Diurnal differences in risk of cardiac arrhythmias during spontaneous hypoglycemia in young people with type 1 diabetes
Abstract
OBJECTIVE Hypoglycemia may exert proarrhythmogenic effects on the heart via sympathoadrenal stimulation and hypokalemia. Hypoglycemia-induced cardiac dysrhythmias are linked to the “dead-in-bed syndrome,” a rare but devastating condition. We examined the effect of nocturnal and daytime clinical hypoglycemia on electrocardiogram (ECG) in young people with type 1 diabetes. RESEARCH DESIGN AND METHODS Thirty-seven individuals with type 1 diabetes underwent 96 h of simultaneous ambulatory ECG and blinded continuous interstitial glucose monitoring (CGM) while symptomatic hypoglycemia was recorded. Frequency of arrhythmias, heart rate variability, and cardiac repolarization were measured during hypoglycemia and compared with time-matched euglycemia during night and day. RESULTS A total of 2,395 h of simultaneous ECG and CGM recordings were obtained; 159 h were designated hypoglycemia and 1,355 h euglycemia. A median duration of nocturnal hypoglycemia of 60 min (interquartile range 40–135) was longer than daytime hypoglycemia of 44 min (30–70) (P = 0.020). Only 24.1% of nocturnal and 51.0% of daytime episodes were symptomatic. Bradycardia was more frequent during nocturnal hypoglycemia compared with matched euglycemia (incident rate ratio [IRR] 6.44 [95% CI 6.26, 6.63], P < 0.001). During daytime hypoglycemia, bradycardia was less frequent (IRR 0.023 [95% CI 0.002, 0.26], P = 0.002) and atrial ectopics more frequent (IRR 2.29 [95% CI 1.19, 4.39], P = 0.013). Prolonged QTc, T-peak to T-end interval duration, and decreased T-wave symmetry were detected during nocturnal and daytime hypoglycemia. CONCLUSIONS Asymptomatic hypoglycemia was common. We identified differences in arrhythmic risk and cardiac repolarization during nocturnal versus daytime hypoglycemia in young adults with type 1 diabetes. Our data provide further evidence that hypoglycemia is proarrhythmogenic.
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A1C has been used as the primary endpoint for many CGM studies.
“A1C is currently recognized as the key surrogate marker for the development of longterm diabetes complications in people with type 1 and type 2 diabetes and has been used the primary endpoint for many CGM studies (1; 3; 4; 6; 32; 33).”
From Clinical Targets for Continuous Glucose Monitoring Data Interpretation: Recommendations From the International Consensus on Time in Range (2019) · cites this paper as [32]
The Baseline Assessment section says HbA1c was measured at the start of this study, while Research Design and Methods identifies arrhythmia-related measures as its outcomes. Searches for A1C as a primary endpoint in CGM studies found no passage in our copy addressing that claim; page numbers were not available. (LLM, conf=0.72)
Experimental — accuracy not yet measuredA1C is currently recognized as the key surrogate marker for the development of long-term diabetes complications in people with type 1 and type 2 diabetes.
“A1C is currently recognized as the key surrogate marker for the development of longterm diabetes complications in people with type 1 and type 2 diabetes and has been used the primary endpoint for many CGM studies (1; 3; 4; 6; 32; 33).”
From Clinical Targets for Continuous Glucose Monitoring Data Interpretation: Recommendations From the International Consensus on Time in Range (2019) · cites this paper as [32]
The Baseline Assessment section says HbA1c was measured at the start of monitoring, but does not describe it as a surrogate marker for long-term complications. The Research Design and Methods section examines arrhythmias during hypoglycemia, not A1C as a primary endpoint in CGM studies. Searches for the surrogate-marker and primary-endpoint claims found no supporting passage in our copy. (LLM, conf=0.76)
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Cites
Heart Rate Variability: Standards of Measurement, Physiological Interpretation, and Clinical Use
Electrophysiology, T. F. O. T. E. S. O. C. T. N. A. (1996) · Circulation · doi:10.1161/01.cir.93.5.1043 · Cited by 17,159 · see citing works
Heart rate variability: Standards of measurement, physiological interpretation, and clinical use
Malik, M., Bigger, J. T., Camm, A. J., Kleiger, R. E., Malliani, A., Moss, A. J., & Schwartz, P. J. (1996) · European Heart Journal · doi:10.1093/oxfordjournals.eurheartj.a014868 · Cited by 15,289 · see citing works
Tesfaye, S., Boulton, A. J. M., Dyck, P. J., Freeman, R., Horowitz, M., Kempler, P., Lauria, G., Malik, R. A., Spallone, V., Vinik, A., et al. (2010) · Diabetes Care · doi:10.2337/dc10-1303 · Cited by 2,690 · see citing works
Montano, N., Ruscone, T. G., Porta, A., Lombardi, F., Pagani, M., & Malliani, A. (1994) · Circulation · doi:10.1161/01.cir.90.4.1826 · Cited by 1,108 · see citing works
Risk of hypoglycaemia in types 1 and 2 diabetes: Effects of treatment modalities and their duration
UK Hypoglycaemia Study Group (2007) · Diabetologia · doi:10.1007/s00125-007-0599-y · Cited by 825 · see citing works
Gold, A. E., Macleod, K. M., & Frier, B. M. (1994) · Diabetes Care · doi:10.2337/diacare.17.7.697 · Cited by 810 · see citing works
Furlan, R., Guzzetti, S., Crivellaro, W., Dassi, S., Tinelli, M., Baselli, G., Cerutti, S., Lombardi, F., Pagani, M., & Malliani, A. (1990) · Circulation · doi:10.1161/01.cir.81.2.537 · Cited by 729 · see citing works
O'Brien, I. A. D., O'Hare, P. J., & Corrall, R. J. M. (1986) · Heart · doi:10.1136/hrt.55.4.348 · Cited by 483 · see citing works
Panikkath, R., Reinier, K., Uy‐Evanado, A., Teodorescu, C., Hattenhauer, J., Mariani, R., Gunson, K., Jui, J., & Chugh, S. S. (2011) · Circulation Arrhythmia and Electrophysiology · doi:10.1161/circep.110.960658 · Cited by 449 · see citing works
Chow, E., Bernjak, A., Williams, S., Fawdry, R. A., Hibbert, S., Freeman, J., Sheridan, P. J., & Heller, S. R. (2014) · Diabetes · doi:10.2337/db13-0468 · Cited by 403 · see citing works
Electrocardiographic quantitation of ventricular repolarization.
Merri, M., Benhorin, J., Alberti, M., Locati, E. H., & Moss, A. J. (1989) · Circulation · doi:10.1161/01.cir.80.5.1301 · Cited by 401 · see citing works
Early afterdepolarizations and cardiac arrhythmias
Weiss, J. N., Garfinkel, A., Karagueuzian, H. S., Chen, P., & Qu, Z. (2010) · Heart Rhythm · doi:10.1016/j.hrthm.2010.09.017 · Cited by 397 · see citing works
Sager, P. T., Nebout, T., & Darpö, B. (2005) · Drug Information Journal · doi:10.1177/009286150503900407 · Cited by 385 · see citing works
Unexplained Deaths of Type 1 Diabetic Patients
Tattersall, R. B., & Gill, G. V. (1991) · Diabetic Medicine · doi:10.1111/j.1464-5491.1991.tb01516.x · Cited by 308 · see citing works
Decreased Epinephrine Responses to Hypoglycemia during Sleep
Jones, T. W., Porter, P., Sherwin, R. S., Davis, E. A., O'Leary, P. C., Frazer, F., Byrne, G. C., Stick, S. M., & Tamborlane, W. V. (1998) · New England Journal of Medicine · doi:10.1056/nejm199806043382303 · Cited by 298 · see citing works
Gill, G. V., Woodward, A., Casson, I. F., & Weston, P. J. (2008) · Diabetologia · doi:10.1007/s00125-008-1177-7 · Cited by 296 · see citing works
Mechanisms of abnormal cardiac repolarization during insulin-induced hypoglycemia
Robinson, R. T. C. E., Harris, N. D., Ireland, R. H., Lee, S., Newman, C., & Heller, S. R. (2003) · Diabetes · doi:10.2337/diabetes.52.6.1469 · Cited by 264 · see citing works
Frequency and Morbidity of Severe Hypoglycaemia in Insulin‐treated Diabetic Patients
MacLeod, K. M., Hepburn, D. A., & Frier, B. M. (1993) · Diabetic Medicine · doi:10.1111/j.1464-5491.1993.tb00051.x · Cited by 250 · see citing works
Glycemic Goals in Diabetes: Trade-off Between Glycemic Control and Iatrogenic Hypoglycemia
Cryer, P. E. (2014) · Diabetes · doi:10.2337/db14-0059 · Cited by 233 · see citing works
Accuracy of the 5-Day FreeStyle Navigator Continuous Glucose Monitoring System
Weinstein, R. L., Schwartz, S. L., Brazg, R., Bugler, J., Peyser, T. A., & McGarraugh, G. V. (2007) · Diabetes Care · doi:10.2337/dc06-1602 · Cited by 228 · see citing works
Tanenberg, R. J., Newton, C. A., & Drake, A. J. (2010) · Endocrine Practice · doi:10.4158/ep09260.cr · Cited by 225 · see citing works
American Diabetes Association (2015) · Diabetes Care · doi:10.2337/dc16-s008 · Cited by 216 · see citing works
Methods of investigation for cardiac autonomic dysfunction in human research studies
Bernardi, L., Spallone, V., Stevens, M. J., Hilsted, J., Frontoni, S., Pop‐Busui, R., Ziegler, D., Kempler, P., Freeman, R. L., Low, P. A., et al. (2011) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.1224 · Cited by 174 · see citing works
Mortality in Childhood-Onset Type 1 Diabetes
Dahlquist, G. G., & Källén, B. A. J. (2005) · Diabetes Care · doi:10.2337/diacare.28.10.2384 · Cited by 157 · see citing works
The case for hypoglycaemia as a proarrhythmic event: basic and clinical evidence
Nordin, C. (2010) · Diabetologia · doi:10.1007/s00125-010-1752-6 · Cited by 143 · see citing works
Robinson, R. T. C. E., Harris, N. D., Ireland, R. H., Macdonald, I. A., & Heller, S. R. (2004) · Diabetologia · doi:10.1007/s00125-003-1292-4 · Cited by 137 · see citing works
Weston, P., & Gill, G. V. (1999) · Diabetic Medicine · doi:10.1046/j.1464-5491.1999.00121.x · Cited by 122 · see citing works
Mortality in childhood-onset type 1 diabetes
Hadzhieva, E., Boyadzhieva, M., Iotova, V., Galcheva, S., Tsochev, Κ., Chalykova, T., Yotov, Y. T., Balev, B. D., Bocheva, Y., Usheva, N., et al. (2019) · Scripta Scientifica Medica · doi:10.14748/ssm.v51i1.5913 · Cited by 112 · see citing works
Dead-in-bed syndrome in young diabetic patients.
Søvik, O., & Thordarson, H. B. (1999) · PubMed · Cited by 97 · see citing works
QT interval analysis on ambulatory electrocardiogram recordings: a selective beat averaging approach
Badilini, F., Maison‐Blanche, P., Childers, R. W., & Coumel, P. (1999) · Medical & Biological Engineering & Computing · doi:10.1007/bf02513269 · Cited by 92 · see citing works
Dead in Bed Syndrome in Young Diabetic Patients in Norway
Thordarson, H. B., & Søvik, O. (1995) · Diabetic Medicine · doi:10.1111/j.1464-5491.1995.tb02080.x · Cited by 86 · see citing works
Influence of Autonomic Neuropathy on QTc Interval Lengthening During Hypoglycemia in Type 1 Diabetes
Lee, S. P., Yeoh, L., Harris, N. D., Davies, C. M., Robinson, R. T. C. E., Leathard, A. D., Newman, C. M. H., Macdonald, I. A., & Heller, S. R. (2004) · Diabetes · doi:10.2337/diabetes.53.6.1535 · Cited by 85 · see citing works
Abnormalities of the electrocardiogram during hypoglycaemia: the cause of the dead in bed syndrome?
Heller, S. R. (2002) · PubMed · Cited by 70 · see citing works
Christensen, T. F., Tarnow, L., Randløv, J., Kristensen, L. E., Struijk, J. J., Eldrup, E., & Hejlesen, O. K. (2010) · Diabetologia · doi:10.1007/s00125-010-1802-0 · Cited by 61 · see citing works
Tu, E., Twigg, S. M., Duflou, J. A., & Semsarian, C. (2008) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.2008.tb01849.x · Cited by 60 · see citing works
Explaining the T-wave shape in the ECG
di Bernardo, D., & Murray, A. (2000) · Nature · doi:10.1038/47409 · Cited by 57 · see citing works
Insulin analogues and severe hypoglycaemia in type 1 diabetes
Kristensen, P. L., Hansen, L., Jespersen, M. J., Pedersen‐Bjergaard, U., Beck‐Nielsen, H., Christiansen, J. S., Nørgaard, K., Perrild, H., Parving, H.-H., Thorsteinsson, B., et al. (2011) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2011.10.046 · Cited by 53 · see citing works
Hypoglycaemia leads to an increased QT interval in normal men
Eckert, B., & Agardh, C. (1998) · Clinical Physiology · doi:10.1046/j.1365-2281.1998.00138.x · Cited by 46 · see citing works
Koivikko, M. L., Tulppo, M. P., Kiviniemi, A. M., Kallio, M., Perkiömäki, J. S., Salmela, P. I., Airaksinen, J. K. E., & Huikuri, H. V. (2012) · Diabetes Care · doi:10.2337/dc11-2120 · Cited by 46 · see citing works
QT Measurement and Heart Rate Correction during Hypoglycemia: Is There a Bias?
Christensen, T. F., Randløv, J., Kristensen, L. E., Eldrup, E., Hejlesen, O. K., & Struijk, J. J. (2010) · Cardiology Research and Practice · doi:10.4061/2010/961290 · Cited by 20 · see citing works
Increased symptoms of hypoglycaemia in the standing position in insulin-dependent diabetes mellitus
Hirsch, I. B., Heller, S. R., & Cryer, P. E. (1991) · Clinical Science · doi:10.1042/cs0800583 · Cited by 17 · see citing works
Marques (1997) · doi:10.1002/(sici)1096-9136(199708)14:8
Flagged first, then by citations
1 of the 43 references couldn’t be matched to a known paper.
Cited by
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Battelino, T., Danne, T., Bergenstal, R. M., Amiel, S. A., Beck, R., Biester, T., Bosi, E., Buckingham, B. A., Cefalu, W. T., Close, K. L., et al. (2019) · Diabetes Care · doi:10.2337/dci19-0028 · Cited by 4,032 · see citing works
Validation of Time in Range as an Outcome Measure for Diabetes Clinical Trials
Beck, R. W., Bergenstal, R. M., Riddlesworth, T. D., Kollman, C., Li, Z., Brown, A. S., & Close, K. L. (2019) · Diabetes Care · doi:10.2337/dc18-1444 · Cited by 793 · see citing works
Amiel, S. A., Aschner, P., Childs, B., Cryer, P. E., de Galan, B. E., Frier, B. M., Gonder-Frederick, L., Heller, S. R., Jones, T., Khunti, K., et al. (2019) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(18)30315-2 · Cited by 526 · see citing works
Abraham, M. B., Jones, T. W., Naranjo, D. M., Karges, B., Oduwole, A. O., Tauschmann, M., & Maahs, D. M. (2018) · Pediatric Diabetes · doi:10.1111/pedi.12698 · Cited by 228 · see citing works
The consequences of hypoglycaemia
Amiel, S. A. (2021) · Diabetologia · doi:10.1007/s00125-020-05366-3 · Cited by 229 · see citing works
Glycemic Monitoring and Management in Advanced Chronic Kidney Disease
Galindo, R. J., Beck, R. W., Scioscia, M. F., Umpierrez, G. E., & Tuttle, K. R. (2020) · Endocrine Reviews · doi:10.1210/endrev/bnaa017 · Cited by 208 · see citing works
Johnson, M. L., Martens, T. W., Criego, A. B., Carlson, A. L., Simonson, G. D., & Bergenstal, R. M. (2019) · Diabetes Technology & Therapeutics · doi:10.1089/dia.2019.0034 · Cited by 104 · see citing works
Realizing a Closed-Loop (Artificial Pancreas) System for the Treatment of Type 1 Diabetes
Lal, R., Ekhlaspour, L., Hood, K. K., & Buckingham, B. A. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00174 · Cited by 97 · see citing works
The risks of nocturnal hypoglycaemia in insulin-treated diabetes
Graveling, A. J., & Frier, B. M. (2017) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2017.08.012 · Cited by 73 · see citing works
Effects of Hypoglycemia on Cardiovascular Function in Patients with Diabetes
Christou, M., Christou, P. A., Kyriakopoulos, C., Christou, G. A., & Tigas, S. K. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24119357 · Cited by 61 · see citing works
Fitzpatrick, C., Chatterjee, S., Seidu, S., Bodicoat, D. H., Ng, G. A., Davies, M. J., & Khunti, K. (2018) · Diabetes, Obesity and Metabolism · doi:10.1111/dom.13348 · Cited by 57 · see citing works
Continuous Glucose Monitoring with Multiple Daily Insulin Treatment: Outcome Studies
McGill, J. B., & Ahmann, A. (2017) · Diabetes Technology & Therapeutics · doi:10.1089/dia.2017.0090 · Cited by 49 · see citing works
Hypoglycaemia and cardiac arrhythmias in diabetes
Andersen, A., Jørgensen, P. G., Knop, F. K., & Vilsbøll, T. (2020) · Therapeutic Advances in Endocrinology and Metabolism · doi:10.1177/2042018820911803 · Cited by 47 · see citing works
Andersen, A., Bagger, J. I., Sørensen, S. K., BALDASSARRE, M. P. A., Pedersen‐Bjergaard, U., Forman, J. L., Gislason, G., Lindhardt, T. B., Knop, F. K., & Vilsbøll, T. (2021) · Cardiovascular Diabetology · doi:10.1186/s12933-021-01425-0 · Cited by 45 · see citing works
Beck, R. W., Bergenstal, R. M., Riddlesworth, T. D., & Kollman, C. (2019) · Diabetes Technology & Therapeutics · doi:10.1089/dia.2018.0362 · Cited by 42 · see citing works
Zaccardi, F., Dhalwani, N. N., Webb, D. R., Davies, M. J., & Khunti, K. K. (2018) · Diabetologia · doi:10.1007/s00125-018-4626-y · Cited by 41 · see citing works
Groener, J. B., Valkanou, A., Κender, Ζ., Pfeiffenberger, J., Kihm, L., Fleming, T. H., Nawroth, P. P., & Kopf, S. (2019) · PLoS ONE · doi:10.1371/journal.pone.0222771 · Cited by 38 · see citing works
Igbe, T., Kandwal, A., Li, J., Yan, Y., Omisore, O. M., Enitan, E., Li, S., Yuhang, L., Wang, L., & Nie, Z. (2020) · Knowledge-Based Systems · doi:10.1016/j.knosys.2020.106464 · Cited by 32 · see citing works
Recent Updates on Type 1 Diabetes Mellitus Management for Clinicians
Iqbal, A., Novodvorský, P., & Heller, S. R. (2018) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2018.42.1.3 · Cited by 33 · see citing works
Gubitosi-Klug, R. A., Braffett, B. H., Bebu, I., Johnson, M. L., Farrell, K., Kenny, D., Trapani, V. R., Meadema-Mayer, L., Soliman, E. Z., Pop-Busui, R., et al. (2022) · Diabetes Care · doi:10.2337/dc21-0629 · Cited by 31 · see citing works
Riddle, M. C., Gerstein, H. C., & Cefalu, W. T. (2017) · Diabetes Care · doi:10.2337/dci17-0049 · Cited by 30 · see citing works
Hypoglycaemia in type 1 diabetes mellitus: risks and practical prevention strategies
Kaur, J., & Seaquist, E. R. (2022) · Nature Reviews Endocrinology · doi:10.1038/s41574-022-00762-8 · Cited by 32 · see citing works
Glucose Homeostasis, Hypoglycemia, and the Burnt-Out Diabetes Phenomenon in Kidney Disease
Rhee, C. M., Kovesdy, C. P., & Kalantar‐Zadeh, K. (2021) · Seminars in Nephrology · doi:10.1016/j.semnephrol.2021.03.004 · Cited by 27 · see citing works
Asymptomatic hypoglycaemia in Type 1 diabetes: incidence and risk factors
Henriksen, M. M., Andersen, H. U., Thorsteinsson, B., & Pedersen‐Bjergaard, U. (2018) · Diabetic Medicine · doi:10.1111/dme.13848 · Cited by 26 · see citing works
Hypoglycemia and Mortality Risk in Incident Hemodialysis Patients
Kang, D., Streja, E., You, A. S., Lee, Y.-K., Narasaki, Y., Rivera, S. T., Novoa-Vargas, A., Kovesdy, C. P., Kalantar‐Zadeh, K., & Rhee, C. M. (2023) · Journal of Renal Nutrition · doi:10.1053/j.jrn.2023.09.001 · Cited by 24 · see citing works
Novel approaches to hypoglycemia and burnt-out diabetes in chronic kidney disease
Rhee, C. M., Kalantar‐Zadeh, K., & Tuttle, K. R. (2021) · Current Opinion in Nephrology & Hypertension · doi:10.1097/mnh.0000000000000756 · Cited by 25 · see citing works
Daskalaki, E., Parkinson, A., Brew‐Sam, N., Hossain, M. Z., O'Neal, D. N., Nolan, C. J., & Suominen, H. (2022) · Journal of Medical Internet Research · doi:10.2196/28901 · Cited by 22 · see citing works
Hallström, S., Pivodic, A., Rosengren, A., Ólafsdóttir, A. F., Svensson, A., & Lind, M. (2019) · Diabetes Care · doi:10.2337/dc18-2457 · Cited by 22 · see citing works
Beck, R. W., & Bergenstal, R. M. (2021) · Diabetes Spectrum · doi:10.2337/ds20-0090 · Cited by 21 · see citing works
Li, G., Zhong, S., Wang, X., & Zhuge, F. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1222409 · Cited by 22 · see citing works
Reno, C. M., Bayles, J., Huang, Y., OXSPRING, M. B., Hirahara, A. M., Dosdall, D. J., & Fisher, S. J. (2019) · Diabetes · doi:10.2337/db19-0306 · Cited by 21 · see citing works
D’Elia, J. A., Mulla, C. M., Liu, J., & Weinrauch, L. A. (2019) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2019.02.015 · Cited by 19 · see citing works
Severe hypoglycemia and incidence of QT interval prolongation among adults with type 2 diabetes
Kaze, A. D., Yuyun, M. F., Erqou, S., Fonarow, G. C., & Echouffo-Tcheugui, J. B. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac195 · Cited by 18 · see citing works
Abdelhamid, Y. A., Bernjak, A., Phillips, L. K., Summers, M. J., Weinel, L. M., Lange, K. M., Chow, E., Kar, P., Horowitz, M., Heller, S. R., et al. (2021) · Critical Care Medicine · doi:10.1097/ccm.0000000000004810 · Cited by 19 · see citing works
Diabetes, Diabetic Complications, and Phosphate Toxicity: A Scoping Review
Brown, R. B. (2019) · Current Diabetes Reviews · doi:10.2174/1573399815666191104113236 · Cited by 17 · see citing works
Bomholt, T., Kofod, D. H., Nørgaard, K., Rossing, P. R., Feldt‐Rasmussen, B., & Hornum, M. (2022) · The Nephron journals/Nephron journals · doi:10.1159/000525676 · Cited by 16 · see citing works
Advanced carbohydrate counting: An engineering perspective
Reiterer, F., & Freckmann, G. (2019) · Annual Reviews in Control · doi:10.1016/j.arcontrol.2019.06.003 · Cited by 16 · see citing works
Hypoglycaemia and Cardiovascular Disease Risk in Patients with Diabetes
Katsiki, N., Kotsa, K., Stoian, A. P., & Mikhailidis, D. P. (2020) · Current Pharmaceutical Design · doi:10.2174/1381612826666200909142658 · Cited by 16 · see citing works
Wei, X., Chang, A. C. H., Chang, H., Xu, S., Xue, Y., Zhang, Y., Lei, M., Chang, A. C. Y., & Zhang, Q. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.800185 · Cited by 15 · see citing works
Pathological basis of cardiac arrhythmias: vicious cycle of immune-metabolic dysregulation
Wang, S. C., Meng, D., Yang, H.-P., Wang, X., Jia, S., Wang, Y., & Wang, P. (2017) · Cardiovascular Disorders and Medicine · doi:10.15761/cdm.1000158 · Cited by 15 · see citing works
Bachmann, S., Auderset, A., Burckhardt, M., Szinnai, G., Hess, M., Zumsteg, U., Denhaerynck, K., & Donner, B. C. (2021) · Pediatric Diabetes · doi:10.1111/pedi.13262 · Cited by 13 · see citing works
Andreasen, C. R., Andersen, A., Hagelqvist, P. G., Maytham, K. B., Lauritsen, J. V., Engberg, S., Faber, J. O., Pedersen‐Bjergaard, U., Knop, F. K., & Vilsbøll, T. (2023) · Diabetes Obesity and Metabolism · doi:10.1111/dom.15005 · Cited by 15 · see citing works
Chen, C., Wang, W., Zhou, W., Jin, J., Chen, W., Zhu, D., & Bi, Y. (2019) · Journal of Diabetes · doi:10.1111/1753-0407.12908 · Cited by 14 · see citing works
Yoo, J. H., Yang, S. H., Jin, S., & Kim, J. H. (2024) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2023.0083 · Cited by 11 · see citing works
Reno, C. M., OXSPRING, M. B., Bayles, J., Huang, E. Y., Holiday, I., & Fisher, S. J. (2022) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00188.2022 · Cited by 11 · see citing works
Zucchini, S., Tumini, S., Scaramuzza, A. E., Bonfanti, R., Delvecchio, M., Franceschi, R., Iafusco, D., Lenzi, L., Mozzillo, E., Passanisi, S., et al. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1387537 · Cited by 10 · see citing works
Glycaemia and cardiac arrhythmias in people with type 1 diabetes: A prospective observational study
Hagelqvist, P. G., Andersen, A., Maytham, K. B., Andreasen, C. R., Engberg, S., Lindhardt, T. B., Forman, J. L., Pedersen‐Bjergaard, U., Knop, F. K., & Vilsbøll, T. (2023) · Diabetes Obesity and Metabolism · doi:10.1111/dom.15108 · Cited by 11 · see citing works
Thomas, A., Shin, J., Jiang, B., McMahon, C., Kolassa, R., & Vigersky, R. A. (2017) · Journal of Diabetes Science and Technology · doi:10.1177/1932296817721242 · Cited by 10 · see citing works
Bernjak, A., Novodvorský, P., Chow, E., Iqbal, A., Sellors, L., Williams, S., Fawdry, R. A., Marques, J. L. B., Jacques, R., Campbell, M. J., et al. (2021) · Diabetes & Metabolism · doi:10.1016/j.diabet.2021.101237 · Cited by 10 · see citing works
Charamba, B., Liew, A., Coen, E., Newell, J., O’Brien, T., Wijns, W. C., & Simpkin, A. J. (2021) · Endocrinology Diabetes & Metabolism · doi:10.1002/edm2.263 · Cited by 10 · see citing works
Uanini, N. (2001) · Dialnet (Universidad de la Rioja) · Cited by 10 · see citing works
Circadian (diurnal/nocturnal) pattern of cardiac arrhythmias
Manolis, A. S., Manolis, A. S., & Manolis, A. S. (2024) · Heart Rhythm · doi:10.1016/j.hrthm.2024.10.013 · Cited by 9 · see citing works
Sleep as a window of cardiometabolic health: The potential of digital sleep and circadian biomarkers
van den Brink, W. J., Oosterman, J. E., Smid, D. J., de Vries, H., Atsma, D. E., Overeem, S., & Wopereis, S. (2025) · Digital Health · doi:10.1177/20552076241288724 · Cited by 8 · see citing works
Bengtsen, M. B., & Møller, N. (2022) · Journal of the Endocrine Society · doi:10.1210/jendso/bvac123 · Cited by 8 · see citing works
The phenomenon of HbA1c stability and the risk of hypoglycemia in long-standing type 1 diabetes
Wolnik, B., Orłowska-Kunikowska, E., Błaszkowska, M., Graff, B., Wolf, J., Czupryniak, L., & Narkiewicz, K. (2019) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2019.05.010 · Cited by 7 · see citing works
Andellini, M., Castaldo, R., Cisuelo, O., Franzese, M., Haleem, M. S., Ritrovato, M., Pecchia, L., & Schiaffini, R. (2024) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2024.111708 · Cited by 6 · see citing works
Kofod, D. H., Diederichsen, S. Z., Bomholt, T., Andersen, M. Ø., Andersen, A., Mannheimer, E. E., Rix, M., Liem, Y. S., Lindhard, K., Hansen, H. P., et al. (2025) · Diabetologia · doi:10.1007/s00125-025-06388-5 · Cited by 6 · see citing works
Frequent hypoglycemia during hemodialysis in ESRD patients leads to higher risk of death
Shi, Y., Wang, T., Ding, Z., Yan, L., Yao, C., & Qian, H. (2025) · Renal Failure · doi:10.1080/0886022x.2025.2484471 · Cited by 6 · see citing works
Glucose variability and predicted cardiovascular risk after gastrectomy
Shibamoto, J., Kubota, T., Ohashi, T., Konishi, H., Shiozaki, A., Fujiwara, H., Okamoto, K. K., & Otsuji, E. (2022) · Surgery Today · doi:10.1007/s00595-022-02496-6 · Cited by 8 · see citing works
Campbell, M. J., Heller, S. R., & Jacques, R. (2018) · Diabetes Care · doi:10.2337/dci17-0067 · Cited by 6 · see citing works
Risk factors for hypoglycaemia in adults with type 1 diabetes: a systematic review and meta-analysis
Zhang, Q. X., Zhou, H., Lin, R., Hu, L., & Zhu, X. (2025) · BMC Endocrine Disorders · doi:10.1186/s12902-025-02122-9 · Cited by 5 · see citing works
Brain Regulation of Cardiac Function during Hypoglycemia
Chambers, M. E., Nuibe, E. H., & Reno, C. M. (2023) · Metabolites · doi:10.3390/metabo13101089 · Cited by 5 · see citing works
Kofod, D. H., Diederichsen, S. Z., Bomholt, T., Andersen, M. Ø., Rix, M., Liem, Y. S., Lindhard, K., Hansen, H. P., Rydahl, C., Lindhardt, M. K., et al. (2023) · BMJ Open · doi:10.1136/bmjopen-2023-077063 · Cited by 5 · see citing works
Ferhatbegović, L., Bećirović, M., Bečirović, E., Sarajlić, S., Ribić, A., Šarić, A., Bećirović, A., & Pojskić, B. (2026) · Frontiers in Clinical Diabetes and Healthcare · doi:10.3389/fcdhc.2026.1765597 · Cited by 4 · see citing works
Ghalati, P. F., Samadi, M. E., Verket, M., Balfanz, P., Müller‐Wieland, D., Jonas, S., Napp, A., Wanner, C., Ketteler, M., Vassiliadou, A., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-81983-x · Cited by 4 · see citing works
Ling, Q., Lü, J., Li, X., Qiao, C., Zhu, D., & Bi, Y. (2020) · Diabetes Therapy · doi:10.1007/s13300-020-00787-0 · Cited by 5 · see citing works
Rončáková, M., Davani, A., Mikušová, V., Ságová, I., Novodvorský, P., & Martinka, E. (2023) · Diabetes Therapy · doi:10.1007/s13300-023-01440-2 · Cited by 4 · see citing works
Hagelqvist, P. G., Andersen, A., Maytham, K. B., Andreasen, C. R., Engberg, S., Lindhardt, T. B., Faber, J. O., Holst, J. J., Forman, J. L., Pedersen‐Bjergaard, U., et al. (2023) · Diabetes Obesity and Metabolism · doi:10.1111/dom.14964 · Cited by 4 · see citing works
Mistry, S., Gouripeddi, R., Reno, C. M., Abdelrahman, S., Fisher, S. J., & Facelli, J. C. (2023) · PLoS ONE · doi:10.1371/journal.pone.0284622 · Cited by 4 · see citing works
Riddle, M. C., & Miller, M. E. (2018) · Diabetes Care · doi:10.2337/dci18-0009 · Cited by 4 · see citing works
A Component-Based Approach for Securing Indoor Home Care Applications
Agirre, A., Armentia, A., Estévez, E., & Marcos, M. (2017) · Sensors · doi:10.3390/s18010046 · Cited by 4 · see citing works
Bernjak, A., Iqbal, A., Heller, S. R., & Clayton, R. H. (2021) · Journal of The Royal Society Interface · doi:10.1098/rsif.2021.0612 · Cited by 4 · see citing works
Novodvorský, P., Bernjak, A., Downs, E., Smith, A., Arshad, M. F., Oprescu, A. I., Jacques, R., Lee, J., Heller, S. R., & Iqbal, A. (2025) · Diabetic Medicine · doi:10.1111/dme.70019 · Cited by 3 · see citing works
Novodvorský, P., Bernjak, A., Robinson, E. J., Iqbal, A., Macdonald, I. A., Jacques, R., Marques, J. L. B., Sheridan, P. J., & Heller, S. R. (2018) · Diabetic Medicine · doi:10.1111/dme.13650 · Cited by 3 · see citing works
Makrilakis, K., Stathi, C., Vlahodimitris, I., Kalopita, S., Thomakos, P., Konstantopoulos, P. S., Perrea, D. N., Katsilambros, Ν., & Liatis, S. (2017) · Diabetes & Metabolism · doi:10.1016/j.diabet.2017.08.005 · Cited by 3 · see citing works
CARDIAC ARRHYTHMIAS IN CERTAIN INTERNAL DISEASES (review)
Иосифович, Ш. И., Genkel, V. V., Kuznetsova, A. S., Lebedev, E. V., & Salashenko, A. O. (2019) · Сибирский научный медицинский журнал · doi:10.15372/ssmj20190504 · Cited by 3 · see citing works
Home, P. D., & Lachin, J. M. (2018) · Diabetes Care · doi:10.2337/dc17-2405 · Cited by 3 · see citing works
Балыкова, Л. А., Владимиров, Д. О., Tyagusheva, E. N., Васильевна, Ш. М., Krasnopolskaya, A. V., & Ивановна, Н. Е. (2025) · Педиатрическая фармакология · doi:10.15690/pf.v22i1.2855 · Cited by 2 · see citing works
Liu, Y., Rao, J., Hu, W., Yu, Y. S., Wang, P., Chen, X., Zhang, Y., & Wang, Z. (2024) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2024.111725 · Cited by 2 · see citing works
Diabetes in Children and Adolescents
Šumnı́k, Z., & Průhová, Š. (2024) · Endocrinology · doi:10.1007/978-3-030-23709-7_10 · Cited by 2 · see citing works
Jenkins, A. J., Kilov, G., SCOTT, E. S., Fulcher, G., O'Neal, D. N., & Januszewski, A. S. (2018) · Madridge Journal of Diabetes · doi:10.18689/mjd-1000111 · Cited by 2 · see citing works
Hypoglycemia: Diagnosis, Management, and Prevention
Faradji, R. N., Uribe-Wiechers, A. C., & Viadero, M. E. S. D. L. M. (2019) · Springer eBooks · doi:10.1007/978-3-030-11815-0_42 · Cited by 2 · see citing works
L’internista ospedaliero nella gestione del paziente diabetico complesso
Magnani, G. E. L., Beltramello, G., Brancato, D., Fontanella, A., & Nardi, R. (2018) · Italian Journal of Medicine · doi:10.4081/itjm.q.2018.2 · Cited by 2 · see citing works
Lyhne, M. K., Vegge, A., Povlsen, G. K., Slaaby, R., Kildegaard, J., Pedersen‐Bjergaard, U., & Olsen, L. H. (2021) · Scientific Reports · doi:10.1038/s41598-021-84758-w · Cited by 2 · see citing works
Bruns, F., Fender, A. C., Poppenborg, T., Dudley, S. C., & Dobrev, D. (2025) · Cardiovascular Research · doi:10.1093/cvr/cvaf252 · Cited by 1 · see citing works
Liu, Y., Guo, C., Li, X., Shen, L., Huang, J., Zhao, L., Zhu, Y., Liu, X., Wang, B., Lin, R., et al. (2026) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1685969 · Cited by 1 · see citing works
Hypoglycemia, insulin resistance, and cardiovascular disease: A possible link
Iqbal, A., Chaudhury, T., & Heller, S. R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-323-85732-1.00028-1 · Cited by 1 · see citing works
Hypoglycemia, Arrythmia and Mortality in Diabetes, an underestimated risk?
Kasperek, B., Tymoszuk, P., Augustowska, K., Żak-Gontarz, A., Sierzpowski, R., Protasiuk, A., Loryś, L., Klimczak, K., & Budzyńska, K. (2025) · Quality in Sport · doi:10.12775/qs.2025.42.61151 · Cited by 1 · see citing works
Inobvious complications of hypoglycaemia
Majkowska, L. (2017) · Clinical Diabetology · doi:10.5603/dk.2017.0025 · Cited by 1 · see citing works
Demirtaş, A. O., İçen, Y. K., Koca, H., Sümbül, H. E., Demirtaş, D., Köseoğlu, Z., & Koç, M. (2019) · Journal of Interventional Cardiac Electrophysiology · doi:10.1007/s10840-019-00549-4 · Cited by 1 · see citing works
Hypoglycemia Induced Mitochondrial Connexin-43 Accumulation Aggravates Diabetic CardiomyopathyPreprint
Wei, X., Chang, A. C. H., Chang, H., Xu, S., Xue, Y., Zhang, Y., Lei, M., Chang, A. C. Y., & Zhang, Q. (2021) · Research Square · doi:10.21203/rs.3.rs-885699/v1 · Cited by 1 · see citing works
Bringer, J., Place, J., & Renard, É. (2017) · Bulletin de l Académie Nationale de Médecine · doi:10.1016/s0001-4079(19)30415-7
Ramos, O., Asenjo-Mardones, S. M., Calzada‐León, R., Bruce, H. G., de Blanco, M. G., Ferraro, M. C., Lema-Izquierdo, A., Martínez-Ariza, L., Orellana-Sáenz, C., Prieto, M., et al. (2020) · Alad · doi:10.24875/alad.19000396
Severe Hypoglycemia in Hospitalized Children with Diabetic Ketoacidosis in Brazzaville
Oko, A. P. G., Kambourou, J., Engoba, M., Laetitia, L., Ngakengni, N. Y., Mandilou, S. V. M., Cardorelle, A. M., & Moyen, G. M. (2020) · Open Journal of Pediatrics · doi:10.4236/ojped.2020.101024
Placement of insulin pump by telemedicine
Foglia, A. (2020) · The Journal of AMD · doi:10.36171/jamd20.23.4.6
Helmi, M. A. M., Norsa’adah, B., & Hussain, S. (2021) · Malaysian Journal of Paediatrics and Child Health · doi:10.51407/mjpch.v27i2.152
Stoica, R. A., Frătița, D., Scafa‐Udriște, A., Fronea, O. F. G., Dorobanţu, M., Ionescu-Tirgoviste, C., & Guja, C. (2022) · Journal of Diabetes Mellitus · doi:10.4236/jdm.2022.122012
Manov, A., House, J., Antonio, S., Banal, M., & Nazha, J. (2023) · World Journal of Advanced Research and Reviews · doi:10.30574/wjarr.2023.17.3.0414
Hypoglycemia: Diagnosis, Management, and Prevention
Faradji, R. N., Uribe-Wiechers, A. C., & de la Maza, E. S. (2023) · Springer eBooks · doi:10.1007/978-3-031-25519-9_45
- Authors
- Novodvorsky, P., Bernjak, A., Chow, E., Iqbal, A., Sellors, L., Williams, S., Fawdry, R. A., Parekh, B., Jacques, R. M., Marques, J. L. B., Sheridan, P. J., & Heller, S. R.
- Affiliations
- Department of Oncology and Metabolism, University of Sheffield, Sheffield, U.K.
- Insigneo (GB)
- Sheffield Teaching Hospitals NHS Foundation Trust (GB)
- University of Sheffield (GB)
- Corresponding author
- Heller, Simon R.
- ORCID
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2017-02-17
- Volume
- 40
- Issue
- 5
- Pages
- 655-662
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- OpenAlex
- W2588258146
- Cited by
- 111
- References
- 43
- Citations by year
- 2026: 6 · 2025: 12 · 2024: 9 · 2023: 14 · 2022: 11 · 2021: 13 · 2020: 8 · 2019: 15 · 2018: 13 · 2017: 9
- FWCI
- 9.72
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes Care (publishedVersion)
- PubMed (publishedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
- Funders
- National Institute for Health and Care Research (NF-SI-0515-10079, ACF-2014-04-002, BRF-2011-004)
- Medical Research Council (MR/M00371X/1)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Diabetes and associated disorders
- Keywords
- type 1 diabetes, hypoglycemia, cardiac arrhythmias, nocturnal hypoglycemia, diurnal variation, bradycardia, cardiac repolarization, QTc prolongation, heart rate variability, asymptomatic hypoglycemia, youth
- MeSH terms
- Adult, Arrhythmias, Cardiac, Circadian Rhythm, Diabetes Mellitus, Type 1, Electrocardiography, Female, Heart Conduction System, Heart Rate, Humans, Hypoglycemia, Male, Risk Factors
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