The impact of the COVID-19 pandemic on children with medical complexity

Background Descriptions of the COVID-19 pandemic’s indirect consequences on children are emerging. We aimed to describe the impacts of the pandemic on children with medical complexity (CMC) and their families. Methods A one-time survey of Canadian paediatricians using the Canadian Paediatric Surveillance Program (CPSP) was conducted in Spring 2021. Results A total of 784 paediatricians responded to the survey, with 70% (n = 540) providing care to CMC. Sixty-seven (12.4%) reported an adverse health outcome due to a COVID-19 pandemic-related disruption in healthcare delivery. Disruption of the supply of medication and equipment was reported by 11.9% of respondents (n = 64). Respondents reported an interruption in family caregiving (47.5%, n = 252) and homecare delivery (40.8%, n = 218). Almost 47% of respondents (n = 253) observed a benefit to CMC due to COVID-19 related changes in healthcare delivery, including increased availability of virtual care and reduction in respiratory illness. Some (14.4%) reported that CMC were excluded from in-person learning when their peers without medical complexity were not. Conclusion Canadian paediatricians reported that CMC experienced adverse health outcomes during the COVID-19 pandemic, including disruptions to family caregiving and community supports. They also describe benefits related to the pandemic including the expansion of virtual care. These results highlight the need for healthcare, community and education policymakers to collaborate with families to optimize their health. Supplementary Information The online version contains supplementary material available at 10.1186/s12887-022-03549-y.


Introduction
During the early part of the pandemic, children, including those with chronic illness, have been less affected by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection than adults, with a small proportion of Open Access *Correspondence: catherine.diskin@sickkids.ca documented coronavirus disease  cases, hospitalizations and deaths affecting children [1][2][3]. The pandemic has resulted in rapid change across many aspects of society, including healthcare and education [1]. Descriptions of the pandemic's indirect consequences on children are emerging, including the impact on children with special health care needs, particularly those with medical complexity [4]. Children with medical complexity (CMC) have special healthcare needs with chronic conditions resulting in caregiver burden, technology dependence, and frequent healthcare interactions across multiple settings, including tertiary and community hospitals, primary care settings, schools, and communities [5]. Family caregivers perform complex medical and therapy-related tasks supporting the delivery of care [6,7]. An example of a CMC is a child with severe neurological impairment secondary to hypoxic-ischaemic encephalopathy who experiences seizures and dystonia and requires an enteral tube to support nutrition following two admissions with aspiration pneumonia. The child receives care at a local hospital and children's development centre and is supported with in-home and in-school nursing.
As a direct consequence of COVID-19 pandemic restrictions, CMC have experienced multiple disruptions in their care [4], including disruption of medical and specialist care, therapy and rehabilitative services, homecare and respite services and education [8]. For example, disruption to school can interrupt the provision of developmental services, out-of-home respite and increase the caregiving demands of parents and caregivers [1]. Further disruption in income, financial supports, transportation and the supply of vital equipment and supplies (e.g. medicines, specialised formulas) provided additional challenges. However, no prior study has examined these effects and adverse outcomes associated with the disruption of services to CMC during the COVID-19 pandemic.
We aimed to describe the indirect impacts of the COVID-19 pandemic on CMC and their families from the perspective of paediatricians. The study focused on (1) medical services, including access to and family experience, (2) community services including home care, respite, and timely access to medication and medical equipment and (3) education, including access to inperson or virtual learning environments, and disruptions to in-school delivery of nursing and therapies.

Methods
We conducted a one-time survey of Canadian paediatricians and subspecialists using the Canadian Paediatric Surveillance Program (CPSP). The CPSP is a joint initiative of the Public Health Agency of Canada (PHAC) and the Canadian Paediatric Society (CPS). The program is responsible for conducting national surveillance into uncommon child and youth health conditions low in frequency but high in associated morbidity and mortality. The program surveys over 2800 paediatricians.

Survey development
The survey was developed collaboratively by the CPSP Scientific Steering Committee, which included clinicians (physicians, nurse practitioners) providing care to CMC across various clinical settings, including academic, community and rural, and the parent of a child with medical complexity.
We asked respondents whether they provided care to CMC as part of their clinical practice; respondents who did completed the survey. The survey collected information on respondent demographics, healthcare delivery, including experiences of adverse health events related to a COVID-19 pandemic-related disruption in routine healthcare delivery, changes in healthcare that benefit CMC, the impact of COVID-19 pandemic on family caregiving, homecare, and supply of medication and equipment. Information about the educational experience of CMC during the pandemic, including virtual learning, school supports, in-school delivery of nursing and therapies, was collected. When respondents reported an indirect impact of the COVID-19 pandemic (e.g., disrupted homecare), they were asked the frequency of outcome or the percentage of CMC and families affected and the frequency of contributing factors. Appendix 1 contains the final copy of the 17-item survey.

Survey distribution
The survey was distributed in English and French in February 2021, with a closing date in April 2021. Two reminders were sent to online respondents who had yet to respond.

Analysis
Microsoft Excel (version 2015) was used to tabulate responses, and statistical analyses were descriptive. There were numerous open-ended questions in the survey. The free text responses were initially categorized descriptively into large categories based on the frequency of responses. Similar responses were collapsed together to facilitate analyses and interpretation. The study was funded through a CPSP in-kind grant. Data elements where the "n" value is less than 5 were reported according to CPSP policy.

Healthcare experience Adverse health outcomes
One in nine respondents (12.4%; n = 67) reported a CMC having an adverse health outcome due to a COVID-19 pandemic-related disruption in healthcare delivery, with responses from all provinces and regions ( Table 2). Respondents reported 546 events of children who experienced an adverse outcome, with a median number of events of 3 (interquartile range [IQR] 1-10) per respondent. The most-reported observed adverse health outcomes are outlined in Table 2. Respondents highlighted delayed presentation to healthcare or deferral of care because of the risk of exposure to SARS-CoV-2 at a tertiary care centre, observed slowing of developmental gains, reduced provision of health surveillance, delays in accessing elective procedures and challenges associated with hospital visitation policies. There were no reported deaths.
Respondents reported that medication, medical equipment and routine vaccination were most frequently impacted. Examples of medications where supplies were interrupted included Clonidine, Fludrocortisone, Salbutamol, Testosterone (injectable), and oral Vitamin K (oral). The supply of specialized enteral feeds was also interrupted along with equipment relating to technology including enteral tubes, tracheostomies and urostomies.
The most frequently cited reasons included medication or supply shortage and delays in dispensing. The impact of difficulties accessing medication or equipment was minor (i.e., short delay, no change in care; n = 27) or moderate (i.e., alternative medication sourced without change in clinical status; n = 26). Seven respondents reported a significant event (i.e., an adverse clinical event), with five reporting that the event resulted in hospitalization. The complications due to the interrupted medication and equipment supply included ill-fitting equipment that required adjustment, including skin breakdown and pain. Other factors impacting medication and equipment supply included the loss of employment of family caregivers, which affected their ability to pay for medication and supplies, challenges with equipment that remained in school, and dispensing practice changed as clinics changed from in-person to virtual.

Family caregiving and homecare delivery
Two-hundred and fifty-two respondents (47.5%) reported that they observed an interruption in family caregiving to CMC during the pandemic, while over 40% of respondents (n = 218) reported that families with CMC experienced disrupted homecare. Of the respondents who reported disruptions to family caregiving and homecare delivery, Table 2 outlines the most frequent reasons.

Benefits in the healthcare experience of CMC as observed by paediatricians
Almost half of the respondents (46.9%; n = 253) reported observing a benefit of COVID-19 related changes in healthcare experienced by CMC. Respondents highlighted the increased availability of virtual care (n = 184), the observed reduction in incidence of respiratory illness among CMC (n = 60) and healthcare system change (n = 12). Table 4 outlines the benefits in the healthcare  When asked about virtual care, respondents highlighted that a virtual visit could not replace all in-person visits -emphasizing the importance of the clinical examination in monitoring disease progression (e.g., scoliosis).
The reasons provided for the observed reduction in CMC experiencing respiratory illness included improved universal infection control precautions, including in healthcare (e.g., reduced numbers in waiting rooms) and their introduction into education settings (e.g., masking), in addition to their siblings not experiencing intercurrent illnesses. Respondents noted that the absence of respiratory illness had promoted CMC's developmental progress.

Educational experience
Of the respondents who could provide details of CMC attending school in 2020 (n = 376), one-quarter (23.6%; n = 89) reported that > 80% of CMC attended in-person school while over one-third (37%; n = 114) reported that < 20% did. Before 2020, 399 paediatricians estimated in-person school attendance, with 75% of respondents estimating that > 80% of CMC in their practice attended in-person school before the pandemic, with few paediatricians (5.5%; n = 22) reporting that less than 20% of CMC attended in-person school. The change in school attendance as observed by participating paediatricians is outlined in Fig. 1.
Seventy-eight respondents (14.4%) reported that CMC were excluded from in-person learning when their peers without medical complexity were not. Two hundred and thirty-two respondents (43%) reported no such experience, and 225 (41.7%) did not know. We invited respondents to share why CMC were excluded from inperson learning. Examples included public health advice that precluded their attendance, including advice regarding aerosol-generating medical procedures (AGMPs) and CMC being resident in a long-term care (LTC) facility, the absence of in-school behaviour support, challenges with transportation, physician recommendation and individual limitations in terms of maintaining physical distancing or mask wearing.
Two-thirds of respondents (66.1%; n = 357) reported that CMC receive healthcare services at school. Very few respondents reported that services transferred from school to home and or community during periods of virtual learning (Table 3).
Respondents described the loss of access to therapy and equipment that typically remains in school as having a deleterious impact on CMC. Respondents also highlighted that many families opted not to send CMC to school during the past year. Others highlighted that learning was impacted by the absence of and challenge of delivering an individualised education plan (IEP) during virtual school.

Regional differences in the indirect impacts of the COVID-19 pandemic
Regional differences in the indirect impacts of the COVID-19 pandemic are outlined in Appendix 2, including the percentages of respondents from each province. There were minimal discernable differences across provinces in responses.

Discussion
A large proportion of Canadian paediatricians reported an indirect impact of the COVID-19 pandemic on their patients with medical complexity. Our national survey identified adverse health outcomes and disruptions to family caregiving, available supports and school attendance. Adverse health impacts resulting in CMC requiring both hospital admissions, including the intensive care unit (ICU) and an extended time in hospital, loss of physical or developmental and unplanned surgery mirrors previously published literature, highlighting disruption caused by the COVID-19 pandemic to safe, timely and effective care [9]. CMC are a vulnerable population and it is important to recognise that they are disproportionately vulnerable to the consequences of the COVID-19 pandemic due to greater healthcare needs, dependency on community-based services and mental health concerns [10]. Respondents highlight this reality for CMC and their families, with over 40% observing a disruption in community services, including homecare services. Clinicians report that homecare is essential to the lives of many CMC and their families [11,12], but limitations regarding its delivery were described before the pandemic [13]. We also describe disruptions in family caregiving, highlighting the emotional and financial stress involved in caregivers of CMC [14]. The impacts of the pandemic as related to family caregiving and community services interact with previously existing challenges, highlighting the vulnerability of this subgroup of children and their families and a pressing need to recognise the stressors CMC and their families are experiencing.
Canadian pediatricians reported major disruption to the educational system during the COVID-19 pandemic, including the well-known reduction in attendance at in-person class [15]. School closures exert a greater influence on vulnerable children, including those with disabilities [16]. Before the pandemic, many families of children with developmental disabilities, would highlight school holidays as times of increased stress [17]. Healthcare providers believe that school is not simply an academic pursuit for many children, including CMC, but a place of therapy, nursing, respite, learning, and socialization. When access to such services are interrupted, it becomes the responsibility of family caregivers to step in. For families of CMC, this can be an additional burden to already overburdened caregivers. As we consider the interplay between education and health sectors, considering the entire experience with an inclusive lens is necessary with collaboration and flexibility between traditional silos so that CMC can receive holistic care.
Almost half of the respondents highlighted some positive changes observed during the pandemic, including the expansion of virtual care and a reduction in children presenting with respiratory illnesses. The accelerated expansion of virtual care during the COVID-19 pandemic is previously described [18]. The experience of respondents who reported a decrease in numbers of CMC presenting with respiratory illness supports empiric evidence [19]. Measures to mitigate the spread of SARS-CoV-2 likely contributed to a decline in other respiratory illnesses, including respiratory syncytial virus (RSV) and influenza [20]. More recently, delayed seasonal surges in RSV have been described in both hemispheres, potentially correlating with the relaxation of some measures [21,22]. The trend in reduced incidence of respiratory infections is particularly important to CMC, considering they experience greater rates of hospitalization and morbidities associated with such infections [23][24][25]. The pandemic highlighted potentially valuable tools to protect the physical health of CMC. Formal evaluation of many interventions, including masking practice, hand washing, smaller class sizes, screening for respiratory symptoms, may have impacted transmission of respiratory illness, would provide an improved understanding of which measures lead to improved health outcomes and support safe and accessible service delivery for CMC and their families.
The observations of participating paediatricians on the experience of CMC and their families are far-reaching, crossing many aspects of CMC care and life. Their oftenisolated experience with a continued need for advocacy was highlighted. For example, the impact of reduced support, such as family caregiving and home care, on families could exacerbate social isolation and loneliness they experienced before the pandemic, for which they receive little support [26]. This study illustrates how the COVID-19 pandemic exacerbated an existing situation for CMC families and providers, who often must navigate silos [26]. Over the past decade, there have been concerted efforts to coordinate CMC's care across these sector silos [27]. A pertinent example is how many CMC receive healthcare, including nursing and various therapies through the education system, and much of the related equipment remains in school. When in-person learning was interrupted, so did their access to healthcare, potentially interrupting their developmental progress. Few respondents reported that school-based resources were transferred elsewhere when schools remained closed. Another important factor that impacted school attendance for some CMC were challenges accessing transport. Many CMC require transportation to and from school, and when unavailable, often cannot attend school.
Our study has several limitations. First, information collected is based on voluntary reporting and is limited by a low response rate (27.7%), incomplete responses and recall bias. The response rate is in line with previous CPSP surveys. Second, respondents provided estimates of the numbers of families and children impacted by various aspects of the pandemic, limiting specific information. As such, we were unable to calculate population-based estimates. Third, we cannot verify that each response is unique, as there may be duplicate entries (e.g. physicians working in the same institution may describe the same event). Fourth, our survey was limited to paediatricians, and CMC receive care from many clinicians, including family physicians, nurse practitioners and therapists who could provide valuable insights. Fifth, paediatricians may often be unaware of all aspects of a child's life, as evidenced by the high number of respondents that did not know the answer to particular questions. Finally, the survey did not include the experience of family caregivers, who are best placed to describe their children's experience during the pandemic. Some indirect impacts on CMC may not have been visible to paediatricians due to the efforts of family caregivers, e.g., stockpiling medications and supplies in case medication or equipment shortages arose.

Conclusion
Consideration of the broad impact on this sub-group of the paediatric population is required to inform pandemic and non-pandemic health policy and planning, including service design and delivery across acute, home and community care sectors, and education policy and service planning for children with CMC.