Abstract
This study aimed to evaluate the psychological symptoms of children and adolescents with rheumatological diseases (RD) and their parents during the outbreak. A web-based questionnaire survey was conducted in a cross-sectional design in RD patients and healthy controls. The Hospital Anxiety and Depression Scale was used to evaluate parental psychiatric status; while the State-Trait Anxiety Inventory for Child was used for children. Four hundred and fifty-nine patients with RD and their parents completed the present study, as well as 336 healthy peers. The age and gender of the children were similar across groups. Under 12 years of age, the trait anxiety of the children and the psychological symptoms of parents were similar across groups; while over 13 years of age, anxiety and depression scores of the parents, as well as trait anxiety of the children were higher than the control groups’ (7.3 ± 3.4 vs 6.3 ± 3.8, p = 0.006 for parental anxiety; 6.6 ± 3.8 vs. 5.3 ± 3.9, p < 0.001 for parental depression; 36.1 ± 8.7 vs. 33.3 ± 7.9, p = 0.002 for child trait anxiety). In patient group, there were no differences in scale scores according to variables such as rheumatological disease diagnosis, the consulting of doctor for treatment, thinking that RD increases the risk of COVID-19, the history of rheumatic disease attack during the pandemic process, and the use of biological agents. The children’s trait anxiety was positively correlated with their parents’ anxiety (r = 0.414, p < 0.001) and depression (r = 0.300, p < 0.001) scores. These findings suggest that clinicians should pay attention to the psychiatric symptoms of both children with RD and their parents during the pandemic.
Keywords: Adolescents, Anxiety, Children, COVID-19, Depression, Rheumatic diseases, Outbreak
Introduction
Coronavirus Disease (COVID-19) was first identified in Wuhan, China, in late 2019, as a variant of severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) [1, 2]. COVID-19 usually presents with symptoms of fever, dry cough and fatigue; its symptoms ranging from mild to severe, and in some cases becoming fatal [3]. Additionally, symptoms that mimic rheumatological diseases such as myalgia, arthralgia, cytopenia, myocarditis, cytokine storm may also present themselves in the course of the disease [4]. It has also been reported that the risk of mortality increases in the presence of underlying diseases, secondary infections and high inflammatory indicators [5]. Furthermore, COVID-19 is milder and less common in children than in adults [6, 7].
Direct or indirect exposure to natural disasters and community-based traumatic events cause psychological distress [8]. As such, it is normal for unexpected and uncertain processes to cause anxiety. Child and adolescent mental health are strongly impacted by the family system, and the pandemic process significantly affects family interactions [9]. SARS-CoV-2 may also cause neurological and psychiatric symptoms by affecting the brain [10, 11]. Thus, the impact of the unique and rapid course of the COVID-19 outbreak on various internalization disorders in children and adolescents is still unclear [12].
An epidemiological study on adolescents in China reported increased symptoms of depression and anxiety during the COVID-19 outbreak [13]. However, there are still a limited number of studies on the psychological effects of COVID-19 in children with chronic diseases and their parents. Moreover, there is no consistency in the results of the existing studies [14, 15]. An example for these inconsistencies is that depression and anxiety scores were not found to be different in adult patients with rheumatic disease when compared to teachers and academicians during the COVID-19 outbreak in one study [16].
After detecting the first cases in Turkey, many public and private hospitals were declared “pandemic hospitals” by the government. To treat more COVID-19 patients, routine appointments in outpatient clinics were reduced and non-emergency surgeries were postponed. While these changes in the present health system facilitated the treatment of COVID-19 patients, they caused disruptions in the follow-up and treatment processes of individuals with chronic diseases who need regular follow-ups. Additionally, as we have established that COVID-19 symptoms can mimic rheumatic diseases, it is noteworthy that in the treatment of COVID-19 drugs such as steroids, hydroxychloroquine and other such biological agents, which are used in patients with rheumatic disease, are used as well. Thus, there may be an uncertain and complex relationship between rheumatic diseases and COVID-19 [17–19]. In this study, we aimed to evaluate the psychological symptoms of children and adolescents with rheumatological diseases and their parents during the outbreak.
Materials and methods
Study groups
The target population comprised of children and adolescents aged 2–18 years. Patients who regularly visited the Cerrahpasa Medical Faculty Pediatric Rheumatology Outpatient Clinic for a rheumatological disease formed the patient group. Rheumatological diseases were separated into three subgroups for the purposes of this study; (1) juvenile idiopathic arthritis (JIA); (2) familial Mediterranean fever (FMF); (3) systemic lupus erythematosus (SLE). All the patients fulfilled the “Systemic Lupus International Collaborating Clinics’’ classification criteria for SLE [20], Turkish Pediatric FMF criteria for FMF [21], “The International League of Associations for Rheumatology (ILAR)’’ criteria for JIA [22] and the diagnosis was made by pediatric rheumatologists. Children and adolescents without chronic diseases who were of similar age and gender, as well as their parents, formed the control group.
Study procedures
A web-based survey was conducted in a cross-sectional design using the Google-Forms platform. A unique link to access the online survey page was provided, and participants were explicitly asked to answer the survey only once. The protocol was approved by the Cerrahpasa Ethics Committee (Decision No: 61911 dated 14.05.2020) and Ministry of Health. The online form was sent out to the parents of participants with a brief description of the study via the phone and e-mail addresses of the outpatient clinic files of 1294 patients. The questionnaire was answered by 520 participants between the 27th of May 2020 and the 30th of June 2020. The response rate was 40.2%. While a certain part of the questionnaire had to be filled out by the parents, 52 patients filled out all parts of the questionnaire themselves. And, 9 patients had a diagnosis other than the 3 specified groups (FMF, JIA and SLE). In total, 61 patients were excluded from the study. Four hundred fifty-nine patients were included in the statistical evaluation. Participants gave their consent to participate in the study by clicking the study link sent to them. The online survey contained three parts. The first part included questions about sociodemographic data in a form prepared by the authors. The second part included the Hospital Anxiety and Depression Scale (HADS) to evaluate parental psychological distress. The third part included the State-Trait Anxiety Inventory for Children (STAI-C). The first and second parts were answered by the parents and the third part by the child.
Measures
Sociodemographic data form
This data form consisted of questions about age, sex, the presence of a COVID-19-positive individual in the family, the suspicion of COVID-19, and the Polymerase Chain Reaction (PCR) result if any such test had been done. Other questions included whether the child was exposed to COVID-19 news from the media, whether there were increased protective measures for the child, and whether the child was exposed to cigarette smoke. Patients’ parents were also asked about their thoughts on the risk of the COVID-19 pandemic related rheumatological diseases (such as the diagnosis and treatment of the child's rheumatological disease, their opinions on the effect of the child's disease and drug treatment on the risk of COVID-19, whether they consulted their doctors of the treatment process, etc.).
The hospital anxiety and depression scale (HADS)
The HADS, which included depression and anxiety subscales, consisted of 14 items. Each item was scored between 0 and 3. Depression and anxiety scores were calculated separately and each ranged from 0 to 21. The cut-off points of the scales were ≥ 11 for anxiety and ≥ 7 for depression. The validity and reliability of the Turkish version of the scale had previously been conducted [23].
The state-trait anxiety inventory for children (STAI-C)
The STAI-C was used as an anxiety measure to evaluate the state and traits of participant anxiety. There were 20 multiple-choice questions for state-trait anxiety. Each item was scored between 1 and 3. Higher scores indicated a higher level of anxiety. The state anxiety section evaluated how individuals felt in the present moment; while the trait anxiety section evaluated how individuals felt in general. Both inventories had been successfully adapted to Turkish by Özusta [24].
Statistical analysis
Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) software (version 21.0). Descriptive statistical measures (Frequency, Percentage, Mean, Standard deviation) were examined and the Kolmogorov–Smirnov distribution test was used to examine the normal distribution. Categorical variables were compared using Pearson’s Chi-square test and the Fischer’s Exact test. Since the data did not yield a normal distribution, the Mann–Whitney U test and the Kruskal–Wallis test were used for group comparisons and Spearman’s correlation analysis was used for intercorrelations between continuous parameters. Reliability results equal to or greater than 0.95 were interpreted and a p-value of < 0.05 was considered significant.
Results
Participant characteristics
In total, we examined 795 children and their parents (459 with rheumatologic diseases and 336 healthy controls). Two hundred sixty-four (57.5%) of the patients with the rheumatic disease were followed up with the diagnosis of FMF, 154 (33.6%) with JIA and 41 (8.9%) with the diagnosis of SLE. Two hundred fifty-seven (56%) of the children with rheumatologic diseases and 190 (57%) of the healthy children were female. The mean age of the patients with the rheumatic disease was 10.8 ± 5.7, and the mean age of the control group was 11.3 ± 4.5 years. There were no significant differences in age and gender between the patient and control groups. While the parents who filled the forms in both groups were most frequently mothers, the proportion of fathers who filled the forms in the patient group was higher than the control group.
Comparison of groups in terms of COVID-19 related questions
Parents reported that children in the patient group were less exposed to news relating to COVID-19 (p = 0.019). The children who experienced difficulties separating from parents when younger were more often in the patient group than in the control (p = 0.002). The results regarding sociodemographic characteristics and the questions regarding the epidemic process are shown in Table 1. Fifteen of the patients with rheumatic disease and four of the control group had known psychiatric diagnosis. The proportion of parents who increased measures to protect their children was similar across groups (92.6% for both groups). While 13 children in the patient group and 14 children in the control group had been referred to the hospital due to suspicions of COVID-19, only two of those in the patient group and three in the control had positive PCR test results.
Table 1.
Comparison of patient and control groups in terms of sociodemographic characteristics, COVID-19 risk and problems related to the pandemic process
| Patient group (n = 459) | Control group (n = 336) | P | |
|---|---|---|---|
| Mean ± SD or n (%) | |||
| Childs age (years) | 10.8 ± 4.7 | 11.3 ± 4.5 | 0.060 |
| Childs sex (F/M) | 257/202 | 190/146 | 0.876 |
| Who filled out the form? | |||
| Mother | 329 (71.7) | 275 (81.8) | |
| Father | 127 (27.7) | 52 (15.5) | < 0.001 |
| Other | 3 (0.7) | 9 (2.7) | |
| Have you used preventive treatment? (such as vitamins) | |||
| Yes | 117 (25.5) | 85 (25.3) | 0.951 |
| No | 342 (74.5) | 251 (74.7) | |
| Is your child exposed to cigarette smoke? | |||
| Yes | 53 (11.5) | 38(11.3) | 0.917 |
| No | 406 (84.5) | 298 (88.7) | |
| Do you continue your job? | |||
| Yes | 221 (48.1) | 215 (64) | < 0.001 |
| No | 238 (51.9) | 121 (36) | |
| Has the time you spent with your child increased? | |||
| Yes | 307 (66.9) | 167 (49.7) | < 0.001 |
| No | 152 (33.1) | 169 (50.3) | |
| Anyone in your family diagnosed COVID-19? | |||
| Yes | 20 (4.4) | 26 (7.7) | 0.044 |
| No | 439 (95.6) | 310 (92.3) | |
| Are there any health workers in the family? | |||
| Yes | 34 (7.4) | 38 (11.3) | 0.058 |
| No | 425 (92.6) | 298 (88.7) | |
| Is your child exposed to news about COVID-19? | |||
| Yes | 318 (69.3) | 258 (76.8) | 0.019 |
| No | 141 (30.7) | 78 (23.2) | |
| Have you created a new layout for your child? | |||
| Yes | 327 (71.2) | 244 (72.6) | 0.670 |
| No | 132 (28.8) | 92 (27.4) | |
| Does your child have more trouble separating from you than before? | |||
| Yes | 94 (20.5) | 41 (12.2) | 0.002 |
| No | 365 (79.5) | 295 (87.8) | |
Comparison of groups in terms of psychological scales
To evaluate the effects of developmental characteristics on children, comparisons of psychological scales were made by dividing children into three groups according to their age: < 8, 8–12 and > 13. There were no significant differences between the parental depression and anxiety scores of those in the patient and in the control groups for the < 8 and 8–12 age groups (for all p > 0.05). The depression and anxiety scores of the parents of patients with the rheumatic disease aged > 13 years were significantly higher than the control group scores (6.6 ± 3.8 vs. 5.3 ± 3.9, p < 0.001 for parental depression and 7.3 ± 3.4 vs. 6.3 ± 3.8, p = 0.006 for parental anxiety).
Between the ages of 8 and 12, STAI -C state anxiety scores in patients with a rheumatic disease (32.0 ± 7.3) were significantly higher than the control group scores (29.1 ± 4.5, p = 0.02). At the age of > 13, STAI-C trait anxiety scores were significantly higher in patients with the rheumatic disease than in the control group (36.1 ± 8.7 vs. 33.3 ± 7.9; p = 0.002) (Table 2).
Table 2.
Comparison of psychological scale scores of patient and control groups according to age groups and gender
| Patient group | Control group | z | p | |
|---|---|---|---|---|
| < 8 years | (n = 132) | (n = 94) | ||
| HADS-anxiety | 7.2 ± 3.8 | 7.5 ± 3.8 | − 0.793 | 0.428 |
| HADS-depression | 6.2 ± 3.8 | 6.0 ± 3.7 | − 0.363 | 0.716 |
| 8–12 years | (n = 155) | (n = 71) | ||
|---|---|---|---|---|
| HADS-anxiety | 7.3 ± 3.8 | 7.5 ± 4.2 | − 0.152 | 0.879 |
| HADS-depression | 6.5 ± 3.8 | 6.9 ± 4.3 | − 0.706 | 0.480 |
| STAI-C state | 32.0 ± 7.3 | 29.1 ± 4.5 | − 2.326 | 0.02 |
| STAI-C trait | 35.5 ± 8.5 | 34.1 ± 8.0 | − 1.297 | 0.195 |
| ≥ 13 years | (n = 172) | (n = 171) | ||
|---|---|---|---|---|
| HADS-anxiety | 7.3 ± 3.4 | 6.3 ± 3.8 | − 2.757 | 0.006 |
| HADS-depression | 6.6 ± 3.8 | 5.3 ± 3.9 | − 3.580 | < 0.001 |
| STAI-C state | 32.3 ± 7.6 | 33.1 ± 5.6 | − 0.883 | 0.377 |
| STAI-C trait | 36.1 ± 8.7 | 33.3 ± 7.9 | − 3.088 | 0.002 |
| Female | (n = 257) | (n = 190) | ||
|---|---|---|---|---|
| HADS-anxiety | 7.5 ± 3.7 | 7.1 ± 4.0 | − 1.263 | 0.207 |
| HADS-depression | 6.4 ± 3.8 | 6.0 ± 4.2 | − 1.427 | 0.154 |
| STAI-C state | 32 ± 6.8 | 32.9 ± 6.2 | − 1.061 | 0.289 |
| STAI-C trait | 35.5 ± 8.2 | 34.9 ± 7.9 | − 1.026 | 0.305 |
| Male | (n = 202) | (n = 146) | ||
|---|---|---|---|---|
| HADS-anxiety | 6.9 ± 3.5 | 6.6 ± 3.7 | − 0.862 | 0.389 |
| HADS-depression | 6.4 ± 3.9 | 5.5 ± 3.7 | − 2.099 | 0.036 |
| STAI-C state | 32.5 ± 7.3 | 30.4 ± 4.4 | − 2.444 | 0.015 |
| STAI-C trait | 35.9 ± 8.4 | 31.2 ± 7.1 | − 4.850 | < 0.001 |
HAD hospital anxiety and depression scale, STAI-C state-trait anxiety inventory for children
When evaluated according to sex, there were no significant differences between the patient and control groups in terms of the parent and child scales for females. However, for males; while the anxiety scores of the parents were similar across groups, the depression scores of the parents of patients were significantly higher than the control group scores (6.4 ± 3.9 vs. 5.5 ± 3.7; p = 0.036 for depression). Additionally, for males; child trait anxiety (32.5 ± 7.3 vs. 30.4 ± 4.4; p = 0.015) and child state anxiety scores (35.9 ± 8.4 vs. 31.2 ± 7.1; p < 0.001) were significantly higher than the control group scores (Table 2).
Comparison of psychological variables according to the types of rheumatic diseases and COVID-19 outbreak-related questions in the patient group
When the patient group was compared according to the types of their rheumatic diseases, no differences were found with the scale scores between the FMF, JIA and SLE groups (Table 3). Four hundred eighteen (91.1%) patients regularly used drugs for their rheumatic diseases. One hundred eighty-seven (40.7%) parents consulted their doctors about follow-ups and treatments during the Covid-19 pandemic process. Three hundred eighty (69.3%) parents thought that their child's rheumatic disease increased the risk of their getting COVID-19. Fifty-nine (12.9%) of the parents reported believing that the drugs they used for rheumatic diseases increased the risk of getting COVID-19, 70 (15.3%) believed they decreased the risk, and 330 (71.9%) believed they made no impact. Two hundred sixty-two (57.1%) parents thought that missing outpatient clinic appointments due to the pandemic were a problem. Thirty-three (7.2%) parents stated that they had problems acquiring their drug supply.
Table 3.
Comparison of psychological scale scores according to the diagnosis of the rheumatology patients
| FMF (n = 264) | JIA (n = 154) | SLE (n = 41) | p | |
|---|---|---|---|---|
| Age | 10.2 ± 4.5 | 10.9 ± 4.9 | 13.9 ± 4.0 | < 0.001 |
| HADS-anxiety | 7.3 ± 3.6 | 7.2 ± 3.7 | 7.3 ± 3.6 | 0.877 |
| HADS-depression | 6.5 ± 3.8 | 6.5 ± 3.9 | 5.7 ± 3.2 | 0.608 |
| STAI-C state | 32.7 ± 7.2 | 31.7 ± 6.6 | 31.1 ± 7.3 | 0.264 |
| STAI-C trait | 35.3 ± 8.8 | 36.1 ± 7.8 | 36.4 ± 6.2 | 0.532 |
HAD hospital anxiety and depression scale, FMF familial Mediterranean fever, JIA juvenile idiopathic arthritis, SLE systemic lupus erythematosus, STAI-C state-trait anxiety inventory for children
When patients with the rheumatic disease were divided into two groups in terms of these various parameters (i.e., their consulting a doctor about treatment during the outbreak, their thinking that the disease increased their likelihood of getting COVID-19, their thinking that missing a clinic appointment was a problem, the presence of their rheumatic disease-related attacks during the pandemic, and their use of biological agents) no significant differences between groups for all HADS and STAI-C scores were found (Table 4). There were no significant differences in terms of scale scores between male and female patients with rheumatic disease. When the patients were grouped according to 8–12 years and > 13 years old, there were no significant differences between scale scores found (p > 0.05 for all).
Table 4.
Comparison of psychological scale scores according to COVID-19 risk perceptions of rheumatology patients
| HADS-anxiety | p | HADS-depression | p | STAI-C state | p | STAI-C trait | p | |
|---|---|---|---|---|---|---|---|---|
| Consulting own doctor about COVID-19 | ||||||||
| Yes (n = 187) | 6.9 ± 3.4 | 0.094 | 6.3 ± 3.9 | 0.574 | 31.8 ± 6.6 | 0.284 | 35.6 ± 7.3 | 0.837 |
| No (n = 272) | 7.5 ± 3.8 | 6.5 ± 3.7 | 32.6 ± 7.5 | 35.8 ± 9.0 | ||||
| Is your child’s rheumatological disease a risk for COVID-19? | ||||||||
| Yes (n = 318) | 7.4 ± 3.7 | 0.492 | 6.5 ± 3.8 | 0.764 | 32.3 ± 7.4 | 0.963 | 35.6 ± 8.6 | 0.888 |
| No (n = 141) | 7.1 ± 3.6 | 6.3 ± 3.8 | 32.2 ± 6.4 | 35.8 ± 7.6 | ||||
| Missing outpatient clinic appointment is a problem? | ||||||||
| Yes (n = 262) | 7.5 ± 3.7 | 0.068 | 6.5 ± 3.6 | 0.390 | 31.8 ± 7.3 | 0.277 | 36.0 ± 9.1 | 0.339 |
| No (n = 197) | 6.9 ± 3.6 | 6.3 ± 4.0 | 32.7 ± 6.8 | 35.3 ± 7.2 | ||||
| Has the child had an attack during the pandemic process? | ||||||||
| Yes (n = 118) | 7.5 ± 3.4 | 0.189 | 6.7 ± 3.3 | 0.216 | 32.2 ± 6.3 | 0.656 | 35.4 ± 7.3 | 0.545 |
| No (n = 341) | 7.2 ± 3.7 | 6.3 ± 4.0 | 32.2 ± 7.4 | 35.8 ± 8.6 | ||||
| Does the child use biological agents? | ||||||||
| Yes (n = 86) | 6.8 ± 3.4 | 0.213 | 6.3 ± 4.0 | 0.580 | 32.4 ± 6.6 | 0.992 | 35.7 ± 7.3 | 0.808 |
| No (n = 371) | 7.0 ± 3.7 | 6.4 ± 3.8 | 32.2 ± 7.2 | 35.7 ± 8.5 | ||||
HAD hospital anxiety and depression scale, STAI-C state-trait anxiety inventory for children
There were no significant correlations between the ages of the children and the scale scores of the parents and children. There was a moderate positive correlation between the HADS anxiety scores of the parents and the STAI-C state and STAI-C trait scores (r = 0.313, p < 0.001; r = 0.414, p < 0.001, respectively). Additionally, there was a moderate positive correlation between the HADS depression scores of the parents and the STAI-C state and STAI-C trait scores (r = 0.367, p < 0.001; r = 0.300, p < 0.001, respectively) (Table 5).
Table 5.
Correlation between parent and children’s scale scores in the patient group
| HADS-anxiety | HADS-depression | STAI-C state | STAI-C trait | |
|---|---|---|---|---|
| Age | − 0.025 | − 0.046 | 0.024 | − 0.032 |
| HADS-anxiety | 0.632*** | 0.313*** | 0.414*** | |
| HADS-depression | 0.367*** | 0.300*** | ||
| STAI-C state | 0.603*** | |||
| STAI-C trait |
HAD hospital anxiety and depression scale, STAI-C state-trait anxiety inventory for children
*P < 0.05
**P < 0.01
***P < 0.001
Discussion
This study showed that, while depression and anxiety scores in the parents of patients with rheumatic disease older than 13 years were higher than that of the control group, there were no differences between the healthy peers in the groups younger than 8 years and between 8 and 12 years. Similarly, the trait anxiety scores of the children who were patients with rheumatic disease older than 13 years were higher than the children who were controls. While psychological scale results were similar across the patient and control groups for female children and their parents, they were significantly higher in the patient group for male children.
Children and adolescents are highly susceptible to the impact of stressors during mentally sensitive developmental periods, and therefore their mental health during and after the pandemic requires special attention [25, 26]. It is known that negative emotional reactions such as anxiety and depression can be experienced in society during epidemics [27, 28]. In a study conducted on adolescents in China in the early stages of the COVID-19 outbreak, a prevalence of 44% for depressive symptoms and 37% for anxiety symptoms was reported [13]. While there are studies reporting an increase in the prevalence of depression after the pandemic when compared to before [29]; there are also studies reporting that depression and anxiety did not increase [30].
Although there are many studies on the psychological effects of the pandemic upon the general population, including healthcare workers, there are fewer studies on individuals with chronic diseases. Once again, in a population-based study in China during the epidemic period, moderate to severe anxiety was found in one-third of participants, while being a woman and having a chronic disease were associated with more negative psychological effects [31]. With the pandemic process, there have been changes in the health systems of countries, closures of inpatient services, limiting of outpatient services to only accommodate emergencies, and uncertainty has arisen in the follow-up and treatment processes of individuals with chronic illnesses. In studies conducted with children with different rheumatological diseases before the pandemic, no differences were found in terms of depression and anxiety scores when they were compared to healthy children [32–35]. However, we thought that the psychiatric symptoms of parents and children with rheumatic diseases would be greater than healthy individuals, due to COVID-19 symptoms mimicking rheumatological diseases and the complex and unclear relationship that emerged with the introduction of some rheumatology drugs into the treatment of COVID-19. Greater results were found in terms of trait anxiety in children older than 13 years and psychiatric symptoms in their parents in the rheumatology group. However, we found no differences between the patient and control groups of the parents of children older than 8 years and between 8 and 12 years. In the literature, while trait anxiety in the mothers of children with cystic fibrosis was found to be higher than the control group during the COVID-19 epidemic [15]; depression and anxiety in children with chronic lung disease and their parents were similar to the control group [14]. The fact that healthy children had not experienced a fear of illness before and that their anxiety increased in cases of serious illness risk may be the cause of no differences between healthy and chronic disease groups.
Patients with autoimmune diseases can develop stronger resilience as an adaptive response to the chronicity of their condition [36–38]. Resilience can be defined as a multidimensional structure that explains the long-term positive effects resulting from the ability to adapt to threatening or traumatic experiences [39]. Resilience is strongly negatively correlated with depression and anxiety [38]. In our study, the similarity of depression and anxiety scores between the patient and control groups of children younger than 12 years and their parents may be related to the resilience that develops adaptively to the presence of chronic disease.
At the same time, the cognitive and emotional processing of the subjective experiences of parents and children after medical trauma such as chronic illness and the adaptation potential of families can provide post-traumatic growth [40, 41]. It was found that problem-focused coping strategies were used more with mothers of children with chronic lung disease than with mothers of healthy children [14]. It is natural that an extraordinary and uncertain situation creates anxiety. The psychological response of the child is determined by the level of cognitive development and understanding of the cause of the disaster, as well as the reactions of family members and the child's personality and coping mechanisms [8]. While we did not find a difference in the trait anxiety scores of children between 8 and 12 years of age, we found that adolescents with rheumatologic diseases had higher trait anxiety scores than controls. Adolescents' higher awareness of the risks rheumatological diseases pose towards COVID-19 may have led to the higher anxiety scores of patients over the age of 13 when compared to the control group. The depression and anxiety scores of parents of adolescents with rheumatological diseases were also higher than the control group scores. The desire of adolescents to act more autonomously and the lower parental control in this age group may increase depression and anxiety in the parents in the patient group.
While the psychiatric symptoms of parents of female children were similar across the patient and control groups; for males, both the state and trait anxiety of the children and the depression scores of their parents were higher in the patient group. In community studies during the COVID-19 outbreak, the female gender was associated with higher anxiety in children, adolescents and adults [13, 42]. In our study, the anxiety scores of females were higher when compared to males within the whole sample. However, there were no differences when only the patient group was compared. Thus, we may extrapolate that the female ability to adapt to chronic illness may be greater than the male.
In our study, when we grouped patients with rheumatic disease as JIA, SLE and FMF, according to their diagnosis, the found scale scores were similar across groups. Similar results have been shown in adult patients with the rheumatic disease [16]. More than half of the parents thought that the child's rheumatological disease increased their risk of getting COVID-19. However, the psychological scale scores of the parents and children did not differ across groups when the parents were grouped according to their thought that the disease increased the risk of getting COVID-19, their consulting their own doctor about their child’s treatment, their use of biological agents, and the presence of their illness-related attacks. Caregivers’ anxiety and stress may be affected not only by the direct effects of the virus and disease risk but also by other factors such as short and long-term financial problems. The mental processes of both parents and children are affected by factors such as the loss of many activities in the children’s lives (e.g. school, extracurricular activities, social interactions, etc.), the reorganizations of their family life, the loss of their support systems, and the families' obligation to inform their children about the epidemic [9, 43]. As parents' own losses (such as work, loved ones in events of death, their own health) increase, their capacity to buffer children's stress decrease and traumatic consequences for children increase [9]. In our study, the depression and anxiety scores of the parents were positively correlated with the anxiety scores of the children. Similarly, in the literature, it has been shown that a mother's depression increases the internalization and externalization problems of their children [44].
In conclusion, the children with rheumatological diseases and their parents were psychologically affected only when older than 13 years of age. Additionally, male patients had higher anxiety scores than their healthy peers. Rheumatological disease diagnosis and disease-related variables had no effect on psychological status.
The limitations of our study can be summarized as follows: First, no data is present regarding the clinical features, biochemical findings and remission status of patients with rheumatic disease. We only asked the participants about the presence of attacks during the COVID-19 pandemic. Although this does not provide all clinical data on disease activation, it may give an indirect idea. Second, we looked at the effects of the presence of rheumatological diseases on psychological status. However, we did not consider factors such as resilience or financial difficulties, that could affect responses to trauma. Since our participants were volunteers, those who were more severely affected by the pandemic may have not participated. We also used self-report scales instead of structured clinical interviews. Furthermore, it is not possible to give causal results, as we did not evaluate the psychological conditions before the outbreak. The results of our study can only provide an insight into the early phase of the pandemic. Long-term effects may differ. Longitudinal studies are needed to evaluate important factors such as financial problems and resilience, that can affect responses to trauma and coping strategies, to better understand the psychological impact of the outbreak, especially on children with chronic diseases and their parents.
Acknowledgments
We wish to thank all the patients who participated in this study and their parents and the staff of the participating center.
Author contributions
GD and AA conceptualized and designed the study, drafted the initial manuscript and had full access to all the data in the study. FH and HD designed the study, conducted the data analyses, drafted the initial manuscript and had full access to all the data in the study. GD, MY and SS drafted the initial manuscript. KB and OK conceptualized and designed the study, drafted the final manuscript and had full access to all the data in the study. All authors reviewed and revised the manuscript and approved the final manuscript as submitted and agree to be accountable for all aspects of the work.
Funding
We have no funding sources that supported our work.
Compliance with ethical standards
Conflict of interest
None of the authors of this paper has a conflict of interest, including specific financial interests, relationships and/or affiliations relevant to the subject matter or materials included.
Ethical approval
The study was reviewed and approved by the local ethics committee.
Footnotes
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Contributor Information
Gizem Durcan, Email: drgizemkaymak@hotmail.com.
Kenan Barut, Email: drkenanbarut@hotmail.com.
Fatih Haslak, Email: drfatihhaslak@gmail.com.
Hilal Doktur, Email: hilaldr2@yahoo.com.
Mehmet Yildiz, Email: yildizmehmet@istanbul.edu.tr.
Amra Adrovic, Email: amra.adrovic@istanbul.edu.tr.
Sezgin Sahin, Email: sezgin@istanbul.edu.tr.
Ozgur Kasapcopur, Email: ozgurkasapcopur@hotmail.com.
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