Psychological Effects and Parent Quality of Life in Children of Vision Loss for Uveitis

Purpose: Juvenile idiopathic arthritis (JIA) is a chronic inammatory disease common in children and young adults. Uveitis is most frequent serious extra-articular JIA manifestation and can lead to severe ocular complications, vision loss and permanent blindness. The aim of this study is to evaluate the quality of life and the psychological effects of JIA associated with uveitis (JIA-U) on these children and to explore the effect of a child’s chronic illness on parents. Materials and Methods: 30 children and adolescents with active uveitis referred to Unit of Ophthalmology, Giovanni XXIII Hospital of Bari and 30 subjects of control group were enrolled with their parents. Informed consent was signed by the subjects and four questionnaires were administered: Child Behaviour Checklist (CBCL), Parent Stress Index in short form (PSI), Pediatric Quality of Life Inventory (PedsQL) and Coping Inventory for Stressful Situations (CISS). Data were collected from February 2020 to December 2020. Results: The analysis of the emotional and behavioral problems of children (CBCL) with JIA associated with uveitis, the rate of parent’s stress (PSI) and the strategies of coping with the stress (CISS) of their families did not show statistically signicant differences between the clinical sample and the control group. Signicant differences were observed in quality of life between the two groups. In particular, signicant differences (p<0,05) were found in all domains of PedsQL: physical functioning (PF), emotional functioning (EF), social functioning (SF) and school functioning (ScF). Conclusions: This study shows a worse quality of life in children with JIA-U. Several ocular complications, eye examinations and the rigor of long-term treatment inuence health-related quality of life in these children. This study suggests the importance of helping children with uveitis cope with chronic disease and may improve outcome. Inclusion of a screening related quality of life should be considered in management of children with JIA-U. Further studies are needed to evaluate the long-term impact on psychological health in these children.


Introduction
Juvenile idiopathic arthritis (JIA) is a chronic in ammatory disease common in children and young adults. 1 The supported etiology is an immunogenic mechanism, and genetic and environment factors are also involved. 2 The uveitis is most frequent serious extra-articular manifestation. 3 Although the eye is known as an immune-privileged organ, when the breakdown of the blood-aqueous humour barrier is made, the non-infectious uvea in ammation is done. 4 The oligoarticular (four or fewer joints involved) and polyarticular (affects ve or more joints) JIA are the most common types associated with uveitis. Especially, the oligoarticular type develops uveitis at a higher rate (20%) than polyarticular (5%) one. 5 According to Standardization of Uveitis Nomenclature (SUN) Criteria, uveitis features associated with JIA include anterior chamber cells, anterior chamber are, vitreous cells, and haze. 6 Other clinical ndings are band keratopathy, posterior synechiae, cataract, glaucoma, and macular edema. 7 JIA is strongly associated with psychosocial distress especially when associated with uveitis. [8][9][10] The sudden or insidious symptoms onset, trend of remission and recrudescence, visual loss, chronic therapy (topical, systemic, or biological molecules), short or medium-long term eye complications of uveitis have a strong psychological impact on the quality of life of children and their families.
The signi cance to investigate psychological changes in patients with chronic diseases is wellacknowledged. 11,12 Similarly, parenting stress in pediatric chronic physical illnesses is well known. For instance, diabetes, 13 cystic brosis, 14 asthma, cancer, epilepsy, sickle cell disease 15,16 are some of the chronic health conditions previously described in literature.
Understanding the measure of parents' stress and strategies used as an adaptation can direct towards an improvement in the therapeutic and family support approach.
The study aims to investigate: 1) the quality of life of children and adolescent with JIA-U (PedsQL), 2) young patients with JIA associated with uveitis behavior from parents' point of view (CBCL Test), 3) the rate of parents' stress (PSI-SF stairs), 4) the strategies applied by their family to cope with stress (CISS scale), and comparing them with children without chronic diseases and their families. The research hypothesis of this study is that the JIA-U worsened the quality of life and the emotional and behavioral problems of these children and increased stress levels in the parents of these patients. The period in which we checked these families and administered the tests coincided with the pandemic period SARS-CoV2. Therefore, all data collected will refer to this period.

Methods
The clinical sample consisted of 30 children and adolescents with active uveitis referred to Unit of Ophthalmology, Giovanni XXIII Hospital of Bari and their parents. The study was carried during the period February-December 2020. Eligibility criteria were active uveitis, having no other systemic or ocular disease that could potentially affect vision and being under aged 18 years. We administrated validated questionnaires such as Child Behaviour Checklist (CBCL), 17 Parent stress Index in short form (PSI), 18 Pediatric Quality of Life Inventory (PedsQL), 19 and Coping Inventory for Stressful Situations (CISS). 20,21 Parent and patient-based questionnaires were completed in person after the ophthalmic examination at the clinic. A member of the research team was available to read the questions to subjects who requested it. The control group consisted of 30 children and adolescents that was random recruited, based on the availability of parents and subjects to participate in the study, from school located in Bari and Foggia.
The study was approved by the local Ethics Committee. An informed consent was obtained from all patients who agreed to participate in the study.

Assessment
The assessment was carried out by administering standardized scales, the "PSI", the "CBCL", the "PedsQL" and the "CISS": the PSI Short Form (PSI / SF) is a reliable questionnaire designed to measure parental stress and di culties about the parenting role. It is a summary form of the Parenting Stress Index (PSI) full-length test. 18 All 36 items on The Short Form are contained on the Long Form and are written at a 5th-grade reading level. Each item requires the parent to respond with a statement on a ve-point Likert scale (1=Strongly Agree, 2=Agree, 3=Not Sure, 4=Disagree, and 5=Strongly Disagree). The PSI consists of the three subscales: parenting distress (PD) scale, dysfunctional interaction parent-child (P-CDI) scale, di cult child (DC) scale. The PD scales de ne the level of distress that a parent perceives in his parenting role. The P-CDI scale expresses the parent's perception of a child who does not respond to his or her expectations and therefore of a non-gratifying interaction with the child. The DC scale values how much the parent perceives his child as easy/di cult to manage. The PSI-SF produces subscales raw scores ranging from 12 to 60 and an overall parenting stress total score that ranges from 36 to 180; a higher score indicates a greater level of stress. A score above the 90th percentile indicates clinically signi cant level of parenting stress. The total stress (TS) scores, obtained by the sum of the scores of the 3 subscales, is an index of total parenting stress. The test includes also a Defensive Responding (DF) scale that indicates the parent tends to give a better self-image, minimizing the problems and the perceived stress in the relationship with the child.
The CBCL is a common questionnaire used to assess emotional and behavioral problems in children, 17 as rated by parents and include CBCL/6-18 and CBCL/1 ½-5 for different ages.
The rst section of the scale includes 20 items related to child's participation in sports, hobbies, games, activities, organizations, jobs, chores, friendships, social interactions during play, independent work, and school functioning. The second section consists of 120 items on behavior or emotional problems during the past 6 months. The main areas investigated are aggression, hyperactivity, bullying, conduct problems, de ance, and violence. Responses are recorded on a Likert scale: 0=Not true, 1=Somewhat or Sometimes true, 2=very true or often true. Lower scores indicate lower functioning on the academic performance and adaptive functioning scales. Higher scores indicate higher levels of maladaptive behavior on the syndrome, total problems, externalizing, and internalizing scales.
The PedsQL is a validated measure of general health-related QOL in children and adolescent from 2 to 18 years of age. 19 It consists of four scales measured on a 5-point-scale: 1: physical functioning (PF)8 items, 2: emotional functioning (EF) 5 items, 3: social functioning (SF) 5 items and 4: school functioning (ScF) 5 items. The questions investigate how many problems children has had in the past month Score range from 0 to 100; higher scores indicate better QoL. Child self-report includes ages 5 to 7, 8 to 12 and 13 to 18 years. Parent-report includes ages 2 to 4 (toddler), 5 to 7 (young child), 8 to 12 (child), 13 to 18 (adolescent). A 5-point response scale is utilized: 0 (never a problem), 1 (almost never a problem), 2 (sometimes a problem), 3 (often a problem), 4 (almost always a problem). To further increase the ease of use for the young child self-report (ages 5-7), the response scale is simpli ed to a 3-point scale: 0 (not at all a problem, 2 (sometimes a problem), 3 (a lot of a problem). Parent-report includes toddler age range, which does not include self-report form and only 3 items for the school functioning scale. Items are reverse-scored and transformed 0 to 100 (0=100, 1=75,2=50, 3=25, 4=0). Higher score indicates a better Health related-QoL (HRQoL).
The CISS measures the following three type of coping styles: Task-Oriented Coping (dealing with the problem at hand), Emotion-Oriented Coping (focus on consequent emotions) and Avoidance -Oriented Coping (Distraction and Social Diversion). 20,21 The CISS includes adolescent and adult forms. They include 48 items and use a ve-point response format. The adolescent version of the CISS is suitable for individuals between the ages of 13 and 18. The adult version of the CISS is suitable for individuals who are 18 years of age and older. For this study we used only the adult version.

Statistical analysis
Descriptive statistics were used to summarize the variables studied and the characteristics of the subjects. Differences among demo-graphic variables were evaluated by the chi-squared test (sex). Nonparametric tests (Mann-Whitney) were used to examine the differences in age, PSI / SF, CBCL, CISS, PedsQL between group. A P value of less than .05 was considered as statistically signi cant. For statistical processing, we used the data processing program the Statistical Package for Social Science, Version 20.0.

Results
The socio-demographic characteristics of the sample and control group are summarized in Table 1. The analysis of the emotional and behavioral problems of the patients included in the study did not show signi cant statistical differences in two groups as shown in table 2.
No statistically signi cant differences were found in variables analyzed in the PSI and CISS questionnaire, as shown in tables 3 and 4.
The analysis conducted to evaluate differences in the quality of life (QoL) highlights statistically signi cant differences in all variables of the PedsQL questionnaire. In particular, signi cant data were found in the variables: PF (p <0.05), EF (p <0.05), SF (p <0.05) and ScF (p<0,.05). They are summarized in Table 5.

Discussion
A poor number of studies examined the impact of QoL in patients with JIA-U.
It is not infrequent that the uveitis appears as asymptomatic or the child does not perceive it, while it being in an advanced stage. Therefore, we are faced already with visual loss, or ocular complications to be managed and sometimes we have to resort to surgery. 22 Most recent studies concern solely adult patients, 8,23,24 contrary very few about children and teens and their parents. Our study is one of them and, to our knowledge, it is the only one to have a control group.
Analyzing the responses to the PedsQL questionnaire signi cant results emerged in all domains: PF, EF, SF, ScF. These results highlight that uveitis has a major impact on the quality of life and affects every aspect of the children's life. Our results agree with most of other studies. 10,[25][26][27][28] In particular a study reviewed groups of children (and their parents) with visual impairment due to ocular conditions apart from the uveitis (and their parents) and found comments from 510 (44%) of 1163 children and 1078 (55%) of 1952 parents related with the QoL, such as psychosocial, impact on the school, expectations and frustrations, dependency, and participation. 25 An other study conducted a semistructured interview on 10 children and adolescents aged between 6 and their parents; impact on the school, social factors, and emotional reactions were investigated, considering clinical evidence and therapeutic strategies were practiced. 26 A recent study had proven a worsening of overall parameters of the QoL among children with a visual impairment, as measured by the PedsQL, version 4.0.6. 27 A series of factors JIA-U-related were contemplated how strongly impactful on the QoL in these patients.
These studies show that indeed uveitis is associated with worse physical and mental health-related quality of life in children because of additional important medical stressors in this population. 10,28 Management of uveitis consists in complicated examinations, which can be frightening for children, and complex regimens of topical and systemic medications, which can be di cult to follow. Parents in fact report that children have di culty understanding treatment regimens. Furthermore, children with uveitis may need to miss numerous school days for eye treatments and often may miss school for long periods because of complications. Many children report di culty compensating for missed course work and this obviously has a negative impact on their academic performance. Absences from school result also in less opportunities to socialize with peers and loss of friends. These children have less time to spent with other children for eye examinations and treatments and often changes in vision affects the ability to play some sports and to take part in play and leisure activities. Furthermore, children nd embarrassing to talk about their eye conditions with their peers and this contributes to the deterioration of interpersonal relationships. Uveitis and generally chronic illness of childhood can also lead to a slower development of autonomy, close relationships with parents and high levels of parental involvement. These children are vulnerable to being unable to manage their disease enough to ask for the help of parents even in adulthood. For all these reasons children with uveitis experience negative emotions as sadness, anxiety and anger for the future, according to the results of our study.
The American Academy of Pediatrics Section on Rheumatology and Section on Ophthalmology recommended then ophthalmology screenings every 3-4 months until 7 years of age to monitor the disease development, considering in the childhood the higher risk to develop uveitis for youngest with JIA. 29 For the correct adherence to the therapy, attention and care of the family is fundamental. 28 The chronic disease so had a strong impact on the child's parents. increase in parenting distress in the pandemic period. [31][32][33] The main stressors for parents were having to reconcile work with family routine. Many parents worked from home, with related logistical problems and at the same time, due to the closure of schools, managing their children in the context of personal autonomy, management of meals, school activities, and free time. Further causes of stress were in many cases the loss of work and a direct experience with Covid-19. This would explain why from our data, parenting stress is high but comparable to those parents of the control sample.
The statistical analysis of the CBCL questionnaire did not show signi cant results. It appears from our data that a chronic disease such as JIA-U does not cause emotional and behavioral problems in children.
To the best of our knowledge, there are no other studies that focused on CBCL in children with JIA-U. A coping with anxiety was reported instead in adolescents. 34 The importance to screen psychological challenges in even younger children origin from the possibility that chronic disease might develop in anxiety and depression in adulthood. [35][36][37][38] For this reason, we believe it is important to evaluate the psychological health of these children through frequent screening.
Our study is also the only one that studied the adaptation of the parents on the child's clinical conditions (CISS Test). In this perspective, parents' adaptative skills may be crucial to manage the clinical condition, depending on this even the child's behavior. However, no signi cant results emerged from the CISS. Several studies show instead that the use of positive coping strategies is considered a necessary step in achieving resiliency and successful adaptation to stress. 39,40 Agree with other study, our impression is that parents help their children when they focus coping efforts on altering controllable factors. 28 In all these cases we have observed various examples of resilience in children and their parents.
Some limitations of our study should be noted. The number of the sample is limited and the interview took place with a single parent, mainly mothers with a low number of fathers recruited. Finally, we collected data in the rst and second wave of the pandemic. We believe this may have affected the stress levels of the general population and acted as a confounding factor on our data.

Conclusion
Children Organs, Eye Clinic, Bari University, Bari, Italy. It adhered to the tenets of the Declaration of Helsinki. This paper is a retrospective study and is approved by the Independent Ethical Committee -IEC, Policlinico of Bari. Written informed consent was obtained from all subjects.

Consent for publication
Not applicable.

Availability of supporting data and materials
The datasets during and/or analysed during the current study available from the corresponding author on reasonable request.

Competing interests
The author(s) declared no potential con icts of interest with respect to the research, authorship, and/or publication of this article.

Funding
None.

Authors' contributions
All authors attest that they meet the current ICMJE criteria for Authorship. All authors reviewed the manuscript.