key: cord-0899788-mgno3ya0
authors: Sabapathy, Thusa; Goss, Megan; Borelli, Jessie; Steinberg-Epstein, Robin
title: A Pediatrician’s Guide to Working with Children on the Autism Spectrum in COVID-19 and Beyond: Retrospect and Prospect
date: 2022-04-05
journal: Adv Pediatr
DOI: 10.1016/j.yapd.2022.04.001
sha: da4eef5c3decb461335f75efa1593f577521e5e6
doc_id: 899788
cord_uid: mgno3ya0

nan

Introduction management, this is not yet standard of care and more research working with the pediatric autistic population, specifically, is needed (7, 8, 9) . Given these multi-tiered risk factors, autistic children must be recognized as a high-risk population for COVID-19.

During the initial part of the pandemic, the autistic community voiced fears of "healthcare rationing": an example of which is prioritizing a neurotypical patient over a patient with a neurodevelopmental disorder should only one ventilator be available (10). Many US states and several European countries issued crisis care guidelines at the pandemic's peak, raising community concerns for exclusion of care in specific adult populations, such as individuals with disabilities and the elderly (11, 12). Such policies must receive critical evaluation, especially given the aforementioned heightened risk for hospitalization and death of the autistic population so that autistic patients are treated fairly and ethically.

Due to scientific innovation and collaboration, at the time of this article, the US Food & Drug Administration (FDA) approved three vaccines against COVID-19 in adults, one with full FDA-approval and two others with Emergency Use Approval (13). Prior to the pandemic, autistic children were vaccinated at lower rates than neurotypical children (14) . Studies published after the pandemic's onset found reasons for vaccine hesitancy in parents of autistic children included beliefs that vaccines led to autism and developmental plateaus (15, 16) .

However, a large study of autistic adults found higher rates of COVID-19 vaccination compared to age-matched controls (17). This could be due to many factors including parental oversight of autistic individuals and concern for more severe COVID-19 illness. A small study found no increased COVID-19 vaccine side-effects, such as fever or fatigue, in autistic patients compared to non-autistic patients (18). These data support favorable trends in combating the pandemic in J o u r n a l P r e -p r o o f autistic individuals, and providers should continue to refer to FDA recommendations regarding updates on vaccination age cut-offs and booster doses to best protect autistic patients. J o u r n a l P r e -p r o o f However, there were drawbacks to this modality of patient care with technology utilization challenges and loss of personal perspectives with telemedicine (22). Providers experienced discomfort with diagnostic reliability, due to lack of in-person physical exams, lack of play observations and difficulties in screening for mental health disorders over telehealth calls.

Despite increased use of telemedicine, a developmental-behavioral study of preschoolers found that most medication initiations and changes still took place in the in-person setting (23). These findings suggest ongoing telehealth should continue to remain an option, but that a hybrid model is the best compromise between convenience and comprehensive care.

The COVID-19 pandemic forced a dramatic shift toward telehealth models. Both providers and families found satisfaction and even benefit from telehealth appointments, however, in-person visits are still important for medication changes, severe behavioral concerns, families with technology limitations, and to verify certain therapeutic modalities.

With the drop in in-person pediatric visits during the early days of the pandemic, opportunities were missed for timely developmental screenings. It is accepted that for some children, autism can be reliably diagnosed by experienced clinicians by 14 months of age or earlier, and that children under 5 years old show tremendous benefit from earlier intervention (24). The early US data on autism identification during the pandemic highlights a multi-tiered challenge: decreased referral rates, increased wait times for evaluation and decreased number of Furthermore, virtual validated tools could potentially be used to identify high-risk children for EI, enabling them to begin services in a timelier manner. Limited data currently exist to support this approach. However, if data from the pandemic can demonstrate strong psychometric properties and these methods are accepted by insurers, the COVID-19 pandemic may serve as a catalyst to utilize alternate virtual assessment tools, such as the SORF (Systematic There has been limited access to evaluations and EI in some parts of the country. This created opportunities for utilizing innovative multi-tiered screeners for earlier autism identification and developing new virtual assessment tools that will hopefully improve patient outcomes and lessen health disparities. When the pandemic struck, delivery of many vital therapy services came to an immediate halt and families lost their support networks. Concurrently, therapists faced unprecedented practice regulations, restrictions and closures (36), and one survey of ABA therapists reported decreased productivity and job insecurity (37) . Restructuring efforts to provide virtual services were deployed. Providing therapies via telehealth is not a new concept, as the World Federation J o u r n a l P r e -p r o o f of Occupational Therapists and Confederation for Physical Therapy has encouraged their providers for many years to offer telehealth programs (38, 39) . During the pandemic's peak, therapy providers implemented nuanced decision-making models that considered the risks and benefits of restarting in-person therapies versus transitioning to teletherapies (40) . During this time of mass transition, many challenges with the virtual modality of therapy delivery arose including internet connection issues, web literacy gaps, and difficulties following therapists' instructions remotely (41). In one study from the SPARK/Simmons Foundation community dataset of over 97,000 autistic individuals, the benefits of teletherapy were perceived to be low and impacted by the lack of interactive play, peer-to-peer interactions, and reinforcers which are hard to deliver remotely (42) . For many families, there was appropriate fear that the disruption in services would lead to a regression in skills and ultimately impact prognosis.

Despite these challenges, the rise of teletherapies in many settings is exciting given its potential to make therapies more accessible by decreasing time and costs related to travel. In one intervention model, in which virtual parental support and rehabilitation was provided, parents reported increased child growth and development, and increased feelings of self-relevance, engagement, perceived support and recognition (43). Helpful parenting tips have emerged, including scheduling regular online consultations with therapy providers, maintaining online therapy, creating structured daily schedules and reinforcement systems, and scheduling daily child-appropriate activities (43).

As service providers explored optimal best practices when offering telehealth options, several virtual tools emerged. The acronym "VIRTUAL" was developed to highlight important domains needed to deliver effective teletherapy: Visual, Information, Relationships, Technology, Unique, Access and Legal (44) . Innovative parent coaching programs that include counseling J o u r n a l P r e -p r o o f and support have also emerged. One program focused on teaching parents to implement simple token reward systems that were positively reinforcing for all (45) . Within CBT models, therapists adopted creative solutions to several challenges posed by the virtual session format, including expanding their virtual rapport-building activities, implementing virtual visual aids/handouts and navigating distractions (46) . Noted advantages to virtual CBT sessions included some children engaging more from the comfort of their home, sharing aspects of their physical environment, and more flexibility in scheduling sessions (46) . The COVID-19 pandemic prompted both families and service providers to become creative in the ways autistic children receive services when in-person options are not possible.

pandemic, leaving families isolated and fearful. Virtual therapies were implemented but not all patients were able to participate. Though virtual programs were expanded, special consideration was made to continue 1:1 therapies for some autistic children where virtual therapies were unrealistic. The COVID-19 crisis opened the door for opportunities to increase accessibility to services through virtual options that can be utilized even beyond the pandemic.

To reduce the spread of COVID-19, schools closed globally in early 2020. Every US state closed its schools in mid-March 2020 and a US study found significant decreases in incidence of and mortality from COVID-19 in states where in-person schools remained closed (47) . Stay-at-home orders, which included school and non-essential business closures, were J o u r n a l P r e -p r o o f associated with decreased incidence of COVID-19 infections (48) . However, a study of schools that resumed in-person classes in Fall 2020 found that the vast majority of students and staff members who contracted COVID-19 during the school year acquired their infections from exposures outside of school (49) . This suggests that interventions that fall short of school closures, such as canceling large gatherings, physical distancing, and masking, may have more effectively prevented COVID-19 spread than school closures. While school closure focused on preventing deaths and avoiding overwhelming hospitals due to COVID-19 cases, models have demonstrated that the mass school closures will lead to higher years of life lost due to (56), and more isolation and decreased physical activity (57). Contrasted with these findings, some children benefited from the distance learning environment, became more relaxed while learning at home, developed independence, and built better relationships with their parents (58, 59, 60) . Though some parents reported preference for virtual learning, this type of education likely failed to meet children's socialization needs. Clinical experience found that in some cases, distance learning was so preferred that there was real fear and anxiety about returning to in-person learning. However, the options for homecharter schools and medical home programs would not adequately support the needs of children with higher support needs as neither program typically offers sufficient special education support.

These findings prompt many questions regarding the future of education for autistic children. If some parents have preference for and data support that students fare better with distance learning during the pandemic, is IDEA obligated to continue facilitating this option?

What emerging lessons can be harnessed to provide the best education to autistic children? How will the education system catch up on the backlogs of IEPs? How will students be provided the opportunity to make up for what they lost, especially those in special education and those attending underserved schools? While early studies are only beginning to highlight the educational impact of COVID-19 on students, time and future studies are needed to fully grasp the impact of the pandemic on education, especially the education of autistic children. 

Autistic children are at greater risk to psychological challenges during the COVID-19 pandemic than their neurotypical peers due to the nature of autism which demands consistency, and is highly associated with comorbid anxiety, depression, and ADHD. One study found increased aggression, behavioral outbursts, and regression more in the autistic population than in other children with neurodevelopmental considerations during the restrictions (55). Anxiety and depression were highest among those with pre-pandemic psychiatric conditions, those who were younger, and those with fewer emotional contacts (55, 61). These effects were worse earlier in the pandemic and compounded by limited access to educational services (53,55). When compared to neurotypical groups, there was a clear pattern that disrupted schedules and services were more problematic for autistic children compared to neurotypical subjects (61) . However, there were benefits found in some studies, where autistic adults reported enjoying isolation with reduced sensory and social overload (61) .

Examining the utilization of the mental health emergency care system during the pandemic demonstrated an increase in mental health acuity, including increased suicide attempts J o u r n a l P r e -p r o o f (62, 63) . Immediately after stay-at-home orders were enacted, the number of pediatric emergency department (ED) visits dropped, but over the next several months, while ED visits remained low, the proportion of ED visits for mental health crises increased dramatically, most notably in patients over 12 years old (63, 64) . Patients with mental health conditions presented more severely during the COVID-19 pandemic and more frequently required admission to the hospital (65) . Unfortunately, in clinical experience, children were boarded in the ED for hours to days as inpatient psychiatric facilities were overwhelmed with patients due to the rise in acute mental health needs from COVID-19 (66) .

With the reality of increased mental health needs during the pandemic, it is important to understand factors that aid in resilience. Having strong family function pre-pandemic and contact with the school system even indirectly were found to be protective (55, 67). In autistic adults' telehealth check-ins, telehealth with a therapist, journaling, maintaining a schedule, walking/exercise and keeping in touch with family via phone/chat were critically important in coping during times of physical distancing (68) . Families reported that social stories, providing breaks, telehealth, hobbies, cooking, and virtual connections were helpful as well. These findings underscore the importance of targeting emotional regulation, continued services, social connection, and creating routine amongst the chaos. Understanding factors that support resilience are critical in offering tools moving forward. 

The COVID-19 pandemic presented many challenges to the families of autistic children.

Schools are an important influence in children's lives as many autistic children receive services in the school setting, thrive in a structured and organized classroom and benefit from the opportunities in school to socialize with peers (69, 70). The loss of in-person education significantly disrupted the lives of autistic children, and in many cases placed more pressure and stress on families to make up for these losses. More time spent in restricted spaces at home with fewer resources, such as being limited to the same toys, can exacerbate children's restricted interests, thus worsening autism symptoms and challenging family dynamics. Parents had difficulties setting limits on play and screen time, leading to more conflict in parent-child relationships (71). Parents of autistic children are already at heightened risk for mental health problems such as stress, depression, and anxiety which was likely exacerbated during the pandemic, due to decreased access to respite care and increased demands in the home environment (72) . Emerging data during the pandemic found that children were at increased risk for abuse in the home in the setting of parental job loss (73) . The mental health of parents and children were linked during COVID-19, so when parents struggled, children were more likely to struggle, and vice versa (74) .

Despite these challenges, some families saw benefits in certain domains for their children that improved family dynamics. For example, some children experienced less stress due to the J o u r n a l P r e -p r o o f decreased social demands and decreased academic pressures of distance learning (60, 75) .

However, this was less likely to be the case for families in which their child had behavioral or learning difficulties. Half of the parents in one small study reported their children being happier and calmer during quarantine (76) . Not having to endure battles over homework completion, for instance, during the first six months of homeschooling, reduced parent and child stress levels and conflict. During the pandemic and the period of remote learning, children were allowed to honor their rhythms of sleep/wake cycles, eating, and physical activity in a way that was more individually beneficial rather than having to meet the needs of an entire student body, which could reduce overall stress load in the home.

children during the pandemic. Families that were able to implement routines in the home environment, adequately limit children's exposure to screens or restricted interests, to continue to expose their children to social environments, and reduced challenges that children face in the in-person school environment, such as teasing, bullying, and academic stressors, may have created an optimal home life for autistic children.

It is important to consider how the disparities that many autistic children experience may have exacerbated the negative impacts the pandemic had on them. Prior to the COVID-19 crisis, families of autistic children and children with developmental disabilities were at higher risk for food insecurity (77) . One study reported worsening of behaviors during the pandemic in autistic children from lower income families and families who were food insecure (78) . During the J o u r n a l P r e -p r o o f pandemic, minority populations were found to have increased rates of food insecurity compared to non-minorities (79, 80) . Consideration of these multiple factors is important as the pandemic likely created a situation of potentially compounding effects and multiple vulnerabilities for autistic children and their families.

The educational crisis during the COVID-19 pandemic exacerbated already present disparities in learning opportunities for children. Less participation in virtual learning activities was found in students in poverty (81) and students in rural communities (82) . Families with monetary means were able to provide innovative solutions to educate their children during times of school closures, such as paying out of pocket for educated adults to lead "pods" of students in a neighborhood (83) . Meanwhile a digital divide and worsening achievement gaps became apparent for students from low income families who experienced limited access to digital equipment and internet (84) . The implications of these findings for autistic children must be considered, especially given the additional challenges they faced with distance learning as mentioned previously.

These considerations are important due to the strong relationship between autism diagnosis and a higher number of Adverse Childhood Events (ACEs) (85). ACEs are a set of ten potentially traumatic events occurring in childhood that have been linked to health problems in adulthood (86) . This is likely due to the families of autistic children being particularly vulnerable to financial difficulties, parental divorce/separation and household mental illness/substance abuse. In addition to delayed diagnosis, the average age of entry into autism services was delayed in patients with higher ACE scores (87) . Given these baseline statistics, the COVID-19 pandemic has likely compounded these disparities further and has placed autistic children at higher risk for negative outcomes, though no studies on this have been published at this time. Advocacy for children and challenging of potentially unethical policies will be needed to lessen disparities and provide care with equity.

During the pandemic, several online services were augmented or created to provide information about autism and tips for care. Many intervention programs were adapted and are now available as caregiver-delivered programs, increasing caregivers' abilities to support their children over the long-term. Webinars and resources were created to help parents encourage prosocial behaviors at home, including Baby Navigator, Autism Speaks, Triad Family First and J o u r n a l P r e -p r o o f Help is in Your Hands (Fig. 2) . These services will hopefully outlive COVID-19 pandemic as useful educational tools for parents and a bridge to services.

When autistic children and their families are exposed to unforeseen circumstances, such as the COVID-19 pandemic, pediatricians can help in many ways as a primary point of contact for these families during difficult times. Below is the Pediatrician's Toolbox for care of the autistic child based on the early findings and needs that have come to light during the COVID-19 crisis. Through all the darkness of this pandemic there is hope and possibility for improvement in care for autistic patients. •Consider in-person appointments for autistic children who do not tolerate telemedicine appointments •Encourage vaccinations and routine screenings •Train staff members explicitly to work with autistic patients •Screen autistic patients for mental health disorders, especially anxiety due to return to in-person school

•Help families advocate for their autistic child's educational rights protected by IDEA and FAPE •Encourage families to maintain contact with teachers and school leadership during prolonged times at home

•During crisis situations, make continued screening for developmental delay a priority •Plug at-risk patients into services early to frontload therapies •Utilize robust interventions through established therapies or innovative online programs developed during times of crisis •Use Parent Training programs to help parents supplement services during times of service shortage 1

•Refer families to online tools for resources and support 2,3,4,5 •Screen families for ACEs and food and housing insecurities •Encourage families to make and maintain schedules and contact with therapists and other service providers during prolonged times at home •Inquire about parents' psychological well-being in light of increased stressors

The Pediatrician's Toolbox 

COVID-19 outcomes among people with intellectual and developmental disability living in residential group homes in New York State

Children with autism spectrum disorder at a pediatric hospital: a systematic review of the literature

Decreasing the use of restraints on children admitted for behavioral health conditions

The needs of people with intellectual disabilities and autism during the pandemic: Making the invisible visible

Simulation-based education for staff managing aggression and externalizing behaviors in children with autism spectrum disorder in the hospital setting: Pilot and feasibility study protocol for a cluster randomized controlled trial

Stepping out of isolation: Autistic people and COVID-19

Disability, disablism, and COVID-19 pandemic triage

New obstacles and widening gaps: A qualitative study of the effects of the COVID-19 pandemic on U.S. adults with disabilities

Vaccination patterns in children after autism spectrum disorder diagnosis and in their younger siblings

Beliefs about causes of autism and vaccine hesitancy among parents of children with autism spectrum disorder

Understanding vaccine hesitancy among parents 36

Einfluss der COVID-19 Pandemie auf die ambulante physiotherapie

Impact of COVID-19 on the applied behavior analysis workforce: Comparison across remote and nonremote workers

The process for the formulation of the international telehealth position statement for occupational therapy

Report of the WCPT/INPTRA Digital Physical Therapy Practice Task Force

A model of support for families of children with autism living in the COVID-19 lockdown: Lessons from Italy

Pediatric teleheath: Opportunities created by the COVID-19 and suggestions to sustain its use to support families of children with disabilities

Families with children with neurodevelopmental disorders during COVID-19: A scoping review

Italian parents welcomed a telehealth familycentered rehabilitation programme for children with disability during COVID-19

An essential service decision model for ABA providers during crisis

The role of compassion and ethics in decision making regarding access to applied behavior analysis services during the COVID-19 crisis: A response to Cox, Plavnick, and Brodhead

Conducting CBT for anxiety in children with autism spectrum disorder during COVID-19 pandemic

Association between statewide school closure and COVID-19 incidence and mortality in the US

Comparison of estimated rates of coronavirus disease 2019 (COVID-19) in border counties in Iowa without a stay-at-home order and border counties in Illinois with a stay-at-home order

Incidence and secondary transmission of SARS-COV-2 infections in schools

Estimation of US children's educational attainment and years of life lost associated with primary school closures during the coronavirus disease 2019 pandemic

Association of the timing of school closings and behavioral changes with the evolution of the coronavirus disease 2019 pandemic in the US

Office for Civil Rights & Office of Special Education and Rehabilitative Services, pandemic -COVID experiences survey

What the COVID-19 school closure left in its wake: Evidence from a regression discontinuity analysis in Japan

Reflections on children with developmental and behavioral challenges who are thriving while sheltering in place

Parental views of families of children with autism spectrum disorder and developmental disorders during the COVID-19 pandemic

How have youth with Autism Spectrum Disorder managed quarantine derived from COVID-19 pandemic? An approach to families perspectives

The psychological impact of the COVID-19 pandemic on adults with autism: A survey study across three countries

Suicide ideation and attempts in a pediatric emergency department before and during COVID-19

Mental healthrelated emergency department visits among children aged <18 years during the COVID--United States

Reasons for admissions to US children's hospitals during the COVID-19 pandemic

US pediatric emergency department visits for mental health conditions during the COVID-19 pandemic

Supporting youth mental health during the COVID-19 pandemic

Change in youth mental health during the COVID-19 pandemic in a majority Hispanic/Latinx US Sample

Coping, fostering resilience, and driving care innovation for autistic people and their families during the COVID-19 pandemic and beyond

Participation in social activities among adolescents with an autism spectrum disorder

Aggression in autism spectrum disorder: Presentation and treatment options

Parents of children with ASD experience more psychological distress, parenting stress, and attachment-related anxiety

Child maltreatment during the COVID-19 pandemic: Consequences of parental job loss on psychological and physical abuse towards children

Be my safe haven: Parent-child relationships and emotional health during COVID-19

The efficacy of WeChat-based parenting training on the psychological well-being of mothers with children with autism during the COVID-19 pandemic: Quasi-experimental study

Autism spectrum disorder symptoms and bullying victimization among children with autism in the United States

Food insecurity in the households of children with autism spectrum disorders and intellectual disabilities in the United

States: Analysis of the National Survey of Children's Health Data

COVID-19 and behaviors in children with autism spectrum disorder: Disparities by income and food security status

Assessing food insecurity among US adults during the COVID-19 pandemic

Food Insecurity in a Low-Income, Predominantly African American Cohort Following the COVID-19 Pandemic

Remote learning in school bands during the COVID-19 shutdown

Impact of coronavirus pandemic on education

We're all teachers now: Remote learning during COVID-19

Why lockdown and distance learning during the COVID-19 pandemic are likely to increase the social class achievement gap

The relationship between adverse childhood events, resiliency and health among children with autism

Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study

Delayed diagnosis and treatment among children with autism who experience adversity