Unveiling risk factors for post-COVID-19 syndrome development in people with type 2 diabetes
Anton Matviichuk, Viktoriia Yerokhovych, Sergii Zemskov, Yeva Ilkiv, Vitalii Gurianov, Zlatoslava Shaienko, Tetyana Falalyeyeva, Oksana Sulaieva, Nazarii Kobyliak
Frontiers in Endocrinology, doi:10.3389/fendo.2024.1459171
Introduction: Post-COVID-19 syndrome (PCS) is a severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection-associated chronic condition characterized by long-term violations of physical and mental health. People with type 2 diabetes (T2D) are at high risk for severe COVID-19 and PCS.
Aim: The current study aimed to define the predictors of PCS development in people with T2D for further planning of preventive measures and improving patient outcomes.
Materials and methods: The data were collected through the national survey targeting persons with T2D concerning the history of COVID-19 course and signs and symptoms that developed during or after COVID-19 and continued for more than 12 weeks and were not explained by an alternative diagnosis. In total, 469 patients from different regions of Ukraine were enrolled in the study. Among them, 227 patients reported PCS development (main group), while 242 patients did not claim PCS symptoms (comparison group). Stepwise multivariate logistic regression and probabilistic neural network (PNN) models were used to select independent risk factors. Results: Based on the survey data, 8 independent factors associated with the risk of PCS development in T2D patients were selected: newly diagnosed T2D (OR 4.86; 95% CI 2.55-9.28; p<0.001), female sex (OR 1.29; 95% CI 0.86-1.94; p=0.220), COVID-19 severity (OR 1.35 95% CI 1.05-1.70; p=0.018), myocardial infarction (OR 2.42 95% CI 1.26-4.64; p=0.002) and stroke (OR 3.68 95% CI 1.70-7.96; p=0.001) in anamnesis, HbA1c above 9.2% (OR 2.17 95% CI 1.37-3.43; p=0.001), and the use of insulin analogs p=0.003) vs human insulin p=0.146). Although obesity aggravated COVID-19 severity, it did not impact PCS development. In ROC analysis, the 8factor multilayer perceptron (MLP) model exhibited better performance (AUC 0.808; 95% CІ 0.770-0.843), allowing the prediction of the risk of PCS development with a sensitivity of 71.4%, specificity of 76%, PPV of 73.6% and NPV of 73.9%.
Ethics statement The studies involving humans were approved by Bogomolets National Medical University. The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study.
Author contributions
Conflict of interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
Publisher's note All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Abumayyaleh, Gil, Mc, Roubin, Romero et al., Post-COVID-19 syndrome and diabetes mellitus: a propensity-matched analysis of the International HOPE-II COVID-19 Registry, Front Endocrinol,
doi:10.3389/FENDO.2023.1167087Bramante, Buse, Liebovitz, Nicklas, Puskarich et al., Outpatient treatment of COVID-19 and incidence of post-COVID-19 condition over 10 months (COVID-OUT): a multicentre, randomised, quadruple-blind, parallelgroup, phase 3 trial, Lancet Infect Dis,
doi:10.1016/S1473-3099(23)00299-2Buchynskyi, Kamyshna, Lyubomirskaya, Moshynets, Kobyliak et al., Efficacy of interferon alpha for the treatment of hospitalized patients with COVID-19: A meta-analysis, Front Immunol,
doi:10.3389/FIMMU.2023.1069894Cao, Baranova, Wei, Wang, Zhang, Bidirectional causal associations between type 2 diabetes and COVID-19, J Med Virol,
doi:10.1002/JMV.28100Dimnjakovićj, Buble, Ivanko, Pristaši, Brborovićo, Association of anti-diabetic drugs and COVID-19 outcomes in patients with diabetes mellitus type 2 and cardiomyopathy, Sci Rep,
doi:10.1038/S41598-024-57871-9Fedotkina, Sulaieva, Ozgumus, Cherviakova, Khalimon et al., Novel reclassification of adult diabetes is useful to distinguish stages of b-cell function linked to the risk of vascular complications: the DOLCE study from northern Ukraine, Front Genet,
doi:10.3389/FGENE.2021.637945Feldman, Savelieff, Hayek, Pennathur, Kretzler et al., COVID-19 and diabetes: A collision and collusion of two diseases, Diabetes,
doi:10.2337/DBI20-0032Fernoández-De-Las-Penas, Guijarro, Torres-Macho, Velasco-Arribas, Plaza-Canteli et al., Diabetes and the risk of long-term post-COVID symptoms, Diabetes,
doi:10.2337/DB21-0329Fignani, Licata, Brusco, Nigi, Grieco et al., SARS-coV-2 receptor angiotensin I-converting enzyme type 2 (ACE2) is expressed in human pancreatic b-cells and in the human pancreas microvasculature, Front Endocrinol,
doi:10.3389/FENDO.2020.596898Fleming, Sacks, Pham, Neoh, Ekinci, An overview of COVID-19 in people with diabetes: Pathophysiology and considerations in the inpatient setting, J Br Diabetic Assoc,
doi:10.1111/DME.14509Hamming, Timens, Bulthuis, Lely, Navis et al., Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis, J Pathol,
doi:10.1002/PATH.1570Harding, Oviedo, Ali, Ofotokun, Gander et al., The bidirectional association between diabetes and long-COVID-19 -A systematic review, Diabetes Res Clin Pract,
doi:10.1016/J.DIABRES.2022.110202Heald, Williams, Jenkins, Stewart, Bakerly et al., The prevalence of long COVID in people with diabetes mellitus-evidence from a UK cohort, EClinicalMedicine,
doi:10.1016/J.ECLINM.2024.102607Hegazy, Lithy, Hamid, Wahba, Ashoush et al., COVID-19 disease outcomes: does gastrointestinal burden play a role?, Clin Exp Gastroenterol,
doi:10.2147/CEG.S297428Khunti, Prato, Mathieu, Kahn, Gabbay et al., COVID-19, hyperglycemia, and new-onset diabetes, Diabetes Care,
doi:10.2337/DC21-1318Kirbišs, Sobotkiewicz, Schaubach, Zavrsňik, Kokol et al., The effects of diabetes and being overweight on patients with post-COVID-19 syndrome, Infect Dis Rep,
doi:10.3390/IDR15060067Kumar, Sridhar, Nair, Banurekha, Nutman et al., Type 2 diabetes mellitus is associated with altered CD8(+) T and natural killer cell function in pulmonary tuberculosis, Immunology,
doi:10.1111/IMM.12421Lai, Yang, Sun, Pan, Wang et al., Risk of incident diabetes after COVID-19 infection: A systematic review and meta-analysis, Metabolism: Clin Exp,
doi:10.1016/J.METABOL.2022.155330Lemhöfer, Bahmer, Baumbach, Besteher, Boekel et al., Variations and predictors of post-COVID syndrome severity in patients attending a post-COVID outpatient clinic, J Clin Med,
doi:10.3390/JCM12124013Li, Zhou, Ma, Zhang, Shao et al., The long-term health outcomes, pathophysiological mechanisms and multidisciplinary management of long COVID, Signal transduction targeted Ther,
doi:10.1038/S41392-023-01640-ZLima-Martıńez, Boada, Madera-Silva, Marıń, Contreras, COVID-19 and diabetes: A bidirectional relationship, Clinica e investigacion en arteriosclerosis: publicacion oficial la Sociedad Espanola Arterioscler,
doi:10.1016/J.ARTERI.2020.10.001Maglietta, Diodati, Puntoni, Lazzarelli, Marcomini et al., Prognostic factors for post-COVID-19 syndrome: A systematic review and metaanalysis, J Clin Med,
doi:10.3390/JCM11061541Marushchak, Kozak, Krynytska, Comorbid overweight/obesity and chronic pancreatitis exacerbate the dyslipidemia progression in type 2 diabetic patients, Endocrine Regulations,
doi:10.2478/enr-2022-0018Matviichuk, Yerokhovych, Ilkiv, Krasnienkov, Korcheva et al., HbA1c and leukocyte mtDNA levels as major factors associated with post-COVID-19 syndrome in type 2 diabetes patients, Sci Rep,
doi:10.1038/S41598-024-77496-2Mittal, Ghosh, Bhatt, Anoop, Ansari et al., High prevalence of post COVID-19 fatigue in patients with type 2 diabetes: A case-control study, Diabetes Metab syndrome,
doi:10.1016/j.dsx.2021.102302Moustafa, Jackson, Brotman, Guan, Villicaña et al., ACE2 expression in adipose tissue is associated with cardio-metabolic risk factors and cell type composition-implications for COVID-19, Int J Obes,
doi:10.1038/S41366-022-01136-WMykhalchyshyn, Kobyliak, Bodnar, Diagnostic accuracy of acyl-ghrelin and it association with non-alcoholic fatty liver disease in type 2 diabetic patients, J Diabetes Metab Disord,
doi:10.1186/s40200-015-0170-1Müller, Groß, Conzelmann, Krüger, Merle et al., SARS-CoV-2 infects and replicates in cells of the human endocrine and exocrine pancreas, Nat Metab,
doi:10.1038/S42255-021-00347-1Nassar, Abosheaishaa, Singh, Misra, Bloomgarden, Noninsulinbased antihyperglycemic medications in patients with diabetes and COVID-19: A systematic review and meta-analysis, J Diabetes,
doi:10.1111/1753-0407.13359Nazari, Pozzilli, Type 2 diabetes and Covid-19: Lessons learnt, unanswered questions and hints for the future, Diabetes Res Clin Pract,
doi:10.1016/J.DIABRES.2023.110896Nguyen, Ho, Nguyen, Ho, Li et al., Preadmission use of antidiabetic medications and mortality among patients with COVID-19 having type 2 diabetes: A meta-analysis, Metabolism: Clin Exp,
doi:10.1016/J.METABOL.2022.155196Ong, Stafford, Mclaughlin, Boyko, Vollset et al., Global, regional, and national burden of diabetes from 1990 to 2021, with projections of prevalence to 2050: a systematic analysis for the Global Burden of Disease Study, Lancet,
doi:10.1016/S0140-6736(23)01301-6Petakh, Kobyliak, Kamyshnyi, Gut microbiota in patients with COVID-19 and type 2 diabetes: A culture-based method, Front Cell infection Microbiol,
doi:10.3389/FCIMB.2023.1142578Peŕez-Belmonte, Torres-Peña, Loṕez-Carmona, Ayala-Gutieŕrez, Fuentes-Jimeńez et al., Mortality and other adverse outcomes in patients with type 2 diabetes mellitus admitted for COVID-19 in association with glucose-lowering drugs: a nationwide cohort study, BMC Med,
doi:10.1186/S12916-020-01832-2Pons, Fodil, Azoulay, Zafrani, The vascular endothelium: the cornerstone of organ dysfunction in severe SARS-CoV-2 infection, Crit Care,
doi:10.1186/S13054-020-03062-7Primorac, Vrdoljak, Brlek, Paveliće, Molnar et al., Adaptive immune responses and immunity to SARS-coV-2, Front Immunol,
doi:10.3389/FIMMU.2022.848582Rajpal, Rahimi, Ismail-Beigi, Factors leading to high morbidity and mortality of COVID-19 in patients with type 2 diabetes, J Diabetes,
doi:10.1111/1753-0407.13085Raveendran, Misra, Post COVID-19 syndrome ("Long COVID") and diabetes: challenges in diagnosis and management, Diabetes Metab syndrome,
doi:10.1016/J.DSX.2021.102235S ̌estan, Marinovićs, Kavazovići, Cekinovićđ, Wueest et al., Virus-induced interferon-g Causes insulin resistance in skeletal muscle and derails glycemic control in obesity, Immunity,
doi:10.1016/J.IMMUNI.2018.05.005Sharma, Tiwari, Deb, Marty, Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2): a global pandemic and treatment strategies, Int J antimicrobial Agents,
doi:10.1016/J.IJANTIMICAG.2020.106054Sherif, Gomez, Connors, Henrich, Reeves, Pathogenic mechanisms of post-acute sequelae of SARS-CoV-2 infection (PASC), eLife,
doi:10.7554/ELIFE.86002Souza, Buzzetti, Pozzilli, Diabetes, COVID-19, and questions unsolved, Diabetes/metabolism Res Rev,
doi:10.1002/DMRR.3666Steenblock, Hassanein, Khan, Yaman, Kamel et al., Diabetes and COVID-19: short-and long-term consequences, Hormone Metab Res = Hormon-und Stoffwechselforschung = Hormones metabolisme,
doi:10.1055/A-1878-9566Sulaieva, Dudin, Botsun, Pischanska, Karpachova et al., The detrimental consequences of two consecutive disasters impacting cytopathology in Ukraine: COVID followed by the war, Cytopathology: Off J Br Soc Clin Cytology,
doi:10.1111/CYT.13236Tsai, Clemente-Casares, Zhou, Lei, Ahn et al., Insulin receptor-mediated stimulation boosts T cell immunity during inflammation and infection, Cell Metab,
doi:10.1016/J.CMET.2018.08.003Turk Wensveen, Gasparini, Rahelićd, Wensveen, Type 2 diabetes and viral infection; cause and effect of disease, Diabetes Res Clin Pract,
doi:10.1016/J.DIABRES.2020.108637Vigili De Kreutzenberg, Long COVID-19 and diabetes mellitus: a short review, Metab Target Organ Damage,
doi:10.20517/MTOD.2022.30Wise, Metformin reduces the risk of developing long term symptoms by 40%, study finds, BMJ (Clinical Res ed),
doi:10.1136/BMJ.P1306Wu, He, Bennett, Li, Chan, Shared genetic mechanism between type 2 diabetes and COVID-19 using pathway-based association analysis, Front Genet,
doi:10.3389/FGENE.2022.1063519Wu, Lidsky, Lee, Cheng, Nakayama, SARS-CoV-2 infects human pancreatic b cells and elicits b cell impairment, Cell Metab,
doi:10.1016/J.CMET.2021.05.013Wu, Zhang, Sun, Wang, Xu et al., Influence of diabetes mellitus on the severity and fatality of SARS-CoV-2 (COVID-19) infection, Diabetes Obes Metab,
doi:10.1111/DOM.14105Yang, Han, Nilsson-Payant, Gupta, Wang et al., A human pluripotent stem cell-based platform to study SARS-coV-2 tropism and model virus infection in human cells and organoids, Cell Stem Cell,
doi:10.1016/J.STEM.2020.06.015Yin, Rohli, Shen, Lu, Liu et al., The epidemiology, pathophysiological mechanisms, and management toward COVID-19 patients with Type 2 diabetes: A systematic review, Primary Care Diabetes,
doi:10.1016/J.PCD.2021.08.014Yousri, Suhre, Yassin, Al-Shakaki, Robay et al., Metabolic and metabo-clinical signatures of type 2 diabetes, obesity, retinopathy, and dyslipidemia, Diabetes,
doi:10.2337/db21-0490Zemni, Gara, Bennasrallah, Ezzar, Kacem et al., Incidence and risk factors of post COVID-19 syndrome: a Tunisian cohort study, BMC Infect Dis,
doi:10.1186/S12879-023-08949-8{ 'indexed': { 'date-parts': [[2024, 12, 12]],
'date-time': '2024-12-12T05:18:20Z',
'timestamp': 1733980700574,
'version': '3.30.2'},
'reference-count': 66,
'publisher': 'Frontiers Media SA',
'license': [ { 'start': { 'date-parts': [[2024, 12, 11]],
'date-time': '2024-12-11T00:00:00Z',
'timestamp': 1733875200000},
'content-version': 'vor',
'delay-in-days': 0,
'URL': 'https://creativecommons.org/licenses/by/4.0/'}],
'funder': [ { 'DOI': '10.13039/100018227',
'name': 'National Research Foundation of Ukraine',
'doi-asserted-by': 'publisher',
'id': [{'id': '10.13039/100018227', 'id-type': 'DOI', 'asserted-by': 'publisher'}]}],
'content-domain': {'domain': ['frontiersin.org'], 'crossmark-restriction': True},
'abstract': '<jats:sec><jats:title>Introduction</jats:title><jats:p>Post-COVID-19 syndrome (PCS) is a '
'severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection-associated chronic '
'condition characterized by long-term violations of physical and mental health. People with '
'type 2 diabetes (T2D) are at high risk for severe COVID-19 and '
'PCS.</jats:p></jats:sec><jats:sec><jats:title>Aim</jats:title><jats:p>The current study aimed '
'to define the predictors of PCS development in people with T2D for further planning of '
'preventive measures and improving patient '
'outcomes.</jats:p></jats:sec><jats:sec><jats:title>Materials and '
'methods</jats:title><jats:p>The data were collected through the national survey targeting '
'persons with T2D concerning the history of COVID-19 course and signs and symptoms that '
'developed during or after COVID-19 and continued for more than 12 weeks and were not '
'explained by an alternative diagnosis. In total, 469 patients from different regions of '
'Ukraine were enrolled in the study. Among them, 227 patients reported PCS development (main '
'group), while 242 patients did not claim PCS symptoms (comparison group). Stepwise '
'multivariate logistic regression and probabilistic neural network (PNN) models were used to '
'select independent risk '
'factors.</jats:p></jats:sec><jats:sec><jats:title>Results</jats:title><jats:p>Based on the '
'survey data, 8 independent factors associated with the risk of PCS development in T2D '
'patients were selected: newly diagnosed T2D (OR 4.86; 95% CI 2.55–9.28; p&lt;0.001), '
'female sex (OR 1.29; 95% CI 0.86–1.94; p=0.220), COVID-19 severity (OR 1.35 95% CI 1.05–1.70; '
'p=0.018), myocardial infarction (OR 2.42 95% CI 1.26–4.64; p=0.002) and stroke (OR 3.68 95% '
'CI 1.70–7.96; p=0.001) in anamnesis, HbA1c above 9.2% (OR 2.17 95% CI 1.37–3.43; p=0.001), '
'and the use of insulin analogs (OR 2.28 95% CI 1.31–3.94; p=0.003) vs human insulin (OR 0.67 '
'95% CI 0.39–1.15; p=0.146). Although obesity aggravated COVID-19 severity, it did not impact '
'PCS development. In ROC analysis, the 8-factor multilayer perceptron (MLP) model exhibited '
'better performance (AUC 0.808; 95% CІ 0.770–0.843), allowing the prediction of the risk of '
'PCS development with a sensitivity of 71.4%, specificity of 76%, PPV of 73.6% and NPV of '
'73.9%.</jats:p></jats:sec><jats:sec><jats:title>Conclusions</jats:title><jats:p>Patients who '
'were newly diagnosed with T2D, had HbA1c above 9.2%, had previous cardiovascular or '
'cerebrovascular events, and had severe COVID-19 associated with mechanical lung ventilation '
'were at high risk for PCS.</jats:p></jats:sec>',
'DOI': '10.3389/fendo.2024.1459171',
'type': 'journal-article',
'created': { 'date-parts': [[2024, 12, 11]],
'date-time': '2024-12-11T05:18:00Z',
'timestamp': 1733894280000},
'update-policy': 'https://doi.org/10.3389/crossmark-policy',
'source': 'Crossref',
'is-referenced-by-count': 0,
'title': 'Unveiling risk factors for post-COVID-19 syndrome development in people with type 2 diabetes',
'prefix': '10.3389',
'volume': '15',
'author': [ {'given': 'Anton', 'family': 'Matviichuk', 'sequence': 'first', 'affiliation': []},
{'given': 'Viktoriia', 'family': 'Yerokhovych', 'sequence': 'additional', 'affiliation': []},
{'given': 'Sergii', 'family': 'Zemskov', 'sequence': 'additional', 'affiliation': []},
{'given': 'Yeva', 'family': 'Ilkiv', 'sequence': 'additional', 'affiliation': []},
{'given': 'Vitalii', 'family': 'Gurianov', 'sequence': 'additional', 'affiliation': []},
{'given': 'Zlatoslava', 'family': 'Shaienko', 'sequence': 'additional', 'affiliation': []},
{'given': 'Tetyana', 'family': 'Falalyeyeva', 'sequence': 'additional', 'affiliation': []},
{'given': 'Oksana', 'family': 'Sulaieva', 'sequence': 'additional', 'affiliation': []},
{'given': 'Nazarii', 'family': 'Kobyliak', 'sequence': 'additional', 'affiliation': []}],
'member': '1965',
'published-online': {'date-parts': [[2024, 12, 11]]},
'reference': [ { 'key': 'B1',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/S0140-6736(23)01301-6',
'article-title': 'Global, regional, and national burden of diabetes from 1990 to 2021, '
'with projections of prevalence to 2050: a systematic analysis for the '
'Global Burden of Disease Study 2021',
'volume': '402',
'author': 'Ong',
'year': '2023',
'journal-title': 'Lancet (London England)'},
{ 'key': 'B2',
'doi-asserted-by': 'publisher',
'first-page': '184',
'DOI': '10.2337/db21-0490',
'article-title': 'Metabolic and metabo-clinical signatures of type 2 diabetes, obesity, '
'retinopathy, and dyslipidemia',
'volume': '71',
'author': 'Yousri',
'year': '2022',
'journal-title': 'Diabetes'},
{ 'key': 'B3',
'doi-asserted-by': 'publisher',
'DOI': '10.2478/enr-2022-0018',
'article-title': 'Comorbid overweight/obesity and chronic pancreatitis exacerbate the '
'dyslipidemia progression in type 2 diabetic patients',
'volume': '56',
'author': 'Marushchak',
'year': '2022',
'journal-title': 'Endocrine Regulations'},
{ 'key': 'B4',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.IJANTIMICAG.2020.106054',
'article-title': 'Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2): a global '
'pandemic and treatment strategies',
'volume': '56',
'author': 'Sharma',
'year': '2020',
'journal-title': 'Int J antimicrobial Agents'},
{ 'key': 'B5',
'doi-asserted-by': 'publisher',
'DOI': '10.1111/CYT.13236',
'article-title': 'The detrimental consequences of two consecutive disasters impacting '
'cytopathology in Ukraine: COVID followed by the war',
'volume': '34',
'author': 'Sulaieva',
'year': '2023',
'journal-title': 'Cytopathology: Off J Br Soc Clin Cytology'},
{ 'key': 'B6',
'doi-asserted-by': 'publisher',
'DOI': '10.3389/FIMMU.2023.1069894',
'article-title': 'Efficacy of interferon alpha for the treatment of hospitalized patients '
'with COVID-19: A meta-analysis',
'volume': '14',
'author': 'Buchynskyi',
'year': '2023',
'journal-title': 'Front Immunol'},
{ 'key': 'B7',
'doi-asserted-by': 'publisher',
'DOI': '10.3389/FENDO.2023.1167087',
'article-title': 'Post-COVID-19 syndrome and diabetes mellitus: a propensity-matched '
'analysis of the International HOPE-II COVID-19 Registry',
'volume': '14',
'author': 'Abumayyaleh',
'year': '2023',
'journal-title': 'Front Endocrinol'},
{ 'key': 'B8',
'doi-asserted-by': 'publisher',
'DOI': '10.3389/FCIMB.2023.1142578',
'article-title': 'Gut microbiota in patients with COVID-19 and type 2 diabetes: A '
'culture-based method',
'volume': '13',
'author': 'Petakh',
'year': '2023',
'journal-title': 'Front Cell infection Microbiol'},
{ 'key': 'B9',
'doi-asserted-by': 'publisher',
'DOI': '10.1002/JMV.28100',
'article-title': 'Bidirectional causal associations between type 2 diabetes and COVID-19',
'volume': '95',
'author': 'Cao',
'year': '2023',
'journal-title': 'J Med Virol'},
{ 'key': 'B10',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.METABOL.2021.154814',
'article-title': 'Diabetes and COVID-19: The past, the present, and the future',
'volume': '121',
'author': 'Pranata',
'year': '2021',
'journal-title': 'Metabolism: Clin Exp'},
{ 'key': 'B11',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.DIABRES.2023.110896',
'article-title': 'Type 2 diabetes and Covid-19: Lessons learnt, unanswered questions and '
'hints for the future',
'volume': '204',
'author': 'Nazari',
'year': '2023',
'journal-title': 'Diabetes Res Clin Pract'},
{ 'key': 'B12',
'doi-asserted-by': 'publisher',
'first-page': '895',
'DOI': '10.1111/1753-0407.13085',
'article-title': 'Factors leading to high morbidity and mortality of COVID-19 in patients '
'with type 2 diabetes',
'volume': '12',
'author': 'Rajpal',
'year': '2020',
'journal-title': 'J Diabetes'},
{ 'key': 'B13',
'doi-asserted-by': 'publisher',
'first-page': '899',
'DOI': '10.1016/J.PCD.2021.08.014',
'article-title': 'The epidemiology, pathophysiological mechanisms, and management toward '
'COVID-19 patients with Type 2 diabetes: A systematic review',
'volume': '15',
'author': 'Yin',
'year': '2021',
'journal-title': 'Primary Care Diabetes'},
{ 'key': 'B14',
'doi-asserted-by': 'publisher',
'DOI': '10.3389/FGENE.2022.1063519',
'article-title': 'Shared genetic mechanism between type 2 diabetes and COVID-19 using '
'pathway-based association analysis',
'volume': '13',
'author': 'Wu',
'year': '2022',
'journal-title': 'Front Genet'},
{ 'key': 'B15',
'doi-asserted-by': 'publisher',
'DOI': '10.2337/DC21-1318',
'article-title': 'COVID-19, hyperglycemia, and new-onset diabetes',
'volume': '44',
'author': 'Khunti',
'year': '2021',
'journal-title': 'Diabetes Care'},
{ 'key': 'B16',
'doi-asserted-by': 'publisher',
'DOI': '10.1210/CLINEM/DGAD284',
'article-title': 'New-onset diabetes after COVID-19',
'volume': '108',
'author': 'Kim',
'year': '2023',
'journal-title': 'J Clin Endocrinol Metab'},
{ 'key': 'B17',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/j.dsx.2021.102302',
'article-title': 'High prevalence of post COVID-19 fatigue in patients with type 2 '
'diabetes: A case-control study',
'volume': '15',
'author': 'Mittal',
'year': '2021',
'journal-title': 'Diabetes Metab syndrome'},
{ 'key': 'B18',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.DSX.2021.102235',
'article-title': 'Post COVID-19 syndrome (“Long COVID”) and diabetes: challenges in '
'diagnosis and management',
'volume': '15',
'author': 'Raveendran',
'year': '2021',
'journal-title': 'Diabetes Metab syndrome'},
{ 'key': 'B19',
'doi-asserted-by': 'publisher',
'first-page': '25533',
'DOI': '10.1038/S41598-024-77496-2',
'article-title': 'HbA1c and leukocyte mtDNA levels as major factors associated with '
'post-COVID-19 syndrome in type 2 diabetes patients',
'volume': '14',
'author': 'Matviichuk',
'year': '2024',
'journal-title': 'Sci Rep'},
{'key': 'B20', 'unstructured': 'Post COVID-19 condition'},
{ 'key': 'B21',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/S2213-8587(22)00044-4',
'article-title': 'Risks and burdens of incident diabetes in long COVID: a cohort study',
'volume': '10',
'author': 'Xie',
'year': '2022',
'journal-title': 'Lancet Diabetes Endocrinol'},
{ 'key': 'B22',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.DIABRES.2022.110202',
'article-title': 'The bidirectional association between diabetes and long-COVID-19 - A '
'systematic review',
'volume': '195',
'author': 'Harding',
'year': '2023',
'journal-title': 'Diabetes Res Clin Pract'},
{ 'key': 'B23',
'doi-asserted-by': 'publisher',
'DOI': '10.3390/IDR15060067',
'article-title': 'The effects of diabetes and being overweight on patients with '
'post-COVID-19 syndrome',
'volume': '15',
'author': 'Kirbiš',
'year': '2023',
'journal-title': 'Infect Dis Rep'},
{ 'key': 'B24',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.METABOL.2022.155330',
'article-title': 'Risk of incident diabetes after COVID-19 infection: A systematic review '
'and meta-analysis',
'volume': '137',
'author': 'Lai',
'year': '2022',
'journal-title': 'Metabolism: Clin Exp'},
{'key': 'B25', 'unstructured': 'Clinical management of COVID-19'},
{ 'key': 'B26',
'doi-asserted-by': 'publisher',
'first-page': '199',
'DOI': '10.2147/CEG.S297428',
'article-title': 'COVID-19 disease outcomes: does gastrointestinal burden play a role',
'volume': '14',
'author': 'Hegazy',
'year': '2021',
'journal-title': 'Clin Exp Gastroenterol'},
{ 'key': 'B27',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.MOLMET.2022.101642',
'article-title': 'Adipose tissue macrophages: Regulators of adipose tissue '
'immunometabolism during obesity',
'volume': '66',
'author': 'Nance',
'year': '2022',
'journal-title': 'Mol Metab'},
{ 'key': 'B28',
'doi-asserted-by': 'publisher',
'DOI': '10.1038/S41366-022-01136-W',
'article-title': 'ACE2 expression in adipose tissue is associated with cardio-metabolic '
'risk factors and cell type composition-implications for COVID-19',
'volume': '46',
'author': 'El-Sayed Moustafa',
'year': '2022',
'journal-title': 'Int J Obes (2005)'},
{ 'key': 'B29',
'doi-asserted-by': 'publisher',
'DOI': '10.1186/s40200-015-0170-1',
'article-title': 'Diagnostic accuracy of acyl-ghrelin and it association with '
'non-alcoholic fatty liver disease in type 2 diabetic patients',
'volume': '14',
'author': 'Mykhalchyshyn',
'year': '2015',
'journal-title': 'J Diabetes Metab Disord'},
{ 'key': 'B30',
'doi-asserted-by': 'publisher',
'DOI': '10.1002/DMRR.3666',
'article-title': 'Diabetes, COVID-19, and questions unsolved',
'volume': '39',
'author': 'D’Souza',
'year': '2023',
'journal-title': 'Diabetes/metabolism Res Rev'},
{ 'key': 'B31',
'doi-asserted-by': 'publisher',
'DOI': '10.3390/JCM11061541',
'article-title': 'Prognostic factors for post-COVID-19 syndrome: A systematic review and '
'meta-analysis',
'volume': '11',
'author': 'Maglietta',
'year': '2022',
'journal-title': 'J Clin Med'},
{ 'key': 'B32',
'doi-asserted-by': 'publisher',
'DOI': '10.3390/JCM12124013',
'article-title': 'Variations and predictors of post-COVID syndrome severity in patients '
'attending a post-COVID outpatient clinic',
'volume': '12',
'author': 'Lemhöfer',
'year': '2023',
'journal-title': 'J Clin Med'},
{ 'key': 'B33',
'doi-asserted-by': 'publisher',
'first-page': '461',
'DOI': '10.1186/S12879-023-08949-8',
'article-title': 'Incidence and risk factors of post COVID-19 syndrome: a Tunisian cohort '
'study',
'volume': '24',
'author': 'Zemni',
'year': '2024',
'journal-title': 'BMC Infect Dis'},
{ 'key': 'B34',
'doi-asserted-by': 'publisher',
'DOI': '10.2337/DB21-0329',
'article-title': 'Diabetes and the risk of long-term post-COVID symptoms',
'volume': '70',
'author': 'Fernóandez-De-las-Penas',
'year': '2021',
'journal-title': 'Diabetes'},
{ 'key': 'B35',
'doi-asserted-by': 'publisher',
'first-page': '86',
'DOI': '10.1111/1753-0407.13359',
'article-title': 'Noninsulin-based antihyperglycemic medications in patients with '
'diabetes and COVID-19: A systematic review and meta-analysis',
'volume': '15',
'author': 'Nassar',
'year': '2023',
'journal-title': 'J Diabetes'},
{ 'key': 'B36',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.METABOL.2022.155196',
'article-title': 'Preadmission use of antidiabetic medications and mortality among '
'patients with COVID-19 having type 2 diabetes: A meta-analysis',
'volume': '131',
'author': 'Nguyen',
'year': '2022',
'journal-title': 'Metabolism: Clin Exp'},
{ 'key': 'B37',
'doi-asserted-by': 'publisher',
'first-page': '7227',
'DOI': '10.1038/S41598-024-57871-9',
'article-title': 'Association of anti-diabetic drugs and COVID-19 outcomes in patients '
'with diabetes mellitus type 2 and cardiomyopathy',
'volume': '14',
'author': 'Dimnjaković',
'year': '2024',
'journal-title': 'Sci Rep'},
{ 'key': 'B38',
'doi-asserted-by': 'publisher',
'first-page': '359',
'DOI': '10.1186/S12916-020-01832-2',
'article-title': 'Mortality and other adverse outcomes in patients with type 2 diabetes '
'mellitus admitted for COVID-19 in association with glucose-lowering '
'drugs: a nationwide cohort study',
'volume': '18',
'author': 'Pérez-Belmonte',
'year': '2020',
'journal-title': 'BMC Med'},
{ 'key': 'B39',
'doi-asserted-by': 'publisher',
'DOI': '10.1080/14656566.2023.2215385',
'article-title': 'Metformin as a potential treatment for COVID-19',
'volume': '24',
'author': 'MCCarthy',
'year': '2023',
'journal-title': 'Expert Opin pharmacotherapy'},
{ 'key': 'B40',
'doi-asserted-by': 'publisher',
'first-page': 'p1306',
'DOI': '10.1136/BMJ.P1306',
'article-title': 'Covid-19: Metformin reduces the risk of developing long term symptoms '
'by 40%, study finds',
'volume': '381',
'author': 'Wise',
'year': '2023',
'journal-title': 'BMJ (Clinical Res ed)'},
{ 'key': 'B41',
'doi-asserted-by': 'publisher',
'DOI': '10.58347/TML.2023.1677E',
'article-title': 'COVID-19 update: Metformin to prevent long COVID',
'volume': '65',
'year': '2023',
'journal-title': 'Med letter Drugs Ther'},
{ 'key': 'B42',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/S1473-3099(23)00299-2',
'article-title': 'Outpatient treatment of COVID-19 and incidence of post-COVID-19 '
'condition over 10 months (COVID-OUT): a multicentre, randomised, '
'quadruple-blind, parallel-group, phase 3 trial',
'volume': '23',
'author': 'Bramante',
'year': '2023',
'journal-title': 'Lancet Infect Dis'},
{ 'key': 'B43',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.ARTERI.2020.10.001',
'article-title': 'COVID-19 and diabetes: A bidirectional relationship',
'volume': '33',
'author': 'Lima-Martínez',
'year': '2021',
'journal-title': 'Clinica e investigacion en arteriosclerosis: publicacion oficial la '
'Sociedad Espanola Arterioscler'},
{ 'key': 'B44',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.ECLINM.2024.102607',
'article-title': 'The prevalence of long COVID in people with diabetes mellitus-evidence '
'from a UK cohort',
'volume': '71',
'author': 'Heald',
'year': '2024',
'journal-title': 'EClinicalMedicine'},
{ 'key': 'B45',
'doi-asserted-by': 'publisher',
'DOI': '10.1111/DOM.14105',
'article-title': 'Influence of diabetes mellitus on the severity and fatality of '
'SARS-CoV-2 (COVID-19) infection',
'volume': '22',
'author': 'Wu',
'year': '2020',
'journal-title': 'Diabetes Obes Metab'},
{ 'key': 'B46',
'doi-asserted-by': 'publisher',
'DOI': '10.1055/A-1878-9566',
'article-title': 'Diabetes and COVID-19: short- and long-term consequences',
'volume': '54',
'author': 'Steenblock',
'year': '2022',
'journal-title': 'Hormone Metab Res = Hormon- und Stoffwechselforschung = Hormones '
'metabolisme'},
{ 'key': 'B47',
'doi-asserted-by': 'publisher',
'DOI': '10.3389/FIMMU.2022.848582',
'article-title': 'Adaptive immune responses and immunity to SARS-coV-2',
'volume': '13',
'author': 'Primorac',
'year': '2022',
'journal-title': 'Front Immunol'},
{ 'key': 'B48',
'doi-asserted-by': 'publisher',
'DOI': '10.1111/DME.14509',
'article-title': 'An overview of COVID-19 in people with diabetes: Pathophysiology and '
'considerations in the inpatient setting',
'volume': '38',
'author': 'Fleming',
'year': '2021',
'journal-title': 'Diabetic medicine: J Br Diabetic Assoc'},
{ 'key': 'B49',
'doi-asserted-by': 'publisher',
'DOI': '10.3389/FGENE.2021.637945',
'article-title': 'Novel reclassification of adult diabetes is useful to distinguish '
'stages of β-cell function linked to the risk of vascular complications: '
'the DOLCE study from northern Ukraine',
'volume': '12',
'author': 'Fedotkina',
'year': '2021',
'journal-title': 'Front Genet'},
{ 'key': 'B50',
'doi-asserted-by': 'publisher',
'DOI': '10.2337/DBI20-0032',
'article-title': 'COVID-19 and diabetes: A collision and collusion of two diseases',
'volume': '69',
'author': 'Feldman',
'year': '2020',
'journal-title': 'Diabetes'},
{ 'key': 'B51',
'doi-asserted-by': 'publisher',
'DOI': '10.1016/J.DIABRES.2020.108637',
'article-title': 'Type 2 diabetes and viral infection; cause and effect of disease',
'volume': '172',
'author': 'Turk Wensveen',
'year': '2021',
'journal-title': 'Diabetes Res Clin Pract'},
{ 'key': 'B52',
'doi-asserted-by': 'publisher',
'first-page': '922',
'DOI': '10.1016/J.CMET.2018.08.003',
'article-title': 'Insulin receptor-mediated stimulation boosts T cell immunity during '
'inflammation and infection',
'volume': '28',
'author': 'Tsai',
'year': '2018',
'journal-title': 'Cell Metab'},
{ 'key': 'B53',
'doi-asserted-by': 'publisher',
'first-page': '164',
'DOI': '10.1016/J.IMMUNI.2018.05.005',
'article-title': 'Virus-induced interferon-γ Causes insulin resistance in skeletal muscle '
'and derails glycemic control in obesity',
'volume': '49',
'author': 'Šestan',
'year': '2018',
'journal-title': 'Immunity'},
{ 'key': 'B54',
'doi-asserted-by': 'publisher',
'DOI': '10.1111/J.1574-695X.1999.TB01397.X',
'article-title': 'Immune dysfunction in patients with diabetes mellitus (DM)',
'volume': '26',
'author': 'Geerlings',
'year': '1999',
'journal-title': 'FEMS Immunol Med Microbiol'},
{ 'key': 'B55',
'doi-asserted-by': 'publisher',
'DOI': '10.1111/IMM.12421',
'article-title': 'Type 2 diabetes mellitus is associated with altered CD8(+) T and '
'natural killer cell function in pulmonary tuberculosis',
'volume': '144',
'author': 'Kumar',
'year': '2015',
'journal-title': 'Immunology'},
{ 'key': 'B56',
'doi-asserted-by': 'publisher',
'first-page': '4',
'DOI': '10.20517/MTOD.2022.30',
'article-title': 'Long COVID-19 and diabetes mellitus: a short review',
'volume': '3',
'author': 'Vigili de Kreutzenberg',
'year': '2023',
'journal-title': 'Metab Target Organ Damage'},
{ 'key': 'B57',
'doi-asserted-by': 'publisher',
'first-page': '416',
'DOI': '10.1038/S41392-023-01640-Z',
'article-title': 'The long-term health outcomes, pathophysiological mechanisms and '
'multidisciplinary management of long COVID',
'volume': '8',
'author': 'Li',
'year': '2023',
'journal-title': 'Signal transduction targeted Ther'},
{ 'key': 'B58',
'doi-asserted-by': 'publisher',
'first-page': '194',
'DOI': '10.1038/S41590-021-01104-Y',
'article-title': 'Pathological sequelae of long-haul COVID',
'volume': '23',
'author': 'Mehandru',
'year': '2022',
'journal-title': 'Nat Immunol'},
{ 'key': 'B59',
'doi-asserted-by': 'publisher',
'DOI': '10.7554/ELIFE.86002',
'article-title': 'Pathogenic mechanisms of post-acute sequelae of SARS-CoV-2 infection '
'(PASC)',
'volume': '12',
'author': 'Sherif',
'year': '2023',
'journal-title': 'eLife'},
{ 'key': 'B60',
'doi-asserted-by': 'publisher',
'first-page': '1565',
'DOI': '10.1016/J.CMET.2021.05.013',
'article-title': 'SARS-CoV-2 infects human pancreatic β cells and elicits β cell '
'impairment',
'volume': '33',
'author': 'Wu',
'year': '2021',
'journal-title': 'Cell Metab'},
{ 'key': 'B61',
'doi-asserted-by': 'publisher',
'first-page': '3',
'DOI': '10.1038/S41575-020-00389-Y',
'article-title': 'COVID-19 and acute pancreatitis: examining the causality',
'volume': '18',
'author': 'de-Madaria',
'year': '2021',
'journal-title': 'Nat Rev Gastroenterol Hepatol'},
{ 'key': 'B62',
'doi-asserted-by': 'publisher',
'DOI': '10.1002/PATH.1570',
'article-title': 'Tissue distribution of ACE2 protein, the functional receptor for SARS '
'coronavirus. A first step in understanding SARS pathogenesis',
'volume': '203',
'author': 'Hamming',
'year': '2004',
'journal-title': 'J Pathol'},
{ 'key': 'B63',
'doi-asserted-by': 'publisher',
'first-page': '353',
'DOI': '10.1186/S13054-020-03062-7',
'article-title': 'The vascular endothelium: the cornerstone of organ dysfunction in '
'severe SARS-CoV-2 infection',
'volume': '24',
'author': 'Pons',
'year': '2020',
'journal-title': 'Crit Care (London England)'},
{ 'key': 'B64',
'doi-asserted-by': 'publisher',
'DOI': '10.3389/FENDO.2020.596898',
'article-title': 'SARS-coV-2 receptor angiotensin I-converting enzyme type 2 (ACE2) is '
'expressed in human pancreatic β-cells and in the human pancreas '
'microvasculature',
'volume': '11',
'author': 'Fignani',
'year': '2020',
'journal-title': 'Front Endocrinol'},
{ 'key': 'B65',
'doi-asserted-by': 'publisher',
'DOI': '10.1038/S42255-021-00347-1',
'article-title': 'SARS-CoV-2 infects and replicates in cells of the human endocrine and '
'exocrine pancreas',
'volume': '3',
'author': 'Müller',
'year': '2021',
'journal-title': 'Nat Metab'},
{ 'key': 'B66',
'doi-asserted-by': 'publisher',
'first-page': '125',
'DOI': '10.1016/J.STEM.2020.06.015',
'article-title': 'A human pluripotent stem cell-based platform to study SARS-coV-2 '
'tropism and model virus infection in human cells and organoids',
'volume': '27',
'author': 'Yang',
'year': '2020',
'journal-title': 'Cell Stem Cell'}],
'container-title': 'Frontiers in Endocrinology',
'original-title': [],
'link': [ { 'URL': 'https://www.frontiersin.org/articles/10.3389/fendo.2024.1459171/full',
'content-type': 'unspecified',
'content-version': 'vor',
'intended-application': 'similarity-checking'}],
'deposited': { 'date-parts': [[2024, 12, 11]],
'date-time': '2024-12-11T05:18:08Z',
'timestamp': 1733894288000},
'score': 1,
'resource': {'primary': {'URL': 'https://www.frontiersin.org/articles/10.3389/fendo.2024.1459171/full'}},
'subtitle': [],
'short-title': [],
'issued': {'date-parts': [[2024, 12, 11]]},
'references-count': 66,
'alternative-id': ['10.3389/fendo.2024.1459171'],
'URL': 'http://dx.doi.org/10.3389/fendo.2024.1459171',
'relation': {},
'ISSN': ['1664-2392'],
'subject': [],
'container-title-short': 'Front. Endocrinol.',
'published': {'date-parts': [[2024, 12, 11]]}}
