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      The Implications of the COVID-19 Pandemic for Pediatric Primary Care Practice in Europe

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      , MD 1 , , MD 1 , , MD, PhD 2 , , , MD 1
      The Journal of Pediatrics
      Elsevier Inc.

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          Abstract

          The COVID-19 pandemic has taken a heavy toll on the adult population 1 . In the US, out of 1.4 million diagnosed with COVID-19, 154 children have died 2 . In a large cohort study of 135,794 children tested for COVID-19, the infection rate was low (4%), many positive children remained asymptomatic, and if signs of illness were present, disease symptoms were typically mild. The case fatality rate in this group was 0.2% 3 . In Europe, early studies showed a low fatality rate (0.69%) in children who tested positive for COVID-19, and 4% developed severe illness 4 . Low mortality and morbidity rates due to COVID-19 in European children during the pandemic were confirmed by the statistical office of the European Union 5 . However, despite the available evidence suggesting that the direct impact of COVID-19 on child and adolescent mortality and morbidity is somehow limited, child services suffered important indirect effects, mainly due to discontinuities shown throughout Europe by many local health systems strained by the pandemic 6 . The disruptions to care-seeking and preventive interventions in the majority of European countries, including checks for healthy children, vaccination plans, and mental disorders programs were extensive and concerned the European pediatric societies 7 . The aim of this commentary, jointly authored by the by the European Confederation of Primary Care Pediatricians (ECPCP) and EPA-UNEPSA, is to raise awareness of the indirect consequences caused by the pandemic on pediatric primary care practice in Europe and the risks for child health and wellbeing. Indirect impact of COVID 19 on pediatric primary care practice in Europe European countries have seen a two-wave pattern in reported cases of coronavirus disease-19 in 2020, with a first wave during the months of March-July, followed by a second wave in late summer and autumn of the same year. The first wave caused a pronounced indirect impact on health services for children and changes in the daily practice of pediatric primary care. Considerable disruption of essential health services took place in many countries7,8,9. The measures taken by governments to contain the crisis often raised criticism from the European pediatrics societies, due to their frequent changes and the overall negative impact largely observed on children’s physical and mental health, and on their education10,11,12. In summer 2020, ECPCP performed a study involving the majority of its member societies. Data from primary care pediatricians working in 17 European countries during the first wave of the COVID-19 pandemic were collected by a questionnaire, with the aim to obtain information about the consequences of the pandemic on pediatric primary care practice in different local realities and their risk for child health 13 , 14 . The study showed that significant adjustments in daily pediatric practice took place during the generalized lockdown accompanying the first pandemic wave of COVID-19. Several changes in routine clinical practice were made by pediatricians in order to minimize the transmission of COVID-19 from patient to patient and among the staff working in the office settings. At the beginning of the pandemic a serious shortage of protective equipment endangered health workers worldwide 15 , particularly in ambulatory settings 16 , 17 . However, 95% of European primary care pediatricians reported a systematic use of personal protective clothing and face masks within a short time from the onset of the pandemic, and their commitment (92%) to maintain this practice beyond its end 13 . With the intent to compensate for potentially infectious encounters, in-person visits were significantly reduced and replaced with phone and, to a lesser extent, video consultations. 55% of primary care pediatricians reported that during Summer 2020 of the COVID-19 pandemic, in-person consultations dropped from 40% to over 80%. However, an effort was made to continue offering the option of pediatrician–patient encounters by applying the “ECPCP empty waiting-room policy,” characterized by well-planned schedules of appointments, which helped minimize the waiting time and discouraged unscheduled walk-in-visits 13 . In most European countries, primary care pediatricians followed the directions recommended by local public health departments and WHO health officials and limited the number of accompanying persons during visits in private setting such that children could only be accompanied by one caretaker 18 , 19 . As a result, crowding of patients in waiting rooms was significantly prevented 13 . Providing separate rooms and separate consulting hours for infectious and non-infectious patients was used as an additional important safety measure, although it was not possible in all circumstances. However, the changes applied to routine practice due to the pandemic and fearful attitudes by parents caused unintended and sometimes negative consequences 13 . As reported by 40% of pediatricians participating in the ECPCP study, at the beginning of the epidemic a considerable number of patients with minor illnesses were discouraged to come to doctor’s offices, which had the unintended effect that serious conditions were sometimes recognized late, thereby increasing the risks for complications 13 . A large number of pediatricians involved in the study (86%) reported that due to the restricted access to emergency services, in many cases, the families of their patients admitted to have failed or delayed to report to the local health authorities, serious health conditions or life-threatening diseases different from COVID 19 involving their children. The health conditions which were most often unreported included diabetic ketoacidosis, hematology and oncology diseases, appendicitis, peritonitis, child abuse, severe bacterial infections such as urinary tract infection, meningitis, pneumonia and acute cardiac problems 13 . Similar data were reported in the US 20 and Israel 21 . A study involving 53 Italian diabetes centers revealed that COVID-19 has significantly worsened the presentation of type 1 diabetes in children 8 . Decline in vaccinations during COVID 19 Since the summer of 2020 the World Health Organization and UNICEF warned of an alarming decline in the number of children receiving life-saving vaccines around the world 22 . According to data collected in collaboration with the US Centers for Disease Control, the Sabin Vaccine Institute, and Johns Hopkins Bloomberg School of Public Health, three quarters of 82 countries involved in a preliminary study, reported a significant COVID-19 related disruptions in their immunization programs by May 2020 22 . Similar alarming data were recorded by the ECPCP study, as primary care pediatricians reported a decrease in vaccination coverage in the various European countries, which ranged from 11% to over 50%, in children under and over 2 years of age. A main obstacle reported by the European pediatricians in the implementation of vaccination programs, was the fear of families to leave home during lockdown and the hesitation to vaccinate their children at all during corona times 22 , 23 . Negative impact of COVID 19 lockdown on children’s social interactions and well-being Social distancing during COVID-19 has caused a drastic upheaval to the way people work and socialize. Many children have been uprooted from their places of education and care, and it may be difficult for them to understand why their routine has been disrupted. Not much is known about the long-term mental health effects of large-scale disease outbreaks on children and adolescents 24 . However, monitoring young people's mental health status over the long term, and studying how prolonged school closures, strict social distancing measures, and the changes in life-styles caused by the pandemic affect the wellbeing of children and adolescents would be greatly useful 24 . Although during school closure parents had the chance to dedicate more valuable time to their children, in many cases COVID-19 has contributed to increased external stressors and lowered the quality of social relationships and family cohesion 25 . In families that spend longer periods of time together, COVID-19 may exacerbate pre-existing vulnerabilities including depression and anxiety, which can harm the stability of relationships and increase the risks of abuse and violence 25 , 26 . The European societies of primary care pediatrics have advised the EU public health authorities about these risks and stressed the importance of a coordinated approach by pediatricians and mental health service providers to properly manage the whole range of conditions affecting the mental wellbeing of children caused by the pandemic 9 . The lockdown due to COVID 19 has also caused socio-economic inequalities to raise, including worsened educational performances of children from poor socio-economic backgrounds, who could not be adequately supported by their parents during home schooling (Figure ; available at www.jpeds.com). In Europe, 76% of ECPCP members interviewed endorsed the statement that children should go back to school to further their social development, as the benefits may outweigh the risks, if all official public health requirements are observed and under the condition that adequate personal protection for the school staff could be guaranteed. Figure 1 Conclusions Coordinated efforts among healthcare professionals 27 will allow maintaining the best provision of child health care both for sick and healthy children during the future course of the pandemic. To maintain a high quality level of pediatric primary care practice in Europe, legislators, health authorities and professional pediatric societies should collaborate closely 28 . In view of the challenges posed by the pandemic, the data provided by ECPCP suggest that it will be essential to implement a strategy aiming at preserving the continuity of preventive services and vaccination programs and focusing on the free fearless access of all children to health services. Uncited reference 10), 11), 12).

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          Behavioral and Emotional Disorders in Children during the COVID-19 Epidemic

          Since December 2019, health systems around the globe have struggled with an increasing number of cases of a viral respiratory syndrome that emerged in China. The cause is a new strain in the coronavirus family, provisionally named 2019 novel coronavirus (2019-nCoV) 1 , SARS-CoV-2 or COVID-19. 2 The European Paediatric Association–Union of National European Paediatric Societies and Associations (EPA-UNEPSA) has established a collaborative working group with key Chinese academic institutions and medical centers with the purpose of facilitating the reciprocal exchange of information and sharing scientific knowledge. The aim of this commentary by the China-EPA-UNEPSA working group is to raise awareness regarding children's psychological needs during epidemics and report early data collected in the COVID-19–affected areas in China during the current outbreak, emphasizing the role of families and caregivers in the timely recognition and management of negative emotions. Epidemiology of COVID-19 The COVID-19 outbreak first erupted in the city of Wuhan in the Hubei Province of China, where several local health facilities reported clusters of patients with pneumonia of unknown cause; they were epidemiologically linked to a seafood and wet animal wholesale market. 3 COVID-19 infection rapidly spread throughout China, involving the provinces of Chongqing, Hunan, Anhui, Henan, Jiangxi, and Shaanxi. 4 Over the next 3 months, COVID-19 spread to other regions of the world, reaching >100 000 cases globally in the first week of March 2020, of which approximately 80% were reported in China, 6% in South Korea, 3% in Iran, and 0.2% in the US. In Europe, the first case of COVID-19 was registered in a patient hospitalized in Munich, Germany in early January 2020, following contact with a traveler from China. 5 Later, several other cases were reported in variable numbers in Germany, Spain, Italy, France, and other European countries, together representing roughly 5% of the cases of COVID-19 recorded worldwide. 4 Genetic studies on viral strains isolated from patients affected by Coronavirus infection throughout the world confirmed that they are all phylogenetically related to the original Chinese mutant strain. 6 In contrast to seasonal influenza, COVID-19 seems to cause a milder clinical infection in children than in adults or older people. Early studies have suggested that children are just as likely as older age groups to become infected with the coronavirus but are far less likely to develop severe symptoms. 7 The risk of severe disease and death is highest for seniors and those with severe health conditions, such as heart disease, chronic lung disease, cancer, and diabetes. 7 COVID-19 has been perceived worldwide as a major threat to health and a danger to the global economy, affecting people's lives by influencing their everyday behavior and causing feelings of panic anxiety, depression, and often triggering intense dread. In China, COVID-19 has affected children aged 3 months to 17 years, most of whom had close contact with infected persons or were part of a family cluster of cases. 8 No official data are available on the number of symptomatic and asymptomatic individuals positive for COVID-19 in the <18 age group. Infected children might appear asymptomatic 9 or present with fever, dry cough, and fatigue, and few have upper respiratory symptoms including nasal congestion and running nose. Some patients present with gastrointestinal symptoms, including abdominal discomfort, nausea, vomiting, abdominal pain, and diarrhea. Most infected children have mild clinical manifestations without fever or symptoms of pneumonia, and the majority recover within 1-2 weeks after disease onset. Few progress to lower respiratory infections. Although children seem to be less vulnerable than adults to COVID-19, initial reports from Chinese areas hit by the outbreak indicate that children and adolescents have been impacted psychologically, manifesting behavioral problems, as discussed below. 10 Early Investigation of Chinese Children's Behavioral and Emotional Reactions to COVID-19 Children are not indifferent to the dramatic impact of the COVID-19 epidemic. They experience fears, uncertainties, and physical and social isolation and may miss school for a prolonged period. Understanding their reactions and emotions is essential to properly address their needs. A preliminary study conducted in Shaanxi Province during the second week of February 2020, which was authorized by the local authorities, showed that the most common psychological and behavioral problems among 320 children and adolescents (168 girls and 142 boys) aged 3-18 were clinginess, distraction, irritability, and fear of asking questions about the epidemic (unpublished data). Because of the Chinese government's mobility restrictions related to epidemics, as enforced by local and national authorities, the study was performed using an online questionnaire to investigate the children's behavioral and emotional responses to the current epidemics. Several children were confined at home under protective isolation because they resided in highly affected areas. The questionnaire, which was completed by the parents, incorporated the Diagnostic and Statistical Manual of Mental Disorders (DSM-5) criteria 10 commonly used for a cross-cultural assessment of anxiety disorders, including depression. 11 Fear of asking about the epidemics and the health of relatives, poor sleep including nightmares, poor appetite, physical discomfort, agitation and inattention, clinginess, and separation problems were among the main psychological conditions investigated. An important factor ensuring the reliability of results collected by questionnaires investigating mental disorders in general and particularly during emergencies is the procedure for data collection and statistical analysis followed by specialized personnel responsible for data collection, registration, and statistical processing, as in this case. The use of standard statistical methods ensures the comparability of the results with other studies. 12 , 13 The purpose of the questionnaire used in the Chinese study was not to establish a final diagnosis of mental disorder and depression or to monitor depression severity, but rather to screen for behavioral and emotional disorders as a “first step” approach. Subjects who screened positive at preliminary investigation of their behavioral and emotional condition should be included in future programs to determine whether they meet criteria for a depressive disorder. Psychological distress in Children Exposed to Adverse Events Although the knowledge base regarding children's responses to trauma and adverse events in general has been expanding, descriptions of their responses during epidemics remain scarce. 14 Yet their vulnerability makes this an important group to study. Several studies have documented the damaging effects of psychological stress due to negative events in children. Anxiety, depression, lethargy, impaired social interaction, and reduced appetite are commonly reported manifestations. Physiological effects include a weakened or compromised immune system.15, 16, 17, 18, 19 In the course of adverse events, children are often forced to stay home for long periods due to enforced isolation and school closure, resulting in limited connection with classmates and reduced physical activity. A preliminary study conducted in the Shaanxi province during the COVID-19 epidemic by the China-EPA-UNEPSA collaborative working group showed that children in the younger age group (3-6 years) were more likely than older children to manifest symptoms, such as clinginess and fear that family members could contract the infection (P = .002). Children aged 6 to 18 years were more likely to show inattention (P = .049) and persistent inquiry (P = .003). Clinging, inattention, and irritability were the most severe psychological conditions demonstrated by the children in all age groups (Figure; available at www.jpeds.com). The rates of fear, anxiety, and other emotions were higher in children residing in highly epidemic areas; however, the differences between areas identified by different levels of epidemic risk were not statistically significant. Media entertainment was largely successfully used by families over reading and physical exercise as a means to relieve their children's distress and address their concerns regarding the negative condition they were experiencing (Table; available at www.jpeds.com). The Importance of Nurturing Resilience in Children Exposed to Epidemics Children facing unexpected and unknown events typically exhibit various stress reactions, as confirmed in the study performed in China during the COVID-19 epidemic. Resilience, the personal attributes that help children manage everything from little disappointments to big life traumas, should be nurtured and implemented by public health programs in children and teens living in areas hit by calamities such as epidemics. If properly supported by healthcare professionals, families, and other social connections, including school environment, children and adolescents can appropriately overcome a condition of distress and prospectively stabilize emotionally and physiologically. 20 Conclusions Pediatricians working in Shaanxi Province, China have pursued the strategy of nurturing resilience in children and adolescents hit by the psychological consequences of the COVID-19 epidemic. The measures suggested by Chinese pediatricians to parents and family members, included increasing communication with children to address their fears and concerns, playing collaborative games to alleviate loneliness, encouraging activities that promote physical activity, and using music therapy in the form of singing to reduce the worry, fear, and stress that the child may feel. All these measures are focused on supporting the child to get through this difficult time. Furthermore, parents should pay attention to sleep difficulties and nightmares, prevent increased daytime sleep and suggest sleep hygiene and relaxation methods, model a positive psychological attitude to reduce stress, and divert attention to more productive and positive directions. The effect of this outbreak is unclear at present, as the situation is rapidly evolving. 21 The China-EPA-UNEPSA working group believes that the preliminary report from the Chinese province of Shaanxi includes useful information for professionals involved in the care of children hit by the current and possible future epidemics. 22
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            Delayed presentation and sub-optimal outcomes of pediatric patients with acute appendicitis during the COVID-19 pandemic

            Objective Early presentation and prompt diagnosis of acute appendicitis are necessary to prevent progression of disease leading to complicated appendicitis. We hypothesize that patients had a delayed presentation of acute appendicitis during the COVID-19 pandemic, which affected severity of disease on presentation and outcomes. Patients and methods We conducted a retrospective review of all patients who were treated for acute appendicitis at Morgan Stanley Children's Hospital (MSCH) between March 1, 2020 and May 31, 2020 when the COVID-19 pandemic was at its peak in New York City (NYC). For comparison, we reviewed patients treated from March 1, 2019 to May 31, 2019, prior to the pandemic. Demographics and baseline patient characteristics were analyzed for potential confounding variables. Outcomes were collected and grouped into those quantifying severity of illness on presentation to our ED, type of treatment, and associated post-treatment outcomes. Fisher's Exact Test and Kruskal-Wallis Test were used for univariate analysis while cox regression with calculation of hazard ratios was used for multivariate analysis. Results A total of 89 patients were included in this study, 41 patients were treated for appendicitis from March 1 to May 31 of 2019 (non-pandemic) and 48 were treated during the same time period in 2020 (pandemic). Duration of symptoms prior to presentation to the ED was significantly longer in patients treated in 2020, with a median of 2 days compared to 1 day (p = 0.003). Additionally, these patients were more likely to present with reported fever (52.1% vs 24.4%, p = 0.009) and had a higher heart rate on presentation with a median of 101 beats per minute (bpm) compared to 91 bpm (p = 0.040). Findings of complicated appendicitis on radiographic imaging including suspicion of perforation (41.7% vs 9.8%, p < 0.001) and intra-abdominal abscess (27.1% vs 7.3%, p = 0.025) were higher in patients presenting in 2020. Patients treated during the pandemic had higher rates of non-operative treatment (25.0% vs 7.3%, p = 0.044) requiring increased antibiotic use and image-guided percutaneous drain placement. They also had longer hospital length of stay by a median of 1 day (p = 0.001) and longer duration until symptom resolution by a median of 1 day (p = 0.004). Type of treatment was not a predictor of LOS (HR = 0.565, 95% CI = 0.357–0.894, p = 0.015) or duration until symptom resolution (HR = 0.630, 95% CI = 0.405–0.979, p = 0.040). Conclusion Patients treated for acute appendicitis at our children's hospital during the peak of the COVID-19 pandemic presented with more severe disease and experienced suboptimal outcomes compared to those who presented during the same time period in 2019. Level of Evidence III
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              Deaths From COVID-19

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                Author and article information

                Journal
                J Pediatr
                J Pediatr
                The Journal of Pediatrics
                Elsevier Inc.
                0022-3476
                1097-6833
                9 March 2021
                9 March 2021
                Affiliations
                [1 ]European Confederation of Primary Care Paediatricians, Lyon, France
                [2 ]European Paediatric Associations, Union of National European Pediatric Societies and Associations, Berlin, Germany
                Author notes
                []Corresponding Author: Massimo Pettoello-Mantovani, MD, PhD Department of Pediatrics, Scientific Institute “Casa Sollievo della Sofferenza”, University of Foggia, Foggia, Italy, - Phone:+39.0881588099 / FAX: +39.0881.733718
                Article
                S0022-3476(21)00215-8
                10.1016/j.jpeds.2021.03.004
                7939972
                33705763
                fe98109e-fc11-4aa1-9dcc-3a84ad083710
                © 2021 Elsevier Inc. All rights reserved.

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

                History
                : 3 March 2021
                : 3 March 2021
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                Pediatrics
                Pediatrics

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