Abstract

The COVID-19 pandemic has taken a heavy toll on the adult population.1Koh H.K. Geller A.C. VanderWeele T.J. Deaths from COVID-19.JAMA. 2021; 325: 133-134PubMed Google Scholar In the US, out of 1.4 million diagnosed with COVID-19, 154 children have died.2American Academy of PediatricsChildren and COVID-19: state-level data report.https://services.aap.org/en/pages/2019-novel-coronavirus-covid-19-infections/children-and-covid-19-state-level-data-report/Date accessed: December 10, 2020Google Scholar 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%.3Bailey L.C. Razzaghi H. Burrows E.K. Bunnell T. Camacho P.E.F. Christakis D.A. et al.Assessment of 135794 paediatric patients tested for severe acute respiratory syndrome coronavirus 2 across the United States.JAMA Pediatr. 2021; 175: 176-184Crossref PubMed Scopus (118) Google Scholar In Europe, early studies showed a low fatality rate of 0.69% in children who tested positive for COVID-19, and 4% developed severe illness.4Götzinger F. Santiago-García B. Noguera-Julián A. Lanaspa M. Lancella L. Calò Carducci F.I. et al.COVID-19 in children and adolescents in Europe: a multinational, multicentre cohort study.Lancet Child Adolesc Health. 2020; 4: 653-661Abstract Full Text Full Text PDF PubMed Scopus (703) Google Scholar 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.5European Statistical Office (eurostat)COVID-19: statistics serving Europe.https://ec.europa.eu/eurostat/web/covid-19/overviewDate accessed: January 31, 2021Google Scholar 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, owing mainly to discontinuities seen throughout Europe by many local health systems strained by the pandemic.6Bensoussan E. Ouldali N. Ashkenazi S. Angoulvant F. Cohen R. Levy C. Impact of coronavirus disease 2019 (COVID-19) pandemic on pediatric infectious disease research.J Pediatr. 2021; 230: 279-281.e2Abstract Full Text Full Text PDF PubMed Scopus (2) Google Scholar 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.7Somekh I. Somech R. Pettoello-Mantovani M. Somekh E. Changes in routine pediatric practice in light of coronavirus 2019 (COVID-19).J Pediatr. 2020; 224: 190-193Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar The aim of this commentary, jointly authored 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 well-being. European countries have seen a two-wave pattern in reported cases of COVID-19 in 2020, with a first wave during the months of March to 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 occurred in many countries.7Somekh I. Somech R. Pettoello-Mantovani M. Somekh E. Changes in routine pediatric practice in light of coronavirus 2019 (COVID-19).J Pediatr. 2020; 224: 190-193Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar, 8Rabbone I. Schiaffini R. Cherubini V. Maffeis C. Scaramuzza A. Diabetes Study Group of the Italian Society for Pediatric Endocrinology and Diabetes. Has COVID-19 delayed the diagnosis and worsened the presentation of type 1 diabetes in children?.Diabetes Care. 2020; 43: 2870-2872Crossref PubMed Scopus (129) Google Scholar, 9Spencer N. Nathawad R. Arpin E. Johnson S. Pandemics, epidemics and inequities in routine childhood vaccination coverage: a rapid review.BMJ Paediatr Open. 2020; 4: e000842Crossref PubMed Scopus (7) Google Scholar The measures taken by governments to contain the crisis often raised criticism from the European pediatric societies because of their frequent changes and the overall negative impact on children's physical and mental health and their education.10Jiao W.Y. Wang L.N. Liu J. Fang S.F. Jiao F.Y. Pettoello-Mantovani M. et al.Behavioral and emotional disorders in children during the COVID-19 epidemic.J Pediatr. 2020; 221: 264-266.e1Abstract Full Text Full Text PDF PubMed Scopus (608) Google Scholar, 11Ferrara P. Franceschini G. Corsello G. Mestrovic J. Giardino I. Vural M. et al.The dark side of the web—a risk for children and adolescents challenged by isolation during the novel coronavirus 2019 pandemic.J Pediatr. 2021; 228: 324-325.e2Abstract Full Text Full Text PDF PubMed Scopus (10) Google Scholar, 12Hoey H. Mestrovic J. Vural M. Baranova L.N. Somekh E. Pettoello–Mantovani M. Children facing natural, economic and public health crisis in Europe: the risks of a predictable unpredictability.Turk Pediatri Ars. 2020; 55: 4-9PubMed Google Scholar In summer 2020, the 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 of obtaining information about the consequences of the pandemic on pediatric primary care practices in different locales and the risks for child health.13European Confederation of Primary Care PediatriciansHow did the COVID-19 pandemic change paediatric primary care? Results of a European primary care survey.https://www.ecpcp.eu/fileadmin/pdf_doc_ppt/Data_results_of_the_PCP_survey__for_Websites_ECPCP_and_EPA-_UNEPSA.pdfDate accessed: February 11, 2021Google Scholar,14Huss G. Magendie C. Pettoello-Mantovani M. Jaeger-Roman E. The implications of the COVID-19 pandemic for pediatric primary care practice in Europe.J Pediatr. 2021; ([Epub ahead of print])https://doi.org/10.1016/j.jpeds.2021.03.004Abstract Full Text Full Text PDF PubMed Scopus (1) Google Scholar 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 to minimize the transmission of COVID-19 from patient to patient and among office staff. At the beginning of the pandemic, a serious shortage of protective equipment endangered health workers worldwide,15UN NewsWe can’t stop COVID-19 without protecting health workers: WHO chief.https://news.un.org/en/story/2020/03/1058581Date: 2020Date accessed: February 14, 2021Google Scholar particularly in ambulatory settings.16American Academy of Paediatrics, AAP NewsAAP issues guidance to ensure continued care for children during pandemic.https://www.aappublications.org/news/2020/04/14/ambulatory041420Date accessed: December 28, 2020Google Scholar,17Walker D. Chandir S. COVID-19és lost generation of unvaccinated children.Lancet Glob Health. 2021; 9: e250Abstract Full Text Full Text PDF PubMed Scopus (4) Google Scholar However, 95% of European primary care pediatricians reported systematic use of personal protective clothing and face masks within a short time from the onset of the pandemic, and 92% expressed their commitment to maintaining this practice beyond its end.13European Confederation of Primary Care PediatriciansHow did the COVID-19 pandemic change paediatric primary care? Results of a European primary care survey.https://www.ecpcp.eu/fileadmin/pdf_doc_ppt/Data_results_of_the_PCP_survey__for_Websites_ECPCP_and_EPA-_UNEPSA.pdfDate accessed: February 11, 2021Google Scholar 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. Slightly more than one-half (55%) of primary care pediatricians reported that during the pandemic period March-August 2020, in-person consultations rates dropped by 40% to >80% compared to previous periods. However, an effort was made to continue to offer the option of pediatrician–patient encounters by applying the “ECPCP empty waiting room policy” characterized by well-planned appointment schedules, which helped minimize waiting times and discouraged unscheduled walk-in visits.13European Confederation of Primary Care PediatriciansHow did the COVID-19 pandemic change paediatric primary care? Results of a European primary care survey.https://www.ecpcp.eu/fileadmin/pdf_doc_ppt/Data_results_of_the_PCP_survey__for_Websites_ECPCP_and_EPA-_UNEPSA.pdfDate accessed: February 11, 2021Google Scholar In most European countries, primary care pediatricians followed the directions recommended by local public health departments and World Health Organization health officials and limited the number of accompanying persons during visits in private settings, such that children could be accompanied by only 1 caretaker.18Agostiniani R. Bozzola E. Staiano A. Del Vecchio A. Mazzone T. Greco L. et al.Providing pediatric well-care and sick visits in the COVID-19 pandemic era: the recommendations of the Italian Pediatric Society.Ital J Pediatr. 2020; 46: 133Crossref PubMed Scopus (7) Google Scholar,19World Health Organization (WHO)Maintaining essential health services during the COVID-19 outbreak.https://www.who.int/emergencies/diseases/novel-coronavirus-2019/related-health-issuesDate accessed: February 16, 2021Google Scholar As a result, crowding of patients in waiting rooms was significantly reduced.13European Confederation of Primary Care PediatriciansHow did the COVID-19 pandemic change paediatric primary care? Results of a European primary care survey.https://www.ecpcp.eu/fileadmin/pdf_doc_ppt/Data_results_of_the_PCP_survey__for_Websites_ECPCP_and_EPA-_UNEPSA.pdfDate accessed: February 11, 2021Google Scholar Providing separate rooms and separate consulting hours for infectious and noninfectious patients was another important safety measure, although it was not possible in all circumstances. However, the changes applied to routine practice because of the pandemic and fearful attitudes by parents caused unintended and sometimes negative consequences.13European Confederation of Primary Care PediatriciansHow did the COVID-19 pandemic change paediatric primary care? Results of a European primary care survey.https://www.ecpcp.eu/fileadmin/pdf_doc_ppt/Data_results_of_the_PCP_survey__for_Websites_ECPCP_and_EPA-_UNEPSA.pdfDate accessed: February 11, 2021Google Scholar 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 of some delays in recognizing serious conditions, thereby increasing the risk of complications.13European Confederation of Primary Care PediatriciansHow did the COVID-19 pandemic change paediatric primary care? Results of a European primary care survey.https://www.ecpcp.eu/fileadmin/pdf_doc_ppt/Data_results_of_the_PCP_survey__for_Websites_ECPCP_and_EPA-_UNEPSA.pdfDate accessed: February 11, 2021Google Scholar A large proportion of the pediatricians involved in the study (86%) reported that due to the restricted access to emergency services, in many cases, family members of their patients admitted failing to report or delaying reporting to local health authorities serious health conditions or life-threatening diseases besides COVID-19 involving their children. The most commonly unreported conditions included diabetic ketoacidosis, hematologic and oncologic diseases, appendicitis, peritonitis, child abuse, severe bacterial infections (eg, urinary tract infection), meningitis, pneumonia, and acute cardiac problems.13European Confederation of Primary Care PediatriciansHow did the COVID-19 pandemic change paediatric primary care? Results of a European primary care survey.https://www.ecpcp.eu/fileadmin/pdf_doc_ppt/Data_results_of_the_PCP_survey__for_Websites_ECPCP_and_EPA-_UNEPSA.pdfDate accessed: February 11, 2021Google Scholar Similar data were reported in the US20Gerall C.D. DeFazio J.R. Kahan A.M. Fan W. Fallon E.M. Middlesworth W. et al.Delayed presentation and sub-optimal outcomes of pediatric patients with acute appendicitis during the COVID-19 pandemic.J Pediatr Surg. 2020; ([Epub ahead of print])https://doi.org/10.1016/j.jpedsurg.2020.10.008Abstract Full Text Full Text PDF Scopus (44) Google Scholar and Israel.21Rosenberg Danziger C. Krause I. Scheuerman O. Luder A. Yulevich A. Dalal I. et al.Pediatrician, watch out for corona-phobia.Eur J Pediatr. 2021; 180: 201-206Crossref PubMed Scopus (11) Google Scholar A study involving 53 Italian diabetes centers revealed that COVID-19 significantly worsened the presentation of type 1 diabetes in children.8Rabbone I. Schiaffini R. Cherubini V. Maffeis C. Scaramuzza A. Diabetes Study Group of the Italian Society for Pediatric Endocrinology and Diabetes. Has COVID-19 delayed the diagnosis and worsened the presentation of type 1 diabetes in children?.Diabetes Care. 2020; 43: 2870-2872Crossref PubMed Scopus (129) Google Scholar In the summer of 2020, the World Health Organization and UNICEF warned of an alarming decline in the number of children receiving life-saving vaccines worldwide.22World Health OrganizationWHO and UNICEF warn of a decline in vaccinations during COVID-19.https://www.who.int/news/item/15-07-2020-who-and-unicef-warn-of-a-decline-in-vaccinations-during-covid-19Date accessed: February 14, 2021Google Scholar 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 the 82 countries involved in a preliminary study reported significant COVID-19–related disruptions in their immunization programs by May 2020.22World Health OrganizationWHO and UNICEF warn of a decline in vaccinations during COVID-19.https://www.who.int/news/item/15-07-2020-who-and-unicef-warn-of-a-decline-in-vaccinations-during-covid-19Date accessed: February 14, 2021Google Scholar 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 >50%, in children <2 years and >2 years of age. A major obstacle to the implementation of vaccination programs reported by European pediatricians is families’ fear of leaving home during lockdown and the hesitation to vaccinate their children during the pandemic.22World Health OrganizationWHO and UNICEF warn of a decline in vaccinations during COVID-19.https://www.who.int/news/item/15-07-2020-who-and-unicef-warn-of-a-decline-in-vaccinations-during-covid-19Date accessed: February 14, 2021Google Scholar,23McIntosh E.D.G. Janda J. Ehrich J.H.H. Pettoello-Mantovani M. Somekh E. Vaccine hesitancy and refusal.J Pediatr. 2016; 175: 248-249.e1Abstract Full Text Full Text PDF PubMed Scopus (41) Google Scholar Social distancing during COVID-19 has caused a drastic upheaval in how 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.24Lee J. Mental health effects of school closures during COVID-19.Lancet Child Adolesc Health. 2020; 4: 421Abstract Full Text Full Text PDF PubMed Scopus (798) Google Scholar 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 lifestyle caused by the pandemic affect the well-being of children and adolescents would be greatly useful.24Lee J. Mental health effects of school closures during COVID-19.Lancet Child Adolesc Health. 2020; 4: 421Abstract Full Text Full Text PDF PubMed Scopus (798) Google Scholar 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.25Herbert J.S. Mitchell A. Brentnall S.J. Bird A.L. Identifying rewards over difficulties buffers the impact of time in COVID-19 lockdown for parents in Australia.Front Psychol. 2020; 11: 606507Crossref PubMed Scopus (12) Google Scholar In families that spend longer periods together, COVID-19 may exacerbate preexisting vulnerabilities, including depression and anxiety, which can harm the stability of relationships and increase the risks of abuse and violence.25Herbert J.S. Mitchell A. Brentnall S.J. Bird A.L. Identifying rewards over difficulties buffers the impact of time in COVID-19 lockdown for parents in Australia.Front Psychol. 2020; 11: 606507Crossref PubMed Scopus (12) Google Scholar,26Ferrara P. Caporale O. Cutrona C. Sbordone A. Amato M. Spina G. et al.Femicide and murdered women's children: which future for these children orphans of a living parent?.Ital J Pediatr. 2015; 41: 68Crossref PubMed Scopus (30) Google Scholar 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 well-being of children caused by the pandemic.9Spencer N. Nathawad R. Arpin E. Johnson S. Pandemics, epidemics and inequities in routine childhood vaccination coverage: a rapid review.BMJ Paediatr Open. 2020; 4: e000842Crossref PubMed Scopus (7) Google Scholar The lockdown due to COVID 19 has also exacerbated socioeconomic inequalities, including worsened educational performance of children from poor socioeconomic 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. Coordinated efforts among healthcare professionals27Ehrich J.H.H. Kerbl R. Pettoello-Mantovani M. Lenton S. Opening the debate on pediatric subspecialties and specialist centers: opportunities for better care or risks of care fragmentation?.J Pediatr. 2015; 167: 1177-1178.e2Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar will help ensure optimum health care for both 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.28Villani A. Giuliani M. Raponi M. Ladogana S. Cristalli P. Sacco M. et al.Child healthcare services offered by the Vatican City State in its national territory and in extra-territorial neighboring Italian areas.Turk Pediatri Ars. 2020; 55: 105-111PubMed Google Scholar In view of the challenges posed by the pandemic, the data provided by the ECPCP suggest that it will be essential to implement a strategy aimed at preserving the continuity of preventive services and vaccination programs and focusing on the free, fearless access of all children to health services.

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