TYPE Original Research PUBLISHED 26 January 2023 DOI 10.3389/fpsyg.2023.1067477 Stress and coping strategies of OPEN ACCESS families of pediatric solid organ transplant recipients in times of EDITED BY Sara Invitto, University of Salento, Italy REVIEWED BY pandemic Flora Koliouli, Aristotle University of Thessaloniki, Greece Heang Lim, Mireia Forner-Puntonet 1,2,3,4*, Laura Gisbert-Gustemps 1,2,3,4, C. S. Mott Children's Hospital, United States Eudald Castell-Panisello 1, Mauricio Larrarte 5, Jesús Quintero 5, *CORRESPONDENCE Gema Ariceta 6, Ferran Gran 7, Ignacio Iglesias-Serrano 8, Mireia Forner-Puntonet mireia.forner@vallhebron.cat Annabella Garcia-Morán 1,2, Gemma Español-Martín 1,2,3,4, SPECIALTY SECTION Pol Ibañez-Jimenez 2,4 and Josep Antoni Ramos-Quiroga 1,2,3,4 This article was submitted to Psychology for Clinical Settings, 1 Department of Mental Health, Hospital Universitari Vall d’Hebron, Barcelona, Catalonia, Spain, 2 Group of a section of the journal Psychiatry, Mental Health and Addictions, Vall d’Hebron Research Institute (VHIR), Barcelona, Catalonia, Frontiers in Psychology Spain, 3 Department of Psychiatry and Forensic Medicine, Universitat Autònoma de Barcelona, Catalonia, Spain, 4 Biomedical Network Research Centre on Mental Health (CIBERSAM), Madrid, Spain, 5 Pediatric RECEIVED 12October 2022 Hepatology and Liver Transplant Department, Hospital Universitari Vall d'Hebron, Universitat Autònoma de ACCEPTED 03 January 2023 Barcelona, Barcelona, Catalonia, Spain, 6 Pediatric Nephrology Department, Hospital Universitari Vall PUBLISHED 26 January 2023 d’Hebron, Universitat Autònoma de Barcelona, Barcelona, Catalonia, Spain, 7 Pediatric Cardiology CITATION Department, Hospital Universitari Vall d’Hebron, Barcelona, Catalonia, Spain, 8 Pediatric Respiratory Medicine Forner-Puntonet M, Gisbert-Gustemps L, Department, Hospital Universitari Vall d’Hebron, Barcelona, Catalonia, Spain Castell-Panisello E, Larrarte M, Quintero J, Ariceta G, Gran F, Iglesias-Serrano I, Garcia-Morán A, Español-Martín G, Ibañez-Jimenez P and Ramos-Quiroga JA (2023) Stress and coping Objective: Pediatric solid organ transplantation (SOT) is a chronic condition strategies of families of pediatric solid organ that impacts the whole family system. The objective of this study is to evaluate transplant recipients in times of pandemic. psychopathology, family stress, and coping strategies in families of SOT recipients Front. Psychol. 14:1067477. doi: 10.3389/fpsyg.2023.1067477 compared to families of healthy children and adolescents. Moreover, it analyzes if the stress related to the COVID-19 pandemic has had an additional impact on these COPYRIGHT © 2023 Forner-Puntonet, Gisbert-Gustemps, families. Castell-Panisello, Larrarte, Quintero, Ariceta, Methods: The sample was recruited between May and July 2021, during the fourth Gran, Iglesias-Serrano, Garcia-Morán, Español- Martín, Ibañez-Jimenez and Ramos-Quiroga. and fifth wave of the pandemic in Spain. It consisted of 102 families, 51 with a pediatric This is an open-access article distributed under recipient who had undergone a SOT (liver, kidney, heart, or lung) and 51 healthy the terms of the Creative Commons Attribution controls, matched by child age and gender. A primary caregiver from each family License (CC BY). The use, distribution or reproduction in other forums is permitted, answered an online sociodemographic questionnaire and different tests to evaluate provided the original author(s) and the family stress, depression, anxiety, coping strategies, and effects of the pandemic on copyright owner(s) are credited and that the the family. original publication in this journal is cited, in accordance with accepted academic practice. Results: Caregivers were mostly mothers (89.2%). Families of SOT recipients showed No use, distribution or reproduction is greater anxiety (U=863.5, p=0.003) and more total stress, stress related to childcare permitted which does not comply with these terms. (t=−2.043; p=0.045), and parent–child interaction stress (U=355.5, p=0.015). SOT families used more avoidance strategies, specifically denial (U=889.5; p=0.010) and abandonment of coping efforts (U=1,013; p=0.047), more religious strategies (U=792.5; p=0.031), and fewer social support coping strategies (t=2.098; p=0.038). No differences were found between groups in terms of exposure, impact, and distress more than 1 year after the start of the pandemic. Conclusion: SOT families showed clinical levels of anxiety, more parent–child interaction stress, more difficulties in taking care of their child, more avoidance and religious strategies, and less use of social support strategies, even 4 years after transplantation. The pandemic did not have an additional differential effect on SOT families. Caregivers of SOT patients can benefit from psychological interventions focused on parents’ mental health, parent–child connectedness, skill building, and social support aid groups, with attention to multiculturalism and promoting a better balance between caregivers. There is a need for family interventions that are Frontiers in Psychology 01 frontiersin.org Forner-Puntonet et al. 10.3389/fpsyg.2023.1067477 maintained over time. Strategies that offer this support to families through digital resources can facilitate adjustment to chronic illness, especially in pandemic times. KEYWORDS pediatric transplantation, solid organ transplantation, family stress, coping strategies, COVID-19, pandemic Introduction Additionally, there is a consistent association between parent and family functioning and child health-related factors, such as adherence, Pediatric solid organ transplantation (SOT) is the treatment of barriers to medications, and number of hospitalizations (Cousino et al., choice for end-stage organ failure (Imam et al., 2020), which allows the 2017). These results reinforce the importance of evaluating family medical situation of a child to change from experiencing a life- functioning, stress, resources, and psychopathology to offer specific threatening disease to having a chronic health condition (Annunziato treatments. Currently, in Spain, psychological support or treatment for et al., 2012). Caregivers are an essential figure in SOT; even so, we still families of pediatric transplant patients is scarce. A pre-transplant have limited understanding of the experience of caregiving through the assessment and some initial post-transplant follow-up are usually entire process of transplantation, and there are limited data examining carried out. However, interventions with greater continuity over time the long-term impact. Therefore, it is a high research priority (Jesse are lacking, particularly considering that it is a chronic disease that can et al., 2021). affect children and family day-to-day life. In general, parents of children with chronic illnesses experience Finally, we must point out that the COVID-19 pandemic has been greater parenting stress than parents of healthy children (Cousino and a major burden on families (Fegert et al., 2020); parents of children with Hazen, 2013). Specifically, in pediatric SOT, although it improves physical or mental conditions in particular have reported more parental quantity and quality of life, pre-transplantation and post-transplantation burnout and less perceived social support (Fontanesi et al., 2020). In line produce many stressors and burdens for patients and families (Cousino with this, Zhao et al. (2020) found that these caregivers presented higher et al., 2017). The long-term nature of transplantation and post-transplant prevalence of depressive and anxious symptoms in a pandemic context. medical care creates more stress than what is encountered in families In a recent study, Forner-Puntonet et al. (2021) found that, during the that go through a single surgery event, resulting in prolonged parental first wave of the pandemic, families of SOT recipients had exposed stress (Farley et al., 2007). themselves less and protected themselves more from COVID-19 than Although these families may demonstrate resilience in coping with the families of healthy children did, probably because they were used to stressors, the demanding challenges and responsibilities beyond the prevention measures and saw contagion as a graver risk. Additionally, usual concerns of raising a child and the uncertainty regarding the the families of SOT recipients perceived isolation and prevention transplant process may negatively impact family functioning (Cousino measures as being protective and destigmatizing. and Hazen, 2013). For instance, caregivers of SOT recipients show stress The first aim of this study is to evaluate and compare the levels of related to communicating, decision-making, balancing the demands of parenting stress, anxiety, and depression and coping strategies in multiple roles, and facing the emotional consequences of parenting a families of SOT recipients and in healthy controls. The second aim is to child with an illness. Moreover, after transplantation, children can have analyze if the pandemic has had an additional impact on families. complex emotional and physical needs, which can result in greater strain We hypothesize that SOT families will show higher levels of stress, on the family system (Farley et al., 2007). depression, and anxiety. Moreover, we hypothesize that the coping Greater parenting stress is associated with psychological distress, strategies used to face uncertainty will be different in families of SOT e.g., depressive and anxious symptomatology in the case of caregivers of pediatric recipients in comparison with the controls. Concerning the children with chronic illness (Cousino and Hazen, 2013), with anxiety effects of COVID-19, we believe that the impact of the pandemic on being the most frequent psychological disorder (Toledano-Toledano and these families more than 1 year after its beginning will be similar to the Moral de la Rubia, 2018). In a recent study, Cushman et al. (2021) found impact on the controls. an improvement in children’s health-related quality of life from pre-transplantation to 6 months post-transplantation, but caregivers’ psychological depression, anxiety, and global stress symptoms did not Materials and methods similarly improve. Caregivers’ adaptive coping can be a protective factor in the process Participants of children adjustment to a chronic illness (Toledano-Toledano and Moral de la Rubia, 2018). Caregivers’ optimistic and self-confident The total study sample consisted of 102 caregivers, 51 of whom coping strategies have been associated with fewer internalizing represented families where one member had undergone a pediatric symptoms and a better quality of life in adolescents during the process transplant process (SOT group) and 51 families of healthy children and of transplantation (Yilmaz Kafali et al., 2021). However, the use of more adolescents (control group). The inclusion criteria were: (1) for the SOT emotion-focused coping behaviors (e.g., avoidance) in caregivers of group, being an adult primary caregiver in a family of a pediatric patient, children with chronic illness was associated with greater parenting stress with clinical stability, who was 18 years of age or younger and had gone (Rodenburg et al., 2007) and poorer psychosocial adaptation through a SOT (liver, kidney, heart, or lung) (2) for the control group, (Livneh, 2019). being an adult primary caregiver in a family with a child or adolescent Frontiers in Psychology 02 frontiersin.org Forner-Puntonet et al. 10.3389/fpsyg.2023.1067477 18 years or younger without chronic illness, (3) having user-level The Hospital Anxiety and Depression Scale (HADS; Zigmond and computer skills, and (4) agreeing to take part in the study. Language Snaith, 1983) is a widely used self-administered questionnaire to barriers in respondents were set as exclusion criteria, since all the evaluate anxiety and depression. It has been validated in Spanish by questionnaires were in Spanish. The approval of the Ethics Committee Herrero et al. (2003). It is comprised of seven items on anxiety and seven (PR(AG)195/2021) of the Hospital Universitari Vall d’Hebron was items on depression; each item is rated on a Likert scale from 0 to 3. obtained for the research. They are scored as being without anxiety or depression to having mild, moderate, or severe anxiety or depression. The COPE Inventory (Carver et al., 1989) is a multidimensional Procedure coping inventory to assess the different ways in which people respond to stress. The inventory consists of 60 items to which participants The sample was recruited between May and July 2021, during the respond how frequently they used each coping strategy, rated on a fourth and fifth wave of the COVID-19 pandemic in Spain. We used four-point scale (between “usually do not do this at all” to “usually convenience sampling; the sample of the SOT group was obtained do this a lot”). Crespo and Cruzado (1997) have adapted, through families of consecutive patients who consulted the different standardized, and validated the instrument for Spanish samples. The pediatric transplant teams (liver, kidney, heart, or lung) at the Hospital COPE Inventory is formed by 15 subscales: Social Support, Religion, Universitari Vall d’Hebron in person or on-line. Pediatric teams Humor, Substance use, Planification and Active Coping, explained the study goals, participation rights, and data treatment Abandonment of Coping Efforts, Focus on and venting of emotions, procedure, and asked primary self-perceived caregivers, who could only Acceptance, Denial, Restraint, Concentrate efforts on solving the complete the survey after giving their consent to participate. They were situation, Personal Growth, Positive Reinterpretation, Distraction, contacted twice by emails that included access to a web survey and Evasion. application, which provided the sociodemographic questionnaire and The COVID-19 Exposure and Family Impact Survey (CEFIS) was the assessment instruments. In total, 59 caregivers belonging to a family developed by the Center for Pediatric Traumatic Stress (2020), using a with a SOT recipient were contacted, and 51 of them responded to the rapid iterative process, in late March/early April 2020, and it has been full survey (86% answer rate). validated by Enlow et al. (2022). The CEFIS is available in English and To recruit the control group participants, all the SOT group families Spanish and should be completed by a caregiver. The CEFIS assesses agreed to forward the received email to one or two families with a child exposure, impact, and distress of COVID-19 in the family. Exposure of the same age and gender as their child. They sent it to a total of 78 consists of 25 items with dichotomous responses (yes/no) that measures caregivers of healthy children of whom 57 answered the full survey (73% the participants’ degree of exposure to COVID-19 and related events. answer rate). Control group participants were matched with SOT group The Total Exposure score is the sum of all the items. Impact consists of participants by their children’s age and gender and were selected in order 10 items using a four-point Likert scale (also offering a “does not apply” of response. choice) to rate the impact on the participant’s and family’s life. Distress scale consists of two 10-point distress scales to assess how much distress caregivers and their children have experienced due to the pandemic. Instruments Item responses are averaged within each scale to yield the Impact and Distress scale scores. Higher scores indicate mean greater levels of The following data were collected regarding the sociodemographic exposure, impact, and distress. The CEFIS asks the respondents to and clinical characteristics of the primary caregiver: age, gender, race/ answer by thinking about the period from March 2020 to the present, ethnicity, education level, marital status, number of children, and therefore addressing the full time period since the pandemic has had relationship with the child or adolescent. Regarding child or adolescent consequences in western countries. information, the following information was requested: age, gender, basic disease for which the child or adolescent had required a transplant, type of pediatric SOT, and age at transplantation, if applicable. Data analysis The Parenting Stress Index-Short Form (PSI-SF; Abidin, 1995) is a self-report tool for parents of children until 12 years old that identifies All data collected were analyzed using SPSS version 28.0. First, a the sources and types of stress that come with parenting. It has been descriptive synthesis of the main variables was performed. The analysis validated in Spanish by Díaz-Herrero et al. (2010). The PSI-SF has 36 of the normality condition was carried out using Shapiro–Wilk statistics, items that use a five-point Likert-scale; it is divided into three subscales the result of which guided subsequent calculations by parametric and yields a Total Stress score. The subscales are: (1) Parental Distress— (PSI-SF: Parental Distress, Difficult Child, Total Stress; COPE: Social the extent to which parents feel competent, restricted, conflicted, Support, Planification and Active Coping, Restraint, Concentrate Efforts supported, and/or depressed in their roles as a parent; (2) Parent–Child on Solving the Situation; CEFIS: Exposure total score, Distress in Dysfunctional Interaction—the extent to which parents feel satisfied Parents, and Distress scale) or non-parametric route. In the first, the with their child and their interactions with them; and (3) Difficult Child comparison of two means was determined with Student’s t-tests and the – how parents perceive their child in terms of whether the child is easy correlational study was developed with Pearson’s test. In the or difficult to take care of. The Total Stress score indicates the overall non-parametric way, the comparison of two means was analyzed with level of stress a person is feeling in their role as a parent. When analyzing Mann–Whitney U tests, and the correlations with Spearman’s test. parental stress scores, it is important to keep in mind that some degree Chi-squared tests were run in order to compare outcomes between of parenting stress is normal. Percentiles between 15 and 80 are groups in qualitative variables and evaluate the possibility of interaction considered typical, high stress scores range from 81 to 84, and clinically between factors. The level of significance was set at 0.05 in all analyses. significant levels of stress are above 85 or 90, depending on the subscale. Cohen’s d was used to determine effect sizes. Frontiers in Psychology 03 frontiersin.org Forner-Puntonet et al. 10.3389/fpsyg.2023.1067477 TABLE 1 Sociodemographic characteristics of the sample. Variables Total sample SOT group Control group χ2 or t Value of p n=102 n=51 n=51 N (%) or M±SD N (%) or M±SD N (%) or M±SD Caregiver gender (relationship with the child) 0.10 0.75  Male (father) 11 (10.8) 5 (45.5) 6 (54.5)  Female (mother) 91 (89.2) 46 (50.5) 45 (49.5) Caregiver age 43.44 ± 15.97 43 ± 6.12 44 ± 5.84 0.64 0.523 Caregiver race 0.061  Caucasian 92 (90.2%) 43 (84.3%) 49 (96.1%)  African American 5 (4.9%) 5 (9.8%) 0  Hispanic 5 (4.9%) 3 (5.9%) 2 (3.9%) Caregiver education 8.14 0.04  Primary to High School 29 (28.4) 21 (72.4) 8 (27.6)  University and Postgraduate 73 (71.6) 30 (41.1) 43 (58.9) Marital status 0.10 0.95  Single 10 (9.8) 5 (50) 5 (50)  Married/Cohabiting 81 (79.4) 40 (49.4) 41 (50.6)  Separated/Divorced 11 (10.8) 6 (54.5) 5 (45.5) Number of children 1.8 ± 0.7 1.7 ± 0.8 1.8 ± 0.6 0.70 0.484 Age of pairing children 9.5 ± 5.3 9.5 ± 5.3 9.5 ± 5.4 −0.07 0.945 Gender of pairing children 0 1  Male 44 (43.1) 22 (50) 22 (50)  Female 58 (56.9) 29 (50) 29 (50) Transplant type – –  Liver 22 (43.1) 22 (43.1) 0  Kidney 14 (27.5) 14 (27.5) 0  Heart 9 (17.6) 9 (17.6) 0  Lung 6 (11.8) 6 (11.8) 0 Age at the time of transplantation 5.2 ± 4.9 5.2 ± 4.9 – – M, Mean; SD, Standard Deviation; SOT group, Solid Organ Transplant group; χ , Chi-squared test; t, Student’s t-test. 2 Results than the control group (t = −2.083; p = 0.041) and significantly higher scores on the Parent–Child Dysfunctional Interaction (U = 355.5; Sociodemographic characteristics from caregivers and children p = 0.015) and Difficult Child scales (t = −2.043; p = 0.045), with in each group are presented in Table 1. All caregivers who responded moderate effect sizes (see Table 2). These results were maintained after were the children’s parents, mostly mothers (89.2%). No differences controlling for the level of education. However, there were no significant were found between groups in terms of the caregivers’ gender, age, differences on Parental Distress between the groups. race/ethnicity, marital status, number of children, or relationship with the child. Significant differences in the level of education (χ2 = 8.14; p = 0.04) were found between caregivers of both groups. Of Anxiety and depression of caregivers the children, 56.9% of the children were girls and the average age of the children sample was 9.5 ± 5.3 years. The SOT group included the Table 3 summarizes the quantitative data extracted from the HADS pediatric recipients of 22 livers, 14 kidneys, 9 hearts, and 6 lungs, related to the anxiety and depression of caregivers. Regarding anxiety, with an average age at transplantation of 5.2 ± 4.9. On average, the the SOT group reported significantly higher levels than the control children in the sample went through transplantation more than group (U = 863.5; p = 0.003), with moderate effect sizes, showing anxious 4 years ago. symptomatology on probable case levels. Families in the SOT group reported themselves to be more tense; feeling sort of frightened, as if something awful was about to happen; feeling more worried, finding it Parenting stress difficult to relax; and experiencing sudden feelings of panic. These results were maintained after controlling for the level of education. No Although all scores were in a non-clinical range, between percentiles significant differences were found between the groups on the 15 and 80, the families in the SOT group showed greater Total Stress Depression Scale. Frontiers in Psychology 04 frontiersin.org Forner-Puntonet et al. 10.3389/fpsyg.2023.1067477 TABLE 2 Parenting Stress Index-Short Form (PSI-SF). Variables Total sample SOT group Control group t or U Value of p Cohen’s d n=66 n=33 n=33 M±SD M±SD M±SD Parental Distress (PD) 29.9 ± 9.7 29.2 ± 9.9 30.6 ± 9.6 0.56 0.578 0.144 Parent–Child Dysfunctional 21.4 ± 6.6 23.4 ± 6.7 19.4 ± 5.8 355.50 0.015 −0.638 Interaction (P-CDI) Difficult Child (DC) 27.3 ± 8.5 29.4 ± 8.8 25.2 ± 7.8 −2.04 0.045 −0.505 Total stress 78.1 ± 15.5 82 ± 16.5 74.2 ± 13.7 −2.08 0.041 −0.514 Included families of children until 12 years old. M, Mean; SD, Standard Deviation; SOT group, Solid Organ Transplant group; t = Student’s t-test; U = Mann–Whitney U-test. TABLE 3 Hospital Anxiety and Depression Scale (HADS). Variables Total sample SOT group Control group U Value of p Cohen’s d n=102 n=51 n=51 M±SD M±SD M±SD Anxiety scale 6.6 ± 4.2 7.9 ± 4.3 5.4 ± 3.8 863.50 0.003 −0.616 Depression scale 4.2 ± 3.7 4.9 ± 4 3.5 ± 3.3 1032.50 0.071 −0.382 M, Mean; SD, Standard Deviation; SOT group, Solid Organ Transplant group; U = Mann–Whitney U-test. Coping strategies a better balance in caregiving (De Piccoli et al., 2016). Therefore, a collaborative relationship between all the main caregivers and SOT Table 4 summarizes the results of the COPE Inventory. SOT families pediatric recipients is essential, as it is a space to share information and used significantly more denial strategies (U = 889.5; p = 0.010), used knowledge about procedures and illness, offer support on emotional religion as a coping strategy more (U = 792.5; p = 0.031), and tended to regulation, or develop skills to help the child and the whole family meet abandon coping efforts (U = 1,013; p = 0.047), with small effect sizes. existing challenges. Families in the control group used more social support as a coping In relation to the first aim of the study, families of pediatric strategy (t = 2.098; p = 0.038) with small effect sizes. Nevertheless, all transplantation recipients reported normal levels of parenting stress, responses were in a normative clinical range. These results were although they showed higher scores on the Difficult Child scale, the maintained after controlling for the level of education. Parent–Child Dysfunctional Interaction Stress scale, and the Total Stress score than the controls did. Higher scores on the Difficult Child scale are related to more stress in taking care of their child and Exposure, impact, and distress of COVID-19 to possible difficulties in managing their child’s behavior. Higher scores on the Parent–Child Dysfunctional Interaction scale indicate More than 1 year after the beginning of the pandemic, no significant that it is more difficult for those parents to create a proper bond with differences were found between both groups in terms of exposure, their child. These difficulties are probably related to child and parent impact, or distress related to the pandemic (see Table 5). anxiety, the physical effects of the illness, and the treatment conditions for chronic illness (Ødegård, 2005). According to Golfenshtein et al. (2016), interventions that focus on the Discussion improvement of the parent–child relationship to enhance connectedness and skill-building interventions (education, problem To our knowledge, this is the first study to analyze family stress and solving, and parental techniques) had a positive impact on parenting coping strategies of SOT families in times of pandemic. In addition, stress, although they have failed until now to demonstrate long-term although SOT is a life-threatening event that not only impacts the effects thus far. patients themselves but their entire family systems, there are very few In our study, caregivers of SOT recipients showed greater levels of studies that delve into family stress, and we did not identify any study anxiety; these results are on a clinical borderline level, reinforcing the that focuses on the coping strategies of caregivers of children and importance of treating these symptoms in parents in order to reduce the adolescents who have undergone transplantation. risk of greater impairment. Interventions for parents of children with First of all, regarding the sociodemographic variables, it is important chronic illness with a focus on the parents’ mental health have been to remark that the majority of respondents and primary caregivers in lacking (Eccleston et al., 2015), although recent studies based on our study were mothers. These results are in line with those of Cardinali cognitive behavioral therapy and acceptance and commitment therapy et al. (2019), which pointed out that mothers usually assume the role of showed promising results (Douma et al., 2021). primary caregivers, implying a greater interference with and more Caregivers of children and adolescents who have undergone limitations in their work and social life, as well as in other life domains. transplantation tend to significantly drop coping efforts and use more It is important to explore specific gender differences regarding caregiving denial strategies than the controls did, although the strategies used by for a child who has undergone SOT in order to reduce gender the families of SOT recipients do not reach clinical levels of significance. stereotypes that are still present in parents’ perceptions and to promote These avoidance strategies have been described as maladaptive; they are Frontiers in Psychology 05 frontiersin.org Forner-Puntonet et al. 10.3389/fpsyg.2023.1067477 TABLE 4 COPE inventory. Variables Total sample SOT group Control group t or U Value of p Cohen’s d n=102 n=51 n=51 M±SD M±SD M±SD Social support 21.9 ± 5.8 20.8 ± 5.3 23.1 ± 6.0 2.10 0.038 0.406 Religion 5.6 ± 2.0 5.9 ± 1.9 5.2 ± 2.1 792.50 0.031 −0.35 Humor 7.4 ± 2.4 7.0 ± 2.3 7.8 ± 2.3 1061.50 0.107 0.348 Substance use 4.2 ± 0.6 4±0 4±1 1285.50 0.867 0 Planification and active coping 16.4 ± 2.8 16.0 ± 2.4 16.7 ± 3.1 1.22 0.226 0.253 Abandonment of coping efforts 4.7 ± 1.2 4.9 ± 1.3 4.4 ± 1.1 1013.00 0.047 −0.415 Focus on and venting of emotions 8.4 ± 2.3 8.2 ± 2.1 8.7 ± 2.4 1125.00 0.386 0.222 Acceptance 11.8 ± 2.2 11.7 ± 2.4 11.9 ± 2.1 1248.50 0.724 0.089 Denial 5.6 ± 1.8 6.1 ± 2.0 5.2 ± 1.6 889.50 0.010 −0.497 Restraint 9.7 ± 2.1 9.5 ± 1.9 10.0.0 ± 2.3 1.26 0.209 0.237 Concentrate efforts on solving the situation 10 ± 2.4 9.8 ± 2.3 10.2 ± 2.4 0.67 0.504 0.17 Personal growth 6.5 ± 1.1 6.6 ± 1.0 6.5 ± 1.1 1121.00 0.564 −0.095 Positive reinterpretation 8.9 ± 1.6 8.8 ± 1.6 9.1 ± 1.6 1105.00 0.232 0.187 Distraction 6.6 ± 1.0 6.4 ± 0.9 6.7 ± 1.0 697.50 0.125 0.21 Evasion 5.3 ± 1.4 5.4 ± 1.5 5.2 ± 1.3 1195.00 0.47 −0.142 M, Mean, SD, Standard Deviation; SOT group, Solid Organ Transplant group; t, Student’s t-test; U = Mann–Whitney U-test. TABLE 5 COVID-19 exposure and family impact survey (CEFIS). Variables Total sample SOT group Control group t or U Value of p Cohen’s d n=102 n=51 n=51 M±SD M±SD M±SD Exposure total score 8.8 ± 2.7 8.7 ± 2.9 9.0 ± 2.5 0.660 0.511 0.111 Impact total score 1.9 ± 1.3 1.9 ± 1.3 1.8 ± 1.3 1250.50 0.735 −0.077  Distress in parents 5.6 ± 2.3 5.9 ± 2.4 5.4 ± 2.2 −1.038 0.302 −0.217  Distress in children 4.8 ± 2.6 4.7 ± 2.6 5.0 ± 2.5 1207.00 0.528 0.118 Distress scale 5.2 ± 2.1 5.0 ± 2 5.3 ± 2.2 −0.235 0.815 0.143 M, Mean; SD, Standard Deviation; SOT group, Solid Organ Transplant group; t, Student’s t-test; U = Mann–Whitney U-test. able to promote some relief in the short term, but induce lower well- religion or spirituality can contribute to the adaptation to chronic being (Waugh et al., 2021) and greater distress in the medium to long illness (Pargament, 2001). term (Cousino and Hazen, 2013). Nap-van der Vlist et al. (2021) In the case of coping strategies, it is additionally important to reinforced the importance of open communication about stress as a first underline that SOT families use less social support coping strategies, step to cope with these ineffective strategies and to provide parent–child although social support represents a key variable associated with positive dyadic coping (Nap-van der Vlist et al., 2021). We hypothesize optimal adjustment to chronic illness (Helgeson and Zajdel, 2017) and that families of SOT recipients’ have learned other strategies to cope can be a buffer to parental stress (Pinquart, 2018). We believe that the with the uncertainty and stress related to transplantation, and that some lower use of social support as a strategy by the caregivers of SOT kind of avoidance behavior, in a non-clinical way, allows them to cope recipients might be due to feelings or perceptions of not being with some difficulties of the transplantation process, permitting them completely understood or emotionally supported by people who are not at the same time to escape a little bit from certain worries in their going through the same process. Promoting support and accompaniment daily life. by a close family member or by social networks could be a positive However, SOT caregivers also used more religious coping factor, but health institutions in particular can mobilize additional social strategies, which probably brought them hope and courage to cope support – for instance, promoting mutual aid groups for SOT families with the process of transplantation. This kind of coping can to come together. Likewise, strategies to educate, inform, and offer these be active (e.g., benevolent religious reappraisals) or passive (e.g., supports among SOT families through digital resources can facilitate waiting for something to change or a miracle), showing that adjustment to chronic illness (DeHoff et al., 2016), especially in religious coping can be adaptive or maladaptive depending on its pandemic times. positive or negative consequences (Peres and Lucchetti, 2010). In line with our results, the Committee on Hospital Care and Attention to multicultural issues is an important element for Institute for Patient- and Family-Centered Care (2012) from the families, especially bearing in mind that active behaviors linked to American Academy of Pediatrics has repeatedly emphasized the need to Frontiers in Psychology 06 frontiersin.org Forner-Puntonet et al. 10.3389/fpsyg.2023.1067477 adopt a patient- and a family-centered approach to children’s chronic In conclusion, families of SOT patients showed more difficulties conditions. In the field of pediatric transplantation, there is a lack of regarding parent–child interaction, more stress in taking care of their studies that explore the supportive needs of SOT recipients’ families; this child, more avoidance coping strategies, less use of social support is crucial for effective child and adolescent coping and adaptation to strategies, and clinically significant levels of anxiety, even 4 years after illness. Caregivers’ levels of anxiety, stress, and coping strategies can transplantation. However, although they initially had a different way of be screened routinely in the transplantation process. These aspects are adapting to the pandemic (Forner-Puntonet et al., 2021), COVID-19 modifiable intervention targets and can facilitate parents and children’s does not seem to add additional stress to families of SOT recipients at adjustment to illness. For instance, cognitive behavioral therapy and the current point. Caregivers of SOT patients can benefit from acceptance commitment therapy could be implemented with the psychological interventions that focus mainly on parents’ mental caregivers of SOT recipients. Intervention programs directed to reduce health, parent–child connectedness, skill building, and social support anxiety to non-clinical levels, help caregivers manage the stress related aid groups, with attention to multiculturalism and promoting a better to the difficulty of adjusting parent–child interaction, and promote balance between caregivers, reflecting the need for family interventions effective, optimistic, and self-confident coping strategies could that are maintained over time. Moreover, there is a critical need to be enhanced. evaluate the efficacy of this interventions to support the health and Regarding the second aim of the study, more than 1 year after the well-being of parents and families (Law et al., 2019) during the whole beginning of the pandemic, there were no differences between the SOT process. Additionally, strategies that offer this support to families exposure, impact, and distress from the pandemic on families of through digital resources can facilitate adjustment to chronic illness, pediatric SOT and controls. Therefore, the pandemic did not have an especially in pandemic times. additional differential effect on SOT families after more than 1 year; the differences found in stress, anxiety, or coping strategies were probably more related to the process of transplantation. However, we cannot Data availability statement forget that the pandemic has had an economic impact on families and that subsidies from the government and other institutions can help to The raw data supporting the conclusions of this article will be made provide economic stability and security to caregivers, thus reducing available by the authors, without undue reservation. anxiety and improving adjustment in the uncertain situation of transplant processes. While the current study is an important first step in understanding Ethics statement caregivers’ psychopathology, family stress, and coping strategies for pediatric SOT in times of pandemic, there were some limitations. The The studies involving human participants were reviewed and sample size was limited, although studies with SOT recipients tend to approved by the Ethics Committee (PR(AG)195/2021) of the Hospital have similar samples due to the specificity of the studied population Universitari Vall d’Hebron was obtained for the research. Written (Cousino et al., 2017); nevertheless, the response rate was good, informed consent to participate in this study was provided by the probably due to the close relationship between families and the medical participants’ legal guardian/next of kin. teams and the proximity of the control families to SOT recipients. Regarding recruitment, although we believe that the acquaintance control method was useful in the pandemic situation, this method of Author contributions recruitment could have influenced the homogeneity of some variables in the sample (e.g., gender). On the other hand, the control group had All the authors have contributed to the intervention, design, higher levels of education, which were controlled for statistical analysis. acquisition, analysis, interpretation, and/or review of the work and These differences could be due to the fact that our center is a reference agree to be accountable for all aspects of the work, ensuring that in transplantation, attending to families with different levels of questions related to the accuracy or integrity of any part of the education from different countries, where such procedures are not work are appropriately investigated and resolved. All authors carried out. Additionally, it is important to include families with diverse contributed to the article and approved the submitted cultural backgrounds in future research in order to study differences in version. stress and coping strategies across cultures. Other family characteristics, such as whether they are single-parent families or how the burden of the childcare is distributed among primary caregivers, should also Acknowledgments be included in future studies. Moreover, the study did not include additional validated measures to evaluate posttraumatic stress disorder The authors would like to thank the patient and family associations on caregivers, quality of life, or resilience, which could provide a ANiNATH, En tus Zapatos, and Hipofam, whose support and broader and more constructive picture of the topic. In terms of future collaboration made this study possible. lines of research, it is important to conduct follow-up studies to evaluate the levels of anxiety, stress, and coping styles of families during the entirety of the transplantation process, as well as to compare them to Conflict of interest other chronic medical conditions, and to identify specific risk times where major stress, anxiety, and coping should be addressed. GA reported lectures and advisory honoraria from Chiesi, Recordati Additionally, psychological intervention studies to improve the stress Rare Diseases, Alexion (Astra Zeneca Rare Diseases), Advicenne, level of SOT families in the follow-up are needed. Dicerna, Alnylam, and Kyowa Kirin. Frontiers in Psychology 07 frontiersin.org Forner-Puntonet et al. 10.3389/fpsyg.2023.1067477 GE-M has received travel grants from Takeda, Laboratorios Rubió, The remaining authors declare that the research was conducted in Lundbeck, and Angelini Pharma España for participating in the absence of any commercial or financial relationships that could psychiatric meetings. be construed as a potential conflict of interest. JAR-Q was on the speakers’ bureau and/or acted as consultant for Eli-Lilly, Janssen-Cilag, Novartis, Shire, Takeda, Bial, Shionogui, Lundbeck, Almirall, Braingaze, Sincrolab, Medice, and Rubió, Raffo in the Publisher’s note last 5 years. He also received travel awards (air tickets + hotel) for taking part in psychiatric meetings from Janssen-Cilag, Rubió, Shire, Takeda, All claims expressed in this article are solely those of the authors and Shionogui, Bial, Medice, and Eli-Lilly. The Department of Psychiatry do not necessarily represent those of their affiliated organizations, or chaired by him received unrestricted educational and research support those of the publisher, the editors and the reviewers. Any product that from the following companies in the last 5 years: Eli-Lilly, Lundbeck, may be evaluated in this article, or claim that may be made by its Janssen-Cilag, Actelion, Shire, Ferrer, Oryzon, Roche, Psious, and Rubió. manufacturer, is not guaranteed or endorsed by the publisher. References Abidin, R. R. (1995). Parenting Stress Index (PSI) Manual, 3rd Edn., Charlottesville, VA, Fontanesi, L., Marchetti, D., Mazza, C., Di Giandomenico, S. D., Roma, P., and Pediatric Psychology Press. Verrocchio, M. C. (2020). The effect of the COVID-19 lockdown on parents: a call to adopt urgent measures. Psychol. Trauma. 12, S79–S81. doi: 10.1037/tra0000672 Annunziato, R. A., Jerson, B., Seidel, J., and Glenwick, D. S. (2012). The psychosocial challenges of solid organ transplant recipients during childhood. Pediatr. Transplant. 16, Forner-Puntonet, M., Castell-Panisello, E., Quintero, J., Ariceta, G., Gran, F., 803–811. doi: 10.1111/j.1399-3046.2012.01749.x Iglesias-Serrano, I., et al. (2021). Impact of COVID-19 on families of pediatric solid organ transplant recipients. J. Pediatr. Psychol. 46, 927–938. doi: 10.1093/jpepsy/jsab058 Cardinali, P., Migliorini, L., and Rania, N. (2019). The caregiving experiences of fathers and mothers of children with rare diseases in Italy: challenges and social support Golfenshtein, N., Srulovici, E., and Deatrick, J. A. (2016). Interventions for reducing perceptions. Front. Psychol. 10:1780. doi: 10.3389/fpsyg.2019.01780 parenting stress in families with pediatric conditions: an integrative review. J. Fam. Nurs. 22, 460–492. doi: 10.1177/1074840716676083 Carver, C. S., Scheier, M. F., and Weintraub, J. K. (1989). Assessing coping strategies: a theoretically based approach. J. Pers. Soc. Psychol. 56, 267–283. doi: Helgeson, V. S., and Zajdel, M. (2017). Adjusting to chronic health conditions. Annu. 10.1037/0022-3514.56.2.267 Rev. Psychol. 68, 545–571. doi: 10.1146/annurev-psych-010416-044014 Center for Pediatric Traumatic Stress (2020). The COVID-19 Exposure and Family Impact Herrero, M. J., Blanch, J., Peri, J. M., De Pablo, J., Pintor, L., and Bulbena, A. (2003). A Survey (CEFIS), Center for Pediatric Traumatic Stress, Nemours Children’s health system: validation study of the hospital anxiety and depression scale (HADS) in a Spanish Wilmington, DE. population. Gen. Hosp. Psych. 25, 277–283. doi: 10.1016/s0163-8343(03)00043-4 Committee on Hospital Care and Institute for Patient- and Family-Centered Care (2012). Imam, A., Karatas, C., Imam, R., Armutlu, A., Mecit, N., Karakaya, A., et al. (2020). Patient- and family-centered care and the pediatrician's role. Pediatrics 129, 394–404. doi: Three consequent pediatric liver transplant deaths in the COVID-19 era. Int. J. Organ 10.1542/peds.2011-3084 Transplant. Med. 11, 202–206. PMID: 33335701 Cousino, M. K., and Hazen, R. A. (2013). Parenting stress among caregivers of children Jesse, M. T., Hansen, B., Bruschwein, H., Chen, G., Nonterah, C., Peipert, J. D., et al. with chronic illness: a systematic review. J. Pediatr. Psychol. 38, 809–828. doi: 10.1093/ (2021). Findings and recommendations from the organ transplant caregiver initiative: jpepsy/jst049 moving clinical care and research forward. Am. J. Transplant. 21, 950–957. doi: 10.1111/ ajt.16315 Cousino, M. K., Rea, K. E., Schumacher, K. R., Magee, J. C., and Fredericks, E. M. (2017). A systematic review of parent and family functioning in pediatric solid organ transplant Law, E., Fisher, E., Eccleston, C., and Palermo, T. M. (2019). Psychological interventions populations. Pediatr. Transplant. 21:e12900. doi: 10.1111/petr.12900 for parents of children and adolescents with chronic illness. Cochrane Database Syst. Rev. 2021:CD009660. doi: 10.1002/14651858.CD009660.pub4 Crespo, M., and Cruzado, J. (1997). La evaluación del afrontamiento: adaptación española del cuestionario COPE con una muestra de estudiantes universitarios. Análisis y Livneh, H. (2019). The use of generic avoidant coping scales for psychosocial adaptation Modificación de conducta 23, 797–830. to chronic illness and disability: a systematic review. Health Psychol. Open. 6:2055102919891396. doi: 10.1177/2055102919891396 Cushman, G., Gutierrez-Colina, A. M., Lee, J. L., Rich, K. L., Mee, L. L., Rea, K., et al. (2021). Caregiver-reported outcomes of pediatric transplantation: changes and predictors Nap-van der Vlist, M. M., van der Wal, R. C., Grosfeld, E., van de Putte, E. M., at 6 months post-transplant. Pediatr. Transplant. 25:e14067. doi: 10.1111/petr.14067 Dalmeijer, G. W., Grootenhuis, M. A., et al. (2021). Parent-child dyadic coping and quality of life in chronically diseased children. Front. Psychol. 12:701540. doi: 10.3389/fpsyg.2021.701540 De Piccoli, N., Ceccarini, L., Gattino, S., and Rollero, C. (2016). “Health and social support from a gender perspective” in Social Support: Gender Differences, Psychological Importance and Ødegård, W. (2005). Chronic illness as a challenge to the attachment process. Clin. Child Impacts on Well-being. ed. C. Castillo (New York, NY: Nova Science Publishers), 1–15. Psychol. Psych. 10, 13–22. doi: 10.1177/1359104505048787 DeHoff, B. A., Staten, L. K., Rodgers, R. C., and Denne, S. C. (2016). The role of online Pargament, K. I. (2001). The Psychology of Religion and Coping: Theory, Research, Practice. social support in supporting and educating parents of young children with special health New York: Guilford Press. care needs in the United States: a scoping review. J. Med. Internet Res. 18:e333. doi: 10.2196/ Peres, M. F., and Lucchetti, G. (2010). Coping strategies in chronic pain. Curr. Pain jmir.6722 Headache Rep. 14, 331–338. doi: 10.1007/s11916-010-0137-3 Díaz-Herrero, Á., de la Nuez, A. G. B., Pina, J. A. L., Pérez-López, J., and Pinquart, M. (2018). Parenting stress in caregivers of children with chronic physical Martínez-Fuentes, M. T. (2010). Estructura factorial y consistencia interna de la versión condition-a meta-analysis. Stress Health. 34, 197–207. doi: 10.1002/smi.2780 española del Parenting Stress Index-Short Form. Psicothema 22, 1033–1038. PMID: 21044549 Rodenburg, R., Meijer, A. M., Deković, M., and Aldenkamp, A. P. (2007). Parents of children with enduring epilepsy: predictors of parenting stress and parenting. Epilepsy Douma, M., Maurice-Stam, H., Gorter, B., Krol, Y., Verkleij, M., Wiltink, L., et al. (2021). Behav. 11, 197–207. doi: 10.1016/j.yebeh.2007.05.001 Online psychosocial group intervention for parents: positive effects on anxiety and depression. J. Pediatr. Psychol. 46, 123–134. doi: 10.1093/jpepsy/jsaa102 Toledano-Toledano, F., and Moral de la Rubia, J. (2018). Factors associated with anxiety in family caregivers of children with chronic diseases. Biopsychosoc. Med. 12:20. doi: Eccleston, C., Fisher, E., Law, E., Bartlett, J., and Palermo, T. M. (2015). Psychological 10.1186/s13030-018-0139-7 interventions for parents of children and adolescents with chronic illness. Cochrane Database Syst. Rev. 4:CD009660. doi: 10.1002/14651858.CD009660.pub3 Waugh, C. E., Leslie-Miller, C. J., Shing, E. Z., Furr, R. M., Nightingale, C. L., and McLean, T. W. (2021). Adaptive and maladaptive forms of disengagement coping in caregivers Enlow, P. T., Phan, T. T., Lewis, A. M., Hildenbrand, A. K., Sood, E., Canter, K. S., et al. of children with chronic illnesses. Stress Health. 37, 213–222. doi: 10.1002/smi.2985 (2022). Validation of the COVID-19 exposure and family impact scales. J. Pediatr. Psychol. 47, 259–269. doi: 10.1093/jpepsy/jsab136 Yilmaz Kafali, H., Kalyoncu, T., Ozbaran, B., Kalyoncu, E., Tuncer, O. N., Ozturk, P., et al. (2021). Association between caregivers' coping and children's psychiatric symptoms in the Farley, L. M., DeMaso, D. R., D'Angelo, E., Kinnamon, C., Bastardi, H., Hill, C. E., et al. heart transplantation process: a pilot study. Artif. Organs. 45, 354–363. doi: 10.1111/ (2007). Parenting stress and parental post-traumatic stress disorder in families after aor.13839 pediatric heart transplantation. J. Heart Lung Transplant 26, 120–126. doi: 10.1016/j. healun.2006.11.013 Zhao, R., Zhou, Q., Wang, X.-W., Liu, C.-H., Wang, M., Yang, Q., et al. (2020). COVID-19 outbreak and management approach for families with children on long-term kidney Fegert, J. M., Vitiello, B., Plener, P. L., and Clemens, V. (2020). Challenges and burden of the replacement therapy. Clin. J. Am. Soc. Nephrol. 15, 1259–1266. doi: 10.2215/CJN.03630320 coronavirus 2019 (COVID-19) pandemic for child and adolescent mental health: a narrative review to highlight clinical and research needs in the acute phase and the long return to Zigmond, A. S., and Snaith, R. P. (1983). The hospital anxiety and depression scale. Acta normality. Child Adolesc. Psychiatry Ment. Health 14:20. doi: 10.1186/s13034-020-00329-3 Psychiatr. Scand. 67, 361–370. doi: 10.1111/j.1600-0447.1983.tb09716.x Frontiers in Psychology 08 frontiersin.org