155
Views
0
CrossRef citations to date
0
Altmetric
Perspective

Examining the associations between COVID-19 infection and pediatric type 1 diabetes

ORCID Icon, ORCID Icon, , &
Pages 489-497 | Received 23 Jan 2023, Accepted 07 Mar 2023, Published online: 12 Mar 2023

References

  • Esposito S, Giannitto N, Squarcia A, et al. Development of psychological problems among adolescents during school closures because of the COVID-19 lockdown phase in italy: a cross-sectional survey. Front Pediatr. 2020;8:628072.
  • Salzano G, Passanisi S, Pira F, et al. Quarantine due to the COVID-19 pandemic from the perspective of adolescents: the crucial role of technology. Ital J Pediatr. 2021;47(1):40. DOI:10.1186/s13052-021-00997-7
  • Dipasquale V, Passanisi S, Cucinotta U, et al. Implications of SARS-COV-2 infection in the diagnosis and management of the pediatric gastrointestinal disease. Ital J Pediatr. 2021;47(1):71. DOI:10.1186/s13052-021-01020-9
  • Passanisi S, Pecoraro M, Pira F, et al. Quarantine due to the covid-19 pandemic from the perspective of pediatric patients with type 1 Diabetes: a web-based survey. Front Pediatr. 2020;8:491.
  • Calcaterra V, Iafusco D, Carnevale Pellino V, et al. “CoVidentary”: an online exercise training program to reduce sedentary behaviours in children with type 1 diabetes during the COVID-19 pandemic. J Clin Transl Endocrinol. 2021;25:100261.
  • WHO Coronavirus (COVID-19) Dashboard [Internet]. [cited 2023 Jan 21]. Available from: https://covid19.who.int
  • Riffe T, Acosta E, Acosta EJ. The coverage-db team. Data resource profile: coverage-DB: a global demographic database of COVID-19 cases and deaths. Int J Epidemiol. 2021;50(2):390.
  • Delahoy MJ, Ujamaa D, Whitaker M, et al. Hospitalizations associated with COVID-19 among children and adolescents — COVID-NET, 14 states, march 1, 2020–august 14, 2021. MMWR Morb Mortal Wkly Rep. 2021;70(36):1255–1260. DOI:10.15585/mmwr.mm7036e2
  • Nikolopoulou GB, Maltezou HC. COVID-19 in children: where do we stand? Arch Med Res. 2022;53(1):1–8.
  • Passanisi S, Lombardo F, Salzano G, et al. Are children most of the submerged part of SARS-CoV-2 iceberg? Front Pediatr. 2020;8:213.
  • Costagliola G, Spada E, Consolini R. Age-related differences in the immune response could contribute to determine the spectrum of severity of COVID-19. Immun Inflamm Dis. 2021;9(2):331–339.
  • Nickbakhsh S, Mair C, Matthews L, et al. Virus–virus interactions impact the population dynamics of influenza and the common cold. Proc Natl Acad Sci U S A. 2019;116(52):27142–27150. DOI:10.1073/pnas.1911083116
  • Ludvigsson JF. Systematic review of COVID-19 in children shows milder cases and a better prognosis than adults. Acta Paediatr. 2020;109(6):1088–1095.
  • Chen J, Jiang Q, Xia X, et al. Individual variation of the SARS-CoV-2 receptor ACE2 gene expression and regulation. Aging Cell. 2020;19:e13168.
  • Ejaz H, Alsrhani A, Zafar A, et al. COVID-19 and comorbidities: deleterious impact on infected patients. J Infect Public Health. 2020;13(12):1833–1839. DOI:10.1016/j.jiph.2020.07.014
  • Gregory GA, Robinson TIG, Linklater SE, et al. Global incidence, prevalence, and mortality of type 1 diabetes in 2021 with projection to 2040: a modelling study. Lancet Diabetes Endocrinol. 2022;10(10):741–760. DOI:10.1016/S2213-8587(22)00218-2
  • Ogle GD, James S, Dabelea D, et al. Global estimates of incidence of type 1 diabetes in children and adolescents: results from the international diabetes federation atlas. 10th Diabet Res Clin Pract. 2022;183:109083
  • Mayer-Davis EJ, Kahkoska AR, Jefferies C, et al. ISPAD clinical practice consensus guidelines 2018: definition, epidemiology, and classification of diabetes in children and adolescents. Pediatr Diabetes. 2018;19(27):7–19. DOI:10.1111/pedi.12773
  • Nguyen C, Varney MD, Harrison LC, et al. Definition of high-risk type 1 diabetes HLA-DR and HLA-DQ types using only three single nucleotide polymorphisms. Diabetes. 2013;62:2135–2140.
  • Dedrick S, Sundaresh B, Huang Q, et al. The role of gut microbiota and environmental factors in type 1 diabetes pathogenesis. Front Endocrinol. 2020;11:78.
  • Krischer JP, Lynch KF, Schatz DA, et al. The 6 year incidence of diabetes-associated autoantibodies in genetically at-risk children: the TEDDY study. Diabetologia. 2015;58:980–987.
  • Rasmussen T, Witsø E, Tapia G, et al. Self-reported lower respiratory tract infections and development of islet autoimmunity in children with the type 1 diabetes high-risk HLA genotype: the MIDIA study. Diabetes Metab Res Rev. 2011;27(8):834–837. DOI:10.1002/dmrr.1258
  • Karvonen M, Jäntti V, Muntoni S, et al. Comparison of the seasonal pattern in the clinical onset of IDDM in finland and sardinia. Diabetes Care. 1998;21:1101–1109.
  • Principi N, Berioli MG, Bianchini S, et al. Type 1 diabetes and viral infections: what is the relationship? J Clin Virol. 2017;96:26–31.
  • Rabbone I, Schiaffini R, Cherubini V, et al. Has COVID-19 delayed the diagnosis and worsened the presentation of type 1 diabetes in children? Diabetes Care. 2020;43:2870–2872.
  • Mameli C, Scaramuzza A, Macedoni M, et al. Type 1 diabetes onset in Lombardy region, Italy, during the COVID-19 pandemic: the double-wave occurrence. EClinicalMedicine. 2021;39:101067.
  • Cinek O, Slavenko M, Pomahačová R, et al. Type 1 diabetes incidence increased during the COVID-19 pandemic years 2020–2021 in Czechia: results from a large population-based pediatric register. Pediatr Diabetes. 2022;23(7):956–960. DOI:10.1111/pedi.13405
  • Kamrath C, Rosenbauer J, Eckert AJ, et al. Incidence of type 1 diabetes in children and adolescents during the COVID-19 pandemic in Germany: results from the DPV registry. Diabetes Care. 2022;45:1762–1771.
  • Pietrzak I, Michalak A, Seget S, et al. Diabetic ketoacidosis incidence among children with new-onset type 1 diabetes in poland and its association with COVID-19 outbreak—two-year cross-sectional national observation by PolPeDiab study group. Pediatr Diabetes. 2022;23(7):944–955. DOI:10.1111/pedi.13379
  • Wolf RM, Noor N, Izquierdo R, et al. Increase in newly diagnosed type 1 diabetes in youth during the COVID-19 pandemic in the United States: a multi-center analysis. Pediatr Diabetes. 2022;23(4):433–438. DOI:10.1111/pedi.13328
  • Leiva-Gea I, Fernández CA, Cardona-Hernandez R, et al. Increased presentation of diabetic ketoacidosis and changes in age and month of type 1 diabetes at onset during the COVID-19 pandemic in spain. J Clin Med. 2022;11(15):4338. DOI:10.3390/jcm11154338
  • Rahmati M, Keshvari M, Mirnasuri S, et al. The global impact of COVID-19 pandemic on the incidence of pediatric new-onset type 1 diabetes and ketoacidosis: a systematic review and meta-analysis. J Med Virol. 2022;94(11):5112–5127. DOI:10.1002/jmv.27996
  • Modarelli R, Sarah S, Ramaker ME, et al. Pediatric diabetes on the rise: trends in incident diabetes during the COVID-19 pandemic. J Endocr Soc. 2022;6(4):bvac024. DOI:10.1210/jendso/bvac024
  • Marks BE, Khilnani A, Meyers A, et al. Increase in the diagnosis and severity of presentation of pediatric type 1 and type 2 diabetes during the COVID-19 pandemic. Horm Res Paediatr. 2021;94(7–8):275–284. DOI:10.1159/000519797
  • Raicevic M, Samardzic M, Soldatovic I, et al. Trends in nationwide incidence of pediatric type 1 diabetes in montenegro during the last 30 years. Front Endocrinol. 2022;13:991533.
  • Unsworth R, Wallace S, Oliver NS, et al. New-onset type 1 diabetes in children during COVID-19: multicenter regional findings in the U.K. Diabetes Care. 2020;43:e170–1.
  • Schiaffini R, Deodati A, Rapini N, et al. Increased incidence of childhood type 1 diabetes during the COVID-19 pandemic. Figures from an Italian tertiary care center. J Diabetes. 2022;14(8):562–563. DOI:10.1111/1753-0407.13298
  • Ansar A, Livett T, Beaton W, et al. Sharp Rise in New-Onset Pediatric Diabetes During the COVID-19 Pandemic. WMJ. 2022;121(3):177–180.
  • Donbaloğlu Z, Tuhan H, Tural Kara T, et al. The Examination of the Relationship Between COVID-19 and New-Onset Type 1 Diabetes Mellitus in Children. Turk Arch Pediatr. 2022;57(2):222–227. DOI:10.5152/TurkArchPediatr.2022.21284
  • Gottesman BL, Yu J, Tanaka C, et al. Incidence of New-Onset Type 1 Diabetes Among US Children During the COVID-19 Global Pandemic. JAMA Pediatr. 2022;176(4):414–415. DOI:10.1001/jamapediatrics.2021.5801
  • Passanisi S, Salzano G, Aloe M, et al. Increasing trend of type 1 diabetes incidence in the pediatric population of the Calabria region in 2019–2021. Ital J Pediatr. 2022;48(1):66. DOI:10.1186/s13052-022-01264-z
  • Kamrath C, Rosenbauer J, Tittel SR, et al. Frequency of Autoantibody-Negative Type 1 Diabetes in Children, Adolescents, and Young Adults During the First Wave of the COVID-19 Pandemic in Germany. Diabetes Care. 2021;44:1540–1546.
  • Reschke F, Lanzinger S, Herczeg V, et al. The COVID-19 Pandemic Affects Seasonality, with Increasing Cases of New-Onset Type 1 Diabetes in Children, from the Worldwide SWEET Registry. Diabetes Care. 2022;45:2594–2601.
  • van den Boom L, Kostev K, Kuss O, et al. Type 1 diabetes incidence in children and adolescents during the COVID-19 pandemic in Germany. Diabet Res Clin Pract. 2022;193:110146.
  • Denina M, Trada M, Tinti D, et al. Increase in newly diagnosed type 1 diabetes and serological evidence of recent SARS-CoV-2 infection: is there a connection? Front Med. 2022;9:927099.
  • Ata A, Jalilova A, Kırkgöz T, et al. Does COVID-19 predispose patients to type 1 diabetes mellitus? Clin Pediatr Endocrinol. 2022;31(1):33–37. DOI:10.1297/cpe.2021-0050
  • Salmi H, Heinonen S, Hästbacka J, et al. New-onset type 1 diabetes in Finnish children during the COVID-19 pandemic. Arch Dis Child. 2022;107(2):180–185. DOI:10.1136/archdischild-2020-321220
  • Nóvoa-Medina Y, Pavlovic-Nesic S, González-Martín JM, et al. Role of the SARS-CoV-2 virus in the appearance of new onset type 1 diabetes mellitus in children in Gran Canaria, Spain. J Pediatr Endocrinol Metab. 2022;35:393–397.
  • Herczeg V, Luczay A, Ténai N, et al. Anti-SARS-CoV-2 Seropositivity Among Children with Newly Diagnosed Type 1 Diabetes Mellitus: a Case-Control Study. Indian Pediatr. 2022;59(10):809–810. DOI:10.1007/s13312-022-2626-y
  • Barrett CE, Koyama AK, Alvarez P, et al. Risk for Newly Diagnosed Diabetes >30 Days After SARS-CoV-2 Infection Among Persons Aged <18 Years - United States, March 1, 2020-June 28, 2021. MMWR Morb Mortal Wkly Rep. 2022;71(2):59–65. DOI:10.15585/mmwr.mm7102e2.
  • Qeadan F, Tingey B, Egbert J, et al. The associations between COVID-19 diagnosis, type 1 diabetes, and the risk of diabetic ketoacidosis: a nationwide cohort from the US using the Cerner Real-World Data. PLoS ONE. 2022;17:e0266809.
  • Kendall EK, Olaker VR, Kaelber DC, et al. Association of SARS-CoV-2 Infection with New-Onset Type 1 Diabetes Among Pediatric Patients from 2020 to 2021. JAMA Netw Open. 2022;5(9):e2233014. DOI:10.1001/jamanetworkopen.2022.33014
  • McKeigue PM, McGurnaghan S, Blackbourn L, et al. Relation of Incident Type 1 Diabetes to Recent COVID-19 Infection: cohort Study Using e-Health Record Linkage in Scotland. Diabetes Care. 2022;dc220385.
  • Pietropaolo M, Hotez P, Giannoukakis N. Incidence of an Insulin-Requiring Hyperglycemic Syndrome in SARS-CoV-2–infected Young Individuals: is It Type 1 Diabetes? Diabetes. 2022;71(12):2656–2663.
  • Montefusco L, Ben Nasr M, D’addio F, et al. Acute and long-term disruption of glycometabolic control after SARS-CoV-2 infection. Nat Metab. 2021;3(6):774–785. DOI:10.1038/s42255-021-00407-6
  • Soliman AT, Al-Amri M, Alleethy K, et al. Newly-onset type 1 diabetes mellitus precipitated by COVID-19 in an 8-month-old infant. Acta Biomed. 2020. DOI:10.23750/abm.v91i3.10074
  • Valenzuela-Vallejo L, López-Ramírez SA, Morales-Burton V, et al. Pediatric diabetic ketoacidosis as type 1 diabetes debut with concurrent SARS-CoV-2 infection: a case report. SAGE Open Med Case Rep. 2022;10:2050313X221097263.
  • Ambati S, Mihic M, Rosario DC, et al. New-Onset Type 1 Diabetes in Children with SARS-CoV-2 Infection. Cureus. 2022;14:e22790.
  • Ordooei M, Behniafard N, Soheilipour F, et al. New onset of diabetes in a child infected with COVID-19: a case report. J Diabetes Metab Disord. 2021;20(2):2129–2132. DOI:10.1007/s40200-021-00900-5
  • Benyakhlef S, Abdellaoui W, Tahri A, et al. Diabetic Ketoacidosis at Onset of Pediatric Type-1 Diabetes Triggered by Covid-19: an Original Case Report. Cureus. 2021;13:e13958.
  • Ratzmann KP, Strese J, Witt S, et al. Mumps infection and insulin-dependent diabetes mellitus (IDDM). Diabetes Care. 1984;7:170–173.
  • Huber S, Ramsingh AI. Coxsackievirus-induced pancreatitis. Viral Immunol. 2004;17(3):358–369.
  • Yang JK, Lin SS, Ji XJ, et al. Binding of SARS coronavirus to its receptor damages islets and causes acute diabetes. Acta Diabetol. 2010;47(3):193–199. DOI:10.1007/s00592-009-0109-4
  • Fignani D, Licata G, Brusco N, et al. SARS-CoV-2 Receptor Angiotensin I-Converting Enzyme Type 2 (ACE2) is Expressed in Human Pancreatic β-Cells and in the Human Pancreas Microvasculature. Front Endocrinol. 2020;11:596898.
  • Salamanna F, Maglio M, Landini MP, et al. Body Localization of ACE-2: on the Trail of the Keyhole of SARS-CoV-2. Front Med. 2020;7:594495.
  • Hoffmann M, Kleine-Weber H, Schroeder S, et al. SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and is Blocked by a Clinically Proven Protease Inhibitor. Cell. 2020;181(2):271–280.e8. DOI:10.1016/j.cell.2020.02.052
  • Rubino F, Amiel SA, Zimmet P, et al. New-Onset Diabetes in Covid-19. N Engl J Med. 2020;383(8):789–790. DOI:10.1056/NEJMc2018688
  • Koch J, Uckeley ZM, Doldan P, et al. TMPRSS2 expression dictates the entry route used by SARS-CoV-2 to infect host cells. Embo J. 2021;40(16):e107821. DOI:10.15252/embj.2021107821
  • Cantuti-Castelvetri L, Ojha R, Pedro LD, et al. Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity. Science. 2020;370:856–860.
  • Wu CT, Lidsky PV, Xiao Y, et al. SARS-CoV-2 infects human pancreatic β cells and elicits β cell impairment. Cell Metab. 2021;33(8):1565–1576.e5. DOI:10.1016/j.cmet.2021.05.013.
  • Clausen TM, Sandoval DR, Spliid CB, et al. SARS-CoV-2 Infection Depends on Cellular Heparan Sulfate and ACE2. Cell. 2020;183(4):1043–1057.e15. DOI:10.1016/j.cell.2020.09.033
  • Kusmartseva I, Wu W, Syed F, et al. Expression of SARS-CoV-2 Entry Factors in the Pancreas of Normal Organ Donors and Individuals with COVID-19. Cell Metab. 2020;32(6):1041–1051.e6. DOI:10.1016/j.cmet.2020.11.005
  • van der Heide V, Jangra S, Cohen P, et al. Limited extent and consequences of pancreatic SARS-CoV-2 infection. Cell Rep. 2022;38:110508.
  • Tang X, Uhl S, Zhang T, et al. SARS-CoV-2 infection induces beta cell transdifferentiation. Cell Metab. 2021;33(8):1577–1591.e7. DOI:10.1016/j.cmet.2021.05.015
  • Grunnet LG, Aikin R, Tonnesen MF, et al. Proinflammatory Cytokines Activate the Intrinsic Apoptotic Pathway in β-Cells. Diabetes. 2009;58(8):1807–1815. DOI:10.2337/db08-0178
  • Ben Nasr M, D’addio F, Montefusco L, et al. Indirect and Direct Effects of SARS-CoV-2 on Human Pancreatic Islets. Diabetes. 2022;71:1579–1590.
  • Nakra NA, Blumberg DA, Herrera-Guerra A, et al. Multi-System Inflammatory Syndrome in Children (MIS-C) Following SARS-CoV-2 Infection: review of Clinical Presentation. Hypothetical Pathogenesis, and Proposed Management Children (Basel). 2020;7(7):69. DOI:10.3390/children7070069
  • Aly HH, Fouda EM, Kotby AA, et al. COVID-19–related Multisystem Inflammatory Syndrome in Children Presenting with New-Onset Type 1 Diabetes in Severe Ketoacidosis: a Case Series. Diabetes Care. 2022;45(4):983–989. DOI:10.2337/dc21-1094
  • Naguib MN, Raymond JK, Vidmar AP. New onset diabetes with diabetic ketoacidosis in a child with multisystem inflammatory syndrome due to COVID-19. J Pediatr Endocrinol Metab. 2021;34(1):147–150.
  • Reiterer M, Rajan M, Gómez-Banoy N, et al. Hyperglycemia in acute COVID-19 is characterized by insulin resistance and adipose tissue infectivity by SARS-CoV-2. Cell Metab. 2021;33(11):2174–2188.e5. DOI:10.1016/j.cmet.2021.09.009
  • Clarke SA, Phylactou M, Patel B, et al. Preserved C-peptide in survivors of COVID-19: post hoc analysis. Diab Obes Metab. 2022;24(3):570–574. DOI:10.1111/dom.14608
  • Keiner ES, Slaughter JC, Datye KA, et al. COVID-19 exacerbates insulin resistance during diabetic ketoacidosis in pediatric patients with type 1 diabetes. Diabetes Care. 2022;45:2406–2411.
  • Huang I, Lim MA, Pranata R. Diabetes mellitus is associated with increased mortality and severity of disease in COVID-19 pneumonia – a systematic review, meta-analysis, and meta-regression. Diabetes Metab Syndr. 2020;14(4):395–403.
  • Barron E, Bakhai C, Kar P, et al. Associations of type 1 and type 2 diabetes with COVID-19-related mortality in England: a whole-population study. Lancet Diabetes Endocrinol. 2020;8(10):813–822. DOI:10.1016/S2213-8587(20)30272-2
  • Gregory JM, Slaughter JC, Duffus SH, et al. COVID-19 Severity is Tripled in the Diabetes Community: a Prospective Analysis of the Pandemic’s Impact in Type 1 and Type 2 Diabetes. Diabetes Care. 2021;44:526–532.
  • Cardona-Hernandez R, Cherubini V, Iafusco D, et al. Children and youth with diabetes are not at increased risk for hospitalization due to COVID-19. Pediatr Diabetes. 2021;22(2):202–206. DOI:10.1111/pedi.13158
  • Tatti P, Tonolo G, Zanfardino A, et al. Is it fair to hope that patients with Type 1 Diabetes (autoimmune) may be spared by the infection of Covid-19? Med Hypotheses. 2020;142:109795.
  • Woodruff RC, Campbell AP, Taylor CA, et al. Risk Factors for Severe COVID-19 in Children. Pediatrics. 2022;149:e2021053418.
  • Kompaniyets L, Agathis NT, Nelson JM, et al. Underlying Medical Conditions Associated with Severe COVID-19 Illness Among Children. JAMA Netw Open. 2021;4(6):e2111182. DOI:10.1001/jamanetworkopen.2021.11182
  • Mann EA, Rompicherla S, Gallagher MP, et al. Comorbidities increase COVID-19 hospitalization in young people with type 1 diabetes. Pediatr Diabetes. 2022;23(7):968–975. DOI:10.1111/pedi.13402
  • Alonso GT, Ebekozien O, Gallagher MP, et al. Diabetic ketoacidosis drives COVID-19 related hospitalizations in children with type 1 diabetes. J Diabetes. 2021;13(8):681–687. DOI:10.1111/1753-0407.13184.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.