.08 <.0001 Behavioral Before 8.00 9.91 (8.20) 1.21 2.44 <.0001 305.5 .027 −0.325 During 11.50 12.85 (9.40) 1.39 2.79 <.0001 Total Before 17.00 19.91 (15.79) 2.33 4.69 <.0001 305.5 .027 −0.325 During 21.50 24.87 (17.65) 2.60 5.24 <.0001 IC-STROKE Emotional Before 4.00 6.93 (7.76) 0.89 1.77 <.0001 584.5 .001 −0.365 (N = 76) During 7.00 10.79 (10.97) 1.26 2.51 <.0001 Behavioral Before 5.00 7.59 (8.40) 0.96 1.92 <.0001 797 .072 −0.206 During 8.00 9.59 (9.32) 1.07 2.13 <.0001 Total Before 9.00 14.53 (14.92) 1.71 3.41 <.0001 663 .004 −0.323 During 15.00 20.38 (19.11) 2.19 4.37 <.0001 Abbreviations: IC-TBI, informal caregivers of people with TBI; IC-STROKE, informal caregivers of people with stroke. 6 of 13 GARCIA-RUDOLPH ET AL . TA B L E 3 Comparison of demographics and clinical characteristics of individuals with stroke (n = 76) and traumatic brain injury (n = 46) Variables Stroke (N = 76) TBI (N = 46) p Sex (%) .935 Male 71.1 71.7 Female 28.9 28.3 Age at the moment of the online assessment, mean (SD) 59.73 (9.03) 48.49 (12.62) <.001 Age >65 at the moment of the online assessment (%) 26.3 13.0 .083 Age ranges at the moment of the online assessment (%) <.001 18–30 0 4.3 31–45 9.2 50.0 46–60 47.4 23.9 61–75 39.5 19.6 76+ 3.9 2.2 Time (in days) since lockdown (March 14) to the online 200 (71) 178 (73) .120 assessment, mean (SD) Time (in years) since closest in-person assessment to 1.73 (0.92) 1.76 (0.83) .334 lockdown (March 14), mean (SD) Time (in years) since injury to online assessment, mean (SD) 6.74 (7.30) 11.34 (6.93) <.001 Age at the moment of injury in years, mean (SD) 50.71 (9.25) 34.89 (16.16) <.001 Severity (%) .642 Mild 13.8 15.6 Moderately severe and severe 86.2 84.4 FIM in-person assessment, mean (SD) Cognitive FIM 28.13 (8.04) 23.76 (9.45) .008 Motor FIM 63.50 (23.01) 57.73 (30.61) .719 Total FIM 91.63 (29.09) 81.50 (38.80) .378 Time in years since FIM in-person assessment to the online 0.80 (1.20) 0.82 (1.50) .395 assessment, mean (SD) Years of education at the moment of online assessment (%) .130 Read and write (<2 years) 9.2 2.2 Primary (2–5 years) 35.5 43.5 Secondary (6–12 years) 34.2 21.7 Higher (>13 years) 21.1 32.6 Marital status. Married (%) 81.6 37.0 <.001 Support in ADLs .210 Daily: 24 h 32.3 35.6 Daily: 12–23 h 6.5 11.1 Daily:6 – 11 h 8.1 2.2 Daily: 3–5 h 19.4 6.7 Daily: less than 3 h 14.5 15.6 Occasional 6.5 17.8 Not needed 12.9 11.1 Location where informal caregivers were living at the .483 moment of answering the online assessment (%) Barcelona 73.3 71.7 Girona 13.3 6.5 Tarragona 8.0 13.0 Lérida 5.3 8.7 All characteristics are presented as percentages (%), unless otherwise indicated. Bold values are for p < 0.05. Abbreviations: ADLs: Activities of Daily Living; FIM, Functional Independence Measure; TBI, traumatic brain injury GARCIA-RUDOLPH ET AL . 7 of 13 TA B L E 4 Head Injury Behavior Scale (HIBS) items comparison (McMenar test) before and during coronavirus disease 2019 (COVID-19) as reported by informal caregivers of people with stroke (IC-STROKE; n = 76) and informal caregivers of people with TBI (IC-TBI; n = 46) when answering the question “does this item cause you mild, moderate or severe stress?” IC-STROKE (N = 76) IC-TBI (N = 46) Before During Before During Id Item Yes (%) Yes (%) p Yes (%) Yes (%) p 1 Anger; difficulty in controlling temper 26.3 27.6 .998 43.5 45.7 .998 2 Impatience; upset when needs not easily met 35.5 52.6 .020 50.0 54.3 .772 3 Frequent complaining 15.8 34.2 .002 28.3 34.8 .546 4 Aggression; violent behavior 9.2 14.5 .342 17.4 19.6 .998 6 Argumentative; often disputes topics 13.2 31.6 .005 30.4 34.8 .789 14 Irritable; snappy; grumpy 15.8 27.6 .0664 26.1 34.8 .386 15 Sudden/rapid mood change 19.7 38.2 .005 32.6 50.0 .061 16 Anxious; tensed; uptight 25.0 32.9 .326 39.1 28.3 .301 17 Depressed; low mood 26.3 35.5 .190 34.8 39.1 .813 19 Overly sensitive; easily upset 18.4 36.8 .014 28.3 32.6 .789 5 Impulsivity; does things without thinking 19.7 30.3 .080 32.6 52.2 .038 7 Lacks control over behavior; behavior is inappropriate 18.4 25.0 .332 19.6 34.8 .096 for social situations 8 Overly dependent; relies on others unnecessarily 25.0 38.2 .033 30.4 47.8 .135 9 Poor decision making; does not think of consequences 27.6 31.6 .662 32.6 45.7 .286 10 Childish; at times behavior is immature 30.3 35.5 .540 23.9 39.1 .145 11 Poor insight; refuses to admit difficulties 25.0 30.3 .522 32.6 39.1 .605 12 Difficulty in becoming interested in things 13.2 22.4 .121 23.9 34.8 .301 13 Lack of initiative; does not think for him/herself 18.4 28.9 .135 32.6 34.8 .998 18 Irresponsible; cannot always be trusted 19.7 25.0 .479 28.3 39.1 .301 20 Lacks motivation; lack of interest in doing things 28.9 31.6 .850 32.6 23.9 .479 Note: HIBS-emotional items: Id = 1, 2, 3, 4, 6, 14, 15, 16, 17, 19, HIBS-behavioral items: Id = 5, 7, 8, 9, 10, 11, 12, 13, 18, 20. We then compared individuals with stroke with individuals with Meanwhile, for IC-STROKE, significant differences were reported TBI considering demographics and clinical variables, as presented in in six items: impatience, frequent complaining, often disputes topics, Table 3. mood change, overly sensitive and overly dependent. Significant differences were found in age at the moment of online A graphical representation of Table 4 (considering only the emo- assessment. Individuals with TBI were significantly younger (p < .001) tional regulation items) is presented in Figure 1. with 50% of them between 31 and 45 years old at the moment of the online assessment, whereas only 9.2% of the individuals with stroke were between 31 and 45 years old at the moment of online assessment 3.2 Stratification by injury severity (p < .001). When comparing functional independence, as assessed using the We then compared the emotional regulation subtotal, the behavioral FIM, cognitive FIM was significantly higher in individuals with stroke regulation subtotal and the total HIBS for informal caregivers of the (p = .008). recipients of care, now stratified according to their injury severity (as We further compared each of the 20 HIBS items separately for IC- defined in Section 2.4). STROKE and IC-TBI, before and during COVID-19, in order to iden- When considering individuals with mild injury (N = 18, 14.7%), no tify specific items causing (mild, moderate or severe) stress, as detailed significant differences were found in the emotional regulation subtotal in Table 4. For IC-TBI only in one of them (item 5: Impulsivity; does (p = .273), and the behavioral regulation subtotal (p = .09) either the things without thinking), a significant increase of the level of stress was total HIBS (p = .23). reported: 32.6% of the informal caregivers had stress due to this item When considering individuals with moderate injury (N = 35, 28.7%), before and during COVID-19, and the percentage of informal care- we found significant differences in the emotional regulation subtotal givers who had stress due to this item significantly increased to 52.2%, (p = .04). No significant differences were found in the behavioral regu- as detailed in Table 4. lation subtotal (p = .62) either the total HIBS (p = .18). 8 of 13 GARCIA-RUDOLPH ET AL . stroke tbi 1. Anger; difficulty controlling temper 26.3 27.6 43.5 45.7 2. Impatience; upset when needs not easily met 35.5 52.6 50 54.3 3. Frequent complaining 15.8 34.2 28.3 34.8 4. Aggression; violent behaviour 9.2 14.5 17.4 19.6 when 6. Argumentative; often disputes topics 13.2 31.6 30.4 34.8 item after 14. Irritable; snappy; grumpy 15.8 27.6 26.1 34.8 before 15. Sudden/rapid mood change 19.7 38.2 32.6 50 16. Anxious; tense; uptight 25 32.9 39.1 28.3 17. Depressed; low mood 26.3 35.5 34.8 39.1 19. Overly sensitive; easily upset 18.4 36.8 28.3 32.6 0 25 50 75 100 0 25 50 75 100 stress F I G U R E 1 Head Injury Behavior Scale (HIBS)-emotional items’ comparison before and during coronavirus decease 2019 (COVID-19) as reported by informal caregivers of individuals with stroke (n = 76) and individuals with traumatic brain injury (TBI; n = 46) TA B L E 5 Paired comparisons for precoronavirus disease 2019 (COVID-19) assessments and during COVID-19 assessments for Head Injury Behavior Scale (HIBS) emotional, behavioral and total stratified by injury severity Wilcoxon Wilcoxon Shapiro-Wilk Signed rank Signed rank SE CI mean normality test (W) or test or t-test Effect Stratification Dimension COVID-19 Median Mean (SD) Mean 0.95% test (p) t-test (p) size (d) Mild (N = 18) Emotional Before 6.00 7.73 (6.77) 1.74 3.75 .15 −1.13 .273 −0.18 During 7.00 11.20 (12.55) 3.24 6.95 .01 Behavioral Before 6.00 7.40 (7.22) 1.86 4.00 .04 21.5 .09 −0.19 During 9.00 10.13 (8.91) 2.30 4.93 .04 Total Before 14.00 15.13 (13.01) 3.36 7.20 .22 −1.24 .23 −0.19 During 15.00 21.33 (20.91) 5.39 11.57 0.05 Moderate Emotional Before 5.00 7.86 (7.78) 1.42 2.90 <.001 112.5 .04 −0.37 (N = 35) During 10.00 12.43 (10.98) 2.01 4.10 .01 Behavioral Before 5.00 7.17 (8.28) 1.51 3.09 <.001 168 .62 −0.10 During 6.00 9.23 (9.62) 1.76 3.59 .001 Total Before 9.50 15.03 (15.37) 2.81 5.74 <.001 133 .18 −0.24 During 17.00 21.66 (19.32) 3.53 7.21 .002 Severe Emotional Before 5.50 8.07 (9.39) 1.23 2.47 <.001 480.5 .03 −0.28 (N = 69) During 7.00 10.36 (9.76) 1.28 2.57 <.001 Behavioral Before 6.00 8.56 (8.32) 1.09 2.19 <.001 461.5 .02 −0.29 During 9.50 11.01 (9.33) 1.22 2.45 <.001 Total Before 13.50 16.64 (15.79) 2.07 4.15 <.001 457.5 .01 −0.32 During 18.50 21.38 (16.95) 2.23 4.46 .001 Finally, when considering individuals with severe injury (N = 69, Injury severity was assessed within 24 h before acute phase dis- 56.6%), we found significant differences in all three of them: the charge, and the mean length of stay in acute phase was 21.3 (8.4) emotional regulation subtotal (p = .03), the behavioral regulation days. Figure 2 presents the total FIM scores boxplots for each sever- subtotal (p = .02) and the total HIBS (p = .01), as presented in ity level, showing that individuals with higher severity still get lower Table 5. FIM scores despite the FIM scores were assessed several years later GARCIA-RUDOLPH ET AL . 9 of 13 stroke, stratified by cause of injury and by injury severity of the recipi- ents of care. A recent survey conducted in Nashville, United States, by Morrow et al. (2021) on 47 individuals in the chronic phase of moderate-severe TBI reported that for 51.06% of the participants, the pandemic has affected their sense of mental and physical well-being. In our case, we analyzed 20 psychological items and only in one of them a significant increase of the level of stress was reported (Impulsivity; does things without thinking). Meanwhile as detailed in Table 4, in caregivers of people with stroke, significant differences were reported in six items: impatience, frequent complaining, often disputes topics, mood change, overly sensitive and overly dependent. Prepandemic studies among family caregivers of community dwelling stroke survivors report that informal caregivers’ total burden score was largely driven by their feel- ings of overly dependence (Morimoto et al., 2001), being dependency and immature behavior major causes of stress (Dankner et al., 2016). Cohen et al. (2021) analyzed self-reported changes in burden (CB) and intensity due to COVID-19 (n = 835) of informal caregivers living F I G U R E 2 Total Functional Independence Measure (FIM) in the United States. They found that men with higher initial levels of boxplots stratified by injury severity levels confidence interval were more likely to have an increase in CB due to the pandemic, but the association was not significant for women. There than the injury severity assessments. As presented in Table 1, the time is no clear explanation for this finding although it may be due to gen- (in years) since injury to the online assessment was 8.47 (7.48) years, der differences in resilience among informal caregivers. Female care- whereas the time in years since the FIM in-person assessment to the givers may be more resilient than male caregivers (Gaugler et al., 2007), online assessment was 0.81 (1.31) years. and this resilience may become magnified under periods of extreme As shown in Figure 2, individuals with mild severity get significantly stress and uncertainty, such as the COVID-19 pandemic. In our case, higher total FIM scores when compared with individuals with severe as presented in Table 1, 71.3% of care recipients were males, suggest- injury, and this is represented with two asterisks in Figure 2. Differ- ing that most of their informal caregivers could be females, though we ences in total FIM scores are not significant when comparing mild with did not collect demographic data on the informal caregivers. Neverthe- moderate and moderate with severe. Nevertheless, Figure 2 clearly less, it is known that women are more likely than men to be informal shows that as severity increases, the FIM score decreases. caregivers, among the whole population of informal caregivers them- We further compared each of the 20 HIBS items separately for selves (Bauer et al., 2015). Cohen et al., concluded that a notable find- moderate and severe recipients of care, before and during COVID-19, ing of their study was that higher initial CB was associated with a higher in order to identify specific items causing (mild, moderate or severe) likelihood of increased CB during the COVID-19 pandemic. This find- stress, as detailed in Table 6. ing may be counterintuitive, as one could expect that there is a poten- For recipients of care with moderate injury, a significant increase of tial for a ceiling effect of CB—in other words, CB could not increase the level of stress was reported by the informal caregivers in two emo- substantially due to the pandemic simply because it was already high tional items (frequent complaining and sudden/rapid mood change). (Hagell et al., 2017). One possible explanation for this finding is that For severe recipients of care, a significant increase of the level of stress the extra burdens of the pandemic, whether due to increased anxiety was reported in two items, one emotional (argumentative; often dis- or other stressors, magnified the effects of caregiving on those with an putes topics) and the other behavioral (impulsivity; does things without already high level of CB. That was not the case in our IC-TBI sample, a thinking). ceiling effect may be occurring for IC-TBI, causing that an already high We did not include recipients of care with mild injury severity in level of stress (as shown in Figure 1) masked the effect of the pandemic Table 6 because (as reported in Table 5) no significant differences were situation. found for them in the emotional regulation subtotal and the behav- Seth et al. (2021) compared prepandemic (January 2020, n = 221) ioral regulation subtotal either the total HIBS. Besides, only 14.7% of and early-pandemic caregiving samples (April–June 2020, n = 177) in all recipients of care presented mild injury severity. the United States and Latin America. They found that COVID-19 did not seem to affect depression and self-efficacy, nor did it affect partic- 4 DISCUSSION ipant’s perception of their general overall health. The lack of impact of COVID-19 on depression or overall health could either be due to the We studied the impact of COVID-19 from a psychological perspective fact that the disease or threat of the disease does not appear to affect (using the HIBS 10 emotional and 10 behavioral items), on informal these parameters or that they were quite high to begin with and maybe caregivers of individuals living in the community with chronic TBI or had already reached a near-ceiling effect. An important acknowledged 10 of 13 GARCIA-RUDOLPH ET AL . TA B L E 6 Head Injury Behavior Scale (HIBS) items comparison (McMenar test) before and during coronavirus disease 2019 (COVID-19) as reported by informal caregivers for moderate (n = 35) and severe (n = 69) recipients of care when answering the question “does this item cause you mild, moderate or severe stress?” Moderate (N = 35) Severe (N = 69) Before During Before During Id Item Yes (%) Yes (%) p Yes (%) Yes (%) p 1 Anger; difficulty controlling temper 30.0 40.0 .505 34.5 34.5 1.00 2 Impatience; upset when needs not easily met 43.3 60.0 .227 37.9 50.0 .121 3 Frequent complaining 20.0 43.3 .045 18.9 27.6 .182 4 Aggression; violent behavior 10.0 13.3 .998 12.1 15.5 .683 6 Argumentative; often disputes topics 23.3 33.3 .546 15.5 32.8 .03 14 Irritable; snappy; grumpy 20.0 36.6 .182 17.2 27.6 .181 15 Sudden/rapid mood change 26.7 56.7 .026 27.6 36.2 .267 16 Anxious; tensed; uptight 33.3 43.3 .579 31.0 27.6 .802 17 Depressed; low mood 33.3 43.3 .579 31.0 34.5 .823 19 Overly sensitive; easily upset 26.7 33.3 .772 22.4 31.0 .332 5 Impulsivity; does things without thinking 30.0 33.3 .998 17.2 37.9 .005 7 Lacks control over behavior; behavior is inappropriate for social situations 13.3 23.3 .505 17.2 27.6 .181 8 Overly dependent; relies on others unnecessarily; 23.3 40.0 .130 34.5 50.0 .095 9 Poor decision making; does not think of consequences 23.3 33.3 .449 24.1 39.6 .109 10 Childish; at times behavior is immature 23.3 30.0 .723 29.3 37.9 .358 11 Poor insight; refuses to admit difficulties 23.3 26.7 .998 27.5 34.4 .453 12 Difficulty in becoming interested in things 13.3 26.7 .220 20.7 25.9 .627 13 Lack of initiative; does not think for him/herself 13.3 30.0 .182 29.3 32.7 .823 18 Irresponsible; cannot always be trusted 23.3 26.7 .998 17.2 27.6 .181 20 Lacks motivation; lack of interest in doing things 30.0 33.3 .998 27.6 32.7 .662 Note: HIBS-emotional items: Id = 1, 2, 3, 4, 6, 14, 15, 16,17 ,19, HIBS-behavioral items: Id = 5, 7, 8, 9, 10, 11, 12, 13, 18, 20. limitation of the study was that authors were not able to determine both groups (PWA vs. control). Lower rates of depression and anxiety whether the caregivers were living with the care recipients and if they were found in PWA compared to the healthy group. Pisano et al. con- were the sole caregivers of the care recipients. clude that this evidence which, at first glance, seems to suggest that Budnick et al. (2021) reported from an ad hoc survey (n = 1000) in PWA have been partially spared from the impact of COVID-19, actu- Germany (April 21 to May 2, 2020) that informal caregivers during the ally masks a dramatic situation that has always characterized this pop- COVID-19 pandemic perceive additional burden. ulation. Indeed, given that PWA already live in a state of social isola- Rodrigues et al. (2021) reported the impact of the pandemic on tion and emotional instability, these conditions might have, paradoxi- informal caregiving in Austria. They used a pre- and postonset of cally, limited the effects of the coronavirus (Pisano et al., 2020). the pandemic research design based on a representative survey car- Our nonsignificant differences in the informal caregivers of individ- ried out in Austria in June 2020 (N = 2000) in combination with uals with TBI in 19 of the 20 items presented in Table 4 may be due to comparable 2015 data from the European Social Survey. Their find- a similar masking effect, as shown in Figure 1 their stress levels were ings suggest that both the prevalence and intensity of informal care already high before the COVID-19 outbreak. In relation to informal remained stable after the onset of the first wave of the pandemic in caregivers of individuals with stroke, we found significant differences Austria. in five out of the 10 HIBS emotional items, indicating a clear impact of We were not able to find studies specifically addressing the impact the pandemic situation on them. Though, we did not stratify them con- of COVID-19 on informal caregivers of people with TBI or stroke. sidering informal caregivers of individuals with aphasia. Pisano et al. (2020) compared 73 individuals with poststroke apha- Injury severity has been reported to play a large role in the type sia (PWA) in chronic phase and 81 matched healthy controls in Italy of sequelae that result following TBI and thus influence the care- (Rome and Turin). The comparison between the two different time giver/family’s function over time (Thompson et al., 2009). In our points (1 month before and 1 month after the COVID-9 lockdown) case, for mild injuries we identified no differences before and during led to a significant increase in depression and anxiety symptoms in COVID-19. For moderate injuries, we identified differences in the total GARCIA-RUDOLPH ET AL . 11 of 13 emotional regulation score and when injuries were severe, we iden- cannot determine questionnaire filling time and participants may aban- tified differences in the three of the assessed totals. Therefore, our don the survey giving partial data; if the participants have a doubt, results suggest that for recipients of care with moderate injuries, sup- researcher cannot clear it immediately. In our case, participants already port to informal caregivers should be focused on emotional aspects knew the questionnaires, because they have already answered them (mainly in frequent complaining and sudden/rapid mood change as during previous in-person visits; therefore, cons were minimized. Fur- shown in Table 6) rather than on behavioral. Meanwhile, for severe thermore, as remarked by Pisano et al. and Morrow et al., access to injuries, support should be focused on both emotional (specifically in home-based remote services is recommended during these pandemic argumentative; often disputes topics) and behavioral aspects (specifi- times. cally in impulsivity; does things without thinking). Future work includes (i) analyzing informal caregivers’ demograph- Acquired brain injury is considered a stressor that changes care- ical variables, psychological status (e.g., HADS assessment) and bur- giver’s psychosocial functioning (Perlesz et al., 2000). Higher distress den (e.g., ZARIT assessment), (ii) conducting a specific analysis on care- and lower life satisfaction of caregivers are associated with low long- givers of individuals with aphasia (approximately 40% of the hospital term functional outcomes of persons with acquired brain injury, even admissions) and (iii) in Table S2, we included a stratification by age in after accounting for injury severity and cognitive functioning of care two groups (≤54 years (N = 55) and > 55 years (N = 67)) and found that recipients (Vangel et al., 2011). As the person with acquired brain injury differences were nonsignificant in the HIBS behavioral subtotal for the and his or her caregiver belongs to the same family system, both are ≥55 years group, whereas in the younger group, differences were sig- influenced and influential agents (Vangel et al., 2011). Our findings nificant in both emotional and behavioral subtotals, leaving room for are in line with such results; furthermore, in Table S3 we analyzed a future analysis. stratification in two groups according to their FIM assessments (inde- pendent vs. dependent). The emotional, behavioral subtotals and total HIBS comparisons yielded that the informal caregivers to the depen- 5 CONCLUSIONS dent group presented higher effect sizes in all three of them. Several limitations to this study are worth mentioning. First, the For the first time, we reported results of the COVID-19 impact from a data were collected from informal caregivers of individuals living in the psychological perspective, considering 10 emotional and 10 behavioral community but who had previously undertaken rehabilitation in one items on informal family caregivers of individuals with stroke or TBI liv- single tertiary center in Catalonia. As presented in Table 1, 72.8% of ing in the community. We identified six specific HIBS items that have them were living in the province of Barcelona. Therefore, the general- been significantly impacted by the COVID-19 in informal caregivers of ization of these results should be considered carefully. Nevertheless, individuals with stroke. We found one item in caregivers of individuals assessments by standardized tools (HIBS, FIM, NIHSS and GCS) allow with TBI, suggesting in their case a possible masking effect due to a pre- for similar comparative studies, and the restricted physical locations existing situation of emotional instability. allow for controlled variability in regional pandemic circumstances. When considering the severity of the recipients of care, we iden- Second, the evolving nature of the pandemic may produce psy- tified two emotional items for informal caregivers of moderate recip- chological effects, for example the COVID-19 vaccination campaign ients of care and one emotional as well as one behavioral item for started on December 27, 2020 in Spain (Vaccination Program, 2021). severe recipients of care. We identified a higher impact on emotional The initial phase of vaccination plan covered residents of senior homes and behavioral subtotals as well as in total HIBS as severity of injury and their carers and continued with healthcare workers and adults with increased, further confirming them to be closely related to their long- major dependencies. Therefore, it did not involve any of the partici- term functional independence outcomes pants in this study, but it could somehow impact in their psychologi- Our results can be used to suggest possible therapeutic interven- cal status. Other contextual circumstances may have had an emotional tions or support provided by clinicians to informal caregivers, specifi- impact (e.g., summer in Spain from June 2020 to September 2020). cally targeting the identified items or subtotals. Third, male gender accounts for about 70% of the individuals with stroke and individuals with TBI, suggesting a sex bias. Nevertheless, the FINANCIAL SUPPORT proportion is similar to recent studies in similar settings (as presented This research was partially funded by H2020 Personalised Medicine by in Supporting Information). Predictive Modeling in Stroke for better Quality of Life (PRECISE4Q) Fourth, demographic data (e.g., age, gender, level of education) were Grant Nr 777107. not collected on informal caregivers. The online assessments were implemented during the COVID-19 lockdown in order to provide a DATA AVAILABILITY STATEMENT remote follow-up service, as performed in-person before the COVID- The data that support the findings of this study are available from the 19 outbreak. Therefore, remote service included the same psycholog- corresponding author upon reasonable request. ical assessments performed as in-person visits, which did not collect demographic data on informal caregivers. PEER REVIEW Fifth, online assessments have been criticized in previous studies. The peer review history for this article is available at https://publons. Several cons have been reported (Silva Durga, 2019): the researcher com/publon/10.1002/brb3.2440 12 of 13 GARCIA-RUDOLPH ET AL . ORCID sectional study. 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