Assessment and management of hypoglycemia in children and adolescents with diabetes

Pediatric Diabetes

Volumn 15, Issue S20, 2014, Pages 180-192

  Ly, Trang T ^a,b   Maahs, David M ^c   Rewers, Arleta ^d   Dunger, David ^e   Oduwole, Abiola ^f   Jones, Timothy W ^b,g,h  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSITY OF COLORADO   (United States)

^d Children's Hospital Colorado   (United States)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f UNIVERSITY OF LAGOS   (Nigeria)

^g PRINCESS MARGARET HOSPITAL FOR CHILDREN   (Australia)

^h UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Guidelines; Hypoglycemia; Pediatrics

Indexed keywords

GLUCOSE; INSULIN; ANTIDIABETIC AGENT;

ADOLESCENT; ARTICLE; AWARENESS; BLOOD GLUCOSE MONITORING; BRAIN DYSFUNCTION; CHILD; DIABETES MELLITUS; DRUG DELIVERY SYSTEM; EXERCISE; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; HUMAN; HYPOGLYCEMIA; INCIDENCE; NOCTURNAL HYPOGLYCEMIA; RISK FACTOR; ADVERSE EFFECTS; BLOOD; CHEMICALLY INDUCED; CIRCADIAN RHYTHM; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DRUG MONITORING; EVIDENCE BASED MEDICINE; HEALTH CARE ORGANIZATION; INFANT; INTERNATIONAL COOPERATION; MEDICINE; MULTIMODALITY CANCER THERAPY; PATHOPHYSIOLOGY; PEDIATRICS; PERSONALIZED MEDICINE; PRACTICE GUIDELINE; PRESCHOOL CHILD; SEVERITY OF ILLNESS INDEX; TRENDS;

ADOLESCENT; ADOLESCENT MEDICINE; CHILD; CHILD, PRESCHOOL; CIRCADIAN RHYTHM; COMBINED MODALITY THERAPY; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DRUG MONITORING; EVIDENCE-BASED MEDICINE; EXERCISE; HUMANS; HYPOGLYCEMIA; HYPOGLYCEMIC AGENTS; INFANT; INSULIN; INTERNATIONAL AGENCIES; PEDIATRICS; PRECISION MEDICINE; RISK FACTORS; SEVERITY OF ILLNESS INDEX; SOCIETIES, SCIENTIFIC;

EID: 84913600184     PISSN: 1399543X     EISSN: 13995448     Source Type: Journal    
DOI: 10.1111/pedi.12174     Document Type: Article

References (91)

1. American Diabetes Association. Standards of medical care in diabetes - 2008. Diabetes Care 2008: 31 (Suppl 1): S12-S54.
2. Davis EA, Keating B, Byrne GC, Russell M, Jones TW. Hypoglycemia: incidence and clinical predictors in a large population-based sample of children and adolescents with IDDM. Diabetes Care 1997: 20: 22-25.
3. Juvenile Diabetes Research Foundation Continuous Glucose Monitoring Study Group. Prolonged nocturnal hypoglycemia is common during 12 months of continuous glucose monitoring in children and adults with type 1 diabetes. Diabetes Care 2010: 33: 1004-1008.
4. Davis EA, Keating B, Byrne GC, Russell M, Jones TW. Impact of improved glycaemic control on rates of hypoglycaemia in insulin dependent diabetes mellitus. Arch Dis Child 1998: 78: 111-115.
5. Buckingham B, Wilson DM, Lecher T, Hanas R, Kaiserman K, Cameron F. Duration of nocturnal hypoglycemia before seizures. Diabetes Care 2008: 31: 2110-2112.
6. Tanenberg RJ, Newton CA, Drake AJ. Confirmation of hypoglycemia in the "dead-in-bed" syndrome, as captured by a retrospective continuous glucose monitoring system. Endocr Pract 2010: 16: 244-248.
7. O'Connell SM, Cooper MN, Bulsara MK, Davis EA, Jones TW. Reducing rates of severe hypoglycemia in a population-based cohort of children and adolescents with type 1 diabetes over the decade 2000-2009. Diabetes Care 2011: 34: 2379-2380.
8. Cooper MN, O'Connell SM, Davis EA, Jones TW. A population-based study of risk factors for severe hypoglycaemia in a contemporary cohort of childhood-onset type 1 diabetes. Diabetologia 2013: 56: 2164-2170.
9. Holl RW, Swift PG, Mortensen HB et al. Insulin injection regimens and metabolic control in an international survey of adolescents with type 1 diabetes over 3 years: results from the Hvidore study group. Eur J Pediatr 2003: 162: 22-29.
10. Wood JR, Miller KM, Maahs DM et al. Most youth with type 1 diabetes in the T1D exchange clinic registry do not meet american diabetes association or international society for pediatric and adolescent diabetes clinical guidelines. Diabetes Care 2013: 36: 2035-2037.
11. Jones TW, Boulware SD, Kraemer DT, Caprio S, Sherwin RS, Tamborlane WV. Independent effects of youth and poor diabetes control on responses to hypoglycemia in children. Diabetes 1991: 40: 358-363.
12. Cryer PE. Mechanisms of hypoglycemia-associated autonomic failure and its component syndromes in diabetes. Diabetes 2005: 54: 3592-3601.
13. Seaquist ER, Anderson J, Childs B et al. Hypoglycemia and diabetes: a report of a workgroup of the American Diabetes Association and the Endocrine Society. Diabetes Care 2013: 36: 1384-1395.
14. Clarke W, Jones T, Rewers A, Dunger D, Klingensmith GJ. Assessment and management of hypoglycemia in children and adolescents with diabetes. Pediatr Diabetes 2008: 9: 165-174.
15. Diabetes Control and Complications Trial Research Group. Effect of intensive diabetes treatment on the development and progression of long-term complications in adolescents with insulin-dependent diabetes mellitus. Diabetes Control and Complications Trial. J Pediatr 1994: 125: 177-188.
16. Rewers A, Chase HP, Mackenzie T et al. Predictors of acute complications in children with type 1 diabetes. JAMA 2002: 287: 2511-2518.
17. Cengiz E, Xing D, Wong JC et al. Severe hypoglycemia and diabetic ketoacidosis among youth with type 1 diabetes in the T1D exchange clinic registry. Pediatr Diabetes 2013: 14: 447-454.
18. Bulsara MK, Holman CD, Davis EA, Jones TW. The impact of a decade of changing treatment on rates of severe hypoglycemia in a population-based cohort of children with type 1 diabetes. Diabetes Care 2004: 27: 2293-2298.
19. Cryer PE. Symptoms of hypoglycemia, thresholds for their occurrence, and hypoglycemia unawareness. Endocrinol Metab Clin North Am 1999: 28: 495-500 v-vi.
20. Jones TW, Borg WP, Borg MA et al. Resistance to neuroglycopenia: an adaptive response during intensive insulin treatment of diabetes. J Clin Endocrinol Metab 1997: 82: 1713-1718.
21. McCrimmon RJ, Gold AE, Deary IJ, Kelnar CJ, Frier BM. Symptoms of hypoglycemia in children with IDDM. Diabetes Care 1995: 18: 858-861.
22. Tupola S, Rajantie J. Documented symptomatic hypoglycaemia in children and adolescents using multiple daily insulin injection therapy. Diabet Med 1998: 15: 492-496.
23. Morris AD, Boyle DI, McMahon AD, Greene SA, MacDonald TM, Newton RW. Adherence to insulin treatment, glycaemic control, and ketoacidosis in insulin-dependent diabetes mellitus. The DARTS/MEMO Collaboration. Diabetes Audit and Research in Tayside Scotland. Medicines Monitoring Unit. Lancet 1997: 350: 1505-1510.
24. Amiel SA, Sherwin RS, Simonson DC, Lauritano AA, Tamborlane WV. Impaired insulin action in puberty. A contributing factor to poor glycemic control in adolescents with diabetes. N Engl J Med 1986: 315: 215-219.
25. Aman J, Wranne L. Hypoglycaemia in childhood diabetes. II. Effect of subcutaneous or intramuscular injection of different doses of glucagon. Acta Paediatr Scand 1988: 77: 548-553.
26. Gunning RR, Garber AJ. Bioactivity of instant glucose. Failure of absorption through oral mucosa. JAMA 1978: 240: 1611-1612.
27. Brodows RG, Williams C, Amatruda JM. Treatment of insulin reactions in diabetics. JAMA 1984: 252: 3378-3381.
28. Georgakopoulos K, Katsilambros N, Fragaki M et al. Recovery from insulin-induced hypoglycemia after saccharose or glucose administration. Clin Physiol Biochem 1990: 8: 267-272.
29. Wiethop BV, Cryer PE. Alanine and terbutaline in treatment of hypoglycemia in IDDM. Diabetes Care 1993: 16: 1131-1136.
30. Tsalikian E, Kollman C, Tamborlane WB et al. Prevention of hypoglycemia during exercise in children with type 1 diabetes by suspending basal insulin. Diabetes Care 2006: 29: 2200-2204.
31. Maahs DM, Hermann JM, DuBose SN et al. Contrasting the clinical care and outcomes of 2, 622 children with type 1 diabetes less than 6 years of age in the United States and German/Austrian DPV registries. Diabetologia 2014.
32. Boileau P, Aboumrad B, Bougneres P. Recurrent comas due to secret self-administration of insulin in adolescents with type 1 diabetes. Diabetes Care 2006: 29: 430-431.
33. Yu L, Brewer KW, Gates S et al. DRB1*04 and DQ alleles: expression of 21-hydroxylase autoantibodies and risk of progression to Addison's disease. J Clin Endocrinol Metab 1999: 84: 328-335.
34. McAulay V, Frier BM. Addison's disease in type 1 diabetes presenting with recurrent hypoglycaemia. Postgrad Med J 2000: 76: 230-232.
35. Phornphutkul C, Boney CM, Gruppuso PA. A novel presentation of Addison disease: hypoglycemia unawareness in an adolescent with insulin-dependent diabetes mellitus. J Pediatr 1998: 132: 882-884.
36. Iafusco D, Rea F, Prisco F. Hypoglycemia and reduction of the insulin requirement as a sign of celiac disease in children with IDDM. Diabetes Care 1998: 21: 1379-1381.
37. Mohn A, Cerruto M, Iafusco D et al. Celiac disease in children and adolescents with type I diabetes: importance of hypoglycemia. J Pediatr Gastroenterol Nutr 2001: 32: 37-40.
38. McMahon SK, Ferreira LD, Ratnam N et al. Glucose requirements to maintain euglycemia after moderate-intensity afternoon exercise in adolescents with type 1 diabetes are increased in a biphasic manner. J Clin Endocrinol Metab 2007: 92: 963-968.
39. Tansey MJ, Tsalikian E, Beck RW et al. The effects of aerobic exercise on glucose and counterregulatory hormone concentrations in children with type 1 diabetes. Diabetes Care 2006: 29: 20-25.
40. Grimm JJ, Ybarra J, Berne C, Muchnick S, Golay A. A new table for prevention of hypoglycaemia during physical activity in type 1 diabetic patients. Diabetes Metab 2004: 30: 465-470.
41. Riddell MC, Iscoe KE. Physical activity, sport, and pediatric diabetes. Pediatr Diabetes 2006: 7: 60-70.
42. Robertson K, Adolfsson P, Riddell MC, Scheiner G, Hanas R. Exercise in children and adolescents with diabetes. Pediatr Diabetes 2008: 9: 65-77.
43. Monaghan MC, Hilliard ME, Cogen FR, Streisand R. Nighttime caregiving behaviors among parents of young children with type 1 diabetes: associations with illness characteristics and parent functioning. Fam Syst Health 2009: 27: 28-38.
44. Jones TW, Porter P, Sherwin RS et al. Decreased epinephrine responses to hypoglycemia during sleep. N Engl J Med 1998: 338: 1657-1662.
45. Matyka KA, Crowne EC, Havel PJ, Macdonald IA, Matthews D, Dunger DB. Counterregulation during spontaneous nocturnal hypoglycemia in prepubertal children with type 1 diabetes. Diabetes Care 1999: 22: 1144-1150.
46. Beregszaszi M, Tubiana-Rufi N, Benali K, Noel M, Bloch J, Czernichow P. Nocturnal hypoglycemia in children and adolescents with insulin-dependent diabetes mellitus: prevalence and risk factors. J Pediatr 1997: 131: 27-33.
47. Matyka KA, Wigg L, Pramming S, Stores G, Dunger DB. Cognitive function and mood after profound nocturnal hypoglycaemia in prepubertal children with conventional insulin treatment for diabetes. Arch Dis Child 1999: 81: 138-142.
48. Kaufman FR, Austin J, Neinstein A et al. Nocturnal hypoglycemia detected with the continuous glucose monitoring system in pediatric patients with type 1 diabetes. J Pediatr 2002: 141: 625-630.
49. Porter PA, Keating B, Byrne G, Jones TW. Incidence and predictive criteria of nocturnal hypoglycemia in young children with insulin-dependent diabetes mellitus. J Pediatr 1997: 130: 366-372.
50. Kalergis M, Schiffrin A, Gougeon R, Jones PJ, Yale JF. Impact of bedtime snack composition on prevention of nocturnal hypoglycemia in adults with type 1 diabetes undergoing intensive insulin management using lispro insulin before meals: a randomized, placebo-controlled, crossover trial. Diabetes Care 2003: 26: 9-15.
51. Ververs MT, Rouwe C, Smit GP. Complex carbohydrates in the prevention of nocturnal hypoglycaemia in diabetic children. Eur J Clin Nutr 1993: 47: 268-273.
52. Kaufman FR, Halvorson M, Kaufman ND. A randomized, blinded trial of uncooked cornstarch to diminish nocturnal hypoglycemia at diabetes camp. Diabetes Res Clin Pract 1995: 30: 205-209.
53. Willi SM, Planton J, Egede L, Schwarz S. Benefits of continuous subcutaneous insulin infusion in children with type 1 diabetes. J Pediatr 2003: 143: 796-801.
54. Weintrob N, Schechter A, Benzaquen H et al. Glycemic patterns detected by continuous subcutaneous glucose sensing in children and adolescents with type 1 diabetes mellitus treated by multiple daily injections vs continuous subcutaneous insulin infusion. Arch Pediatr Adolesc Med 2004: 158: 677-684.
55. Ludvigsson J, Hanas R. Continuous subcutaneous glucose monitoring improved metabolic control in pediatric patients with type 1 diabetes: a controlled crossover study. Pediatrics 2003: 111: 933-938.
56. Ryan C, Vega A, Drash A. Cognitive deficits in adolescents who developed diabetes early in life. Pediatrics 1985: 75: 921-927.
57. Wysocki T, Harris MA, Wilkinson K, Sadler M, Mauras N, White NH. Absence of adverse effects of severe hypoglycemia on cognitive function in school-aged children with diabetes over 18 months. Diabetes Care 2003: 26: 2043-2047.
58. Strudwick SK, Carne C, Gardiner J, Foster JK, Davis EA, Jones TW. Cognitive functioning in children with early onset type 1 diabetes and severe hypoglycemia. J Pediatr 2005: 147: 680-685.
59. Ly TT, Anderson M, McNamara KA, Davis EA, Jones TW. Neurocognitive outcomes in young adults with early-onset type 1 diabetes: a prospective follow-up study. Diabetes Care 2011: 34: 2192-2197.
60. Ho MS, Weller NJ, Ives FJ et al. Prevalence of structural central nervous system abnormalities in early-onset type 1 diabetes mellitus. J Pediatr 2008: 153: 385-390.
61. Perantie DC, Wu J, Koller JM et al. Regional brain volume differences associated with hyperglycemia and severe hypoglycemia in youth with type 1 diabetes. Diabetes Care 2007: 30: 2331-2337.
62. Barnea-Goraly N, Raman M, Mazaika P et al. Alterations in white matter structure in young children with type 1 diabetes. Diabetes Care 2014: 37: 332-340.
63. 1c, age at diagnosis and sex. Diabetologia 2002: 45: 108-114.
64. Ferguson SC, Blane A, Wardlaw J et al. Influence of an early-onset age of type 1 diabetes on cerebral structure and cognitive function. Diabetes Care 2005: 28: 1431-1437.
65. Davis EA, Soong SA, Byrne GC, Jones TW. Acute hyperglycaemia impairs cognitive function in children with IDDM. J Pediatr Endocrinol Metab 1996: 9: 455-461.
66. Perantie DC, Lim A, Wu J et al. Effects of prior hypoglycemia and hyperglycemia on cognition in children with type 1 diabetes mellitus. Pediatr Diabetes 2008: 9: 87-95.
67. Arbelaez AM, Semenkovich K, Hershey T. Glycemic extremes in youth with T1DM: the structural and functional integrity of the developing brain. Pediatr Diabetes 2013: 14: 541-553.
68. Cryer PE. Hypoglycaemia: the limiting factor in the glycaemic management of type I and type II diabetes. Diabetologia 2002: 45: 937-948.
69. Sandoval DA, Guy DL, Richardson MA, Ertl AC, Davis SN. Acute, same-day effects of antecedent exercise on counterregulatory responses to subsequent hypoglycemia in type 1 diabetes mellitus. Am J Physiol Endocrinol Metab 2006: 290: E1331-E1338.
70. Amiel SA, Pottinger RC, Archibald HR et al. Effect of antecedent glucose control on cerebral function during hypoglycemia. Diabetes Care 1991: 14: 109-118.
71. Amiel SA, Gale E. Physiological responses to hypoglycemia. Counterregulation and cognitive function. Diabetes Care 1993: 16 (Suppl 3): 48-55.
72. Amiel SA, Simonson DC, Sherwin RS, Lauritano AA, Tamborlane WV. Exaggerated epinephrine responses to hypoglycemia in normal and insulin-dependent diabetic children. J Pediatr 1987: 110: 832-837.
73. Diabetes Control and Complications Trial Research Group. Epidemiology of severe hypoglycemia in the diabetes control and complications trial. The DCCT Research Group. Am J Med 1991: 90: 450-459.
74. Ly TT, Gallego PH, Davis EA, Jones TW. Impaired awareness of hypoglycemia in a population-based sample of children and adolescents with type 1 diabetes. Diabetes Care 2009: 32: 1802-1806.
75. Cranston I, Lomas J, Maran A, Macdonald I, Amiel SA. Restoration of hypoglycaemia awareness in patients with long-duration insulin-dependent diabetes. Lancet 1994: 344: 283-287.
76. Ly TT, Hewitt J, Davey RJ, Lim EM, Davis EA, Jones TW. Improving epinephrine responses in hypoglycemia unawareness with real-time continuous glucose monitoring in adolescents with type 1 diabetes. Diabetes Care 2011: 34: 50-52.
77. Bergenstal RM, Tamborlane WV, Ahmann A et al. Effectiveness of sensor-augmented insulin-pump therapy in type 1 diabetes. N Engl J Med 2010: 363: 311-320.
78. Buckingham B, Block J, Burdick J et al. Response to nocturnal alarms using a real-time glucose sensor. Diabetes Technol Ther 2005: 7: 440-447.
79. Ly TT, Jones TW, Griffiths A et al. Hypoglycemia does not change the threshold for arousal from sleep in adolescents with type 1 diabetes. Diabetes Technol Ther 2011: 14: 101-104.
80. Ly TT, Nicholas JA, Retterath A, Lim EM, Davis EA, Jones TW. Effect of sensor-augmented insulin pump therapy and automated insulin suspension vs standard insulin pump therapy on hypoglycemia in patients with type 1 diabetes: a randomized clinical trial. JAMA 2013: 310: 1240-1247.
81. Buckingham B, Chase HP, Dassau E et al. Prevention of nocturnal hypoglycemia using predictive alarm algorithms and insulin pump suspension. Diabetes Care 2010: 33: 1013-1017.
82. Maahs DM, Calhoun P, Buckingham BA et al. A randomized trial of a home system to reduce nocturnal hypoglycemia in type 1 diabetes. Diabetes Care 2014: 37: 1885-1891.
83. O'Grady MJ, Retterath AR, Keenan DB et al. The use of an automated, portable glucose control system for overnight glucose control in adolescents and young adults with type 1 diabetes. Diabetes Care 2012: 35: 2182-2187.
84. Weinzimer SA, Steil GM, Swan KL, Dziura J, Kurtz N, Tamborlane WV. Fully automated closed-loop insulin delivery versus semiautomated hybrid control in pediatric patients with type 1 diabetes using an artificial pancreas. Diabetes Care 2008: 31: 934-939.
85. Hovorka R, Allen JM, Elleri D et al. Manual closed-loop insulin delivery in children and adolescents with type 1 diabetes: a phase 2 randomised crossover trial. Lancet 2010: 375: 743-751.
86. Phillip M, Battelino T, Atlas E et al. Nocturnal glucose control with an artificial pancreas at a diabetes camp. N Engl J Med 2013: 368: 824-833.
87. Ly TT, Breton M, Keith-Hynes P et al. Overnight glucose control with an automated, unified safety system in children and adolescents with type 1 diabetes at diabetes camp. Diabetes Care 2014.
88. Tamborlane WV. Closed-loop insulin delivery: we're "virtually" there. Diabetes Technol Ther 2012: 14: 203-204.
89. Eugster EA, Francis G. Position statement: continuous subcutaneous insulin infusion in very young children with type 1 diabetes. Pediatrics 2006: 118: e1244-e1249.
90. O'Connell MA, Gilbertson HR, Donath SM, Cameron FJ. Optimizing postprandial glycemia in pediatric patients with type 1 diabetes using insulin pump therapy: impact of glycemic index and prandial bolus type. Diabetes Care 2008: 31: 1491-1495.
91. Smart CE, Evans M, O'Connell SM et al. Both dietary protein and fat increase postprandial glucose excursions in children with type 1 diabetes, and the effect is additive. Diabetes Care 2013: 36: 3897-3902.