Type 1 diabetes-associated cognitive decline: A meta-analysis and update of the current literature

Journal of Diabetes

Volumn 6, Issue 6, 2014, Pages 499-513

  Tonoli, Cajsa ^a,d   Heyman, Elsa ^d   Roelands, Bart ^a,c   Pattyn, Nathalie ^a,b   Buyse, Luk ^a   Piacentini, Maria Francesca ^a,e   Berthoin, Serge ^d   Meeusen, Romain ^a,f  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b ROYAL MILITARY ACADEMY   (Belgium)

^c RESEARCH FOUNDATION FLANDERS FWO   (Belgium)

^d UNIV LILLE   (France)

^e SAPIENZA UNIVERSITY OF ROME   (Italy)

^f JAMES COOK UNIVERSITY   (Australia)

Author keywords

Diabetes; Diabetes associated cognitive decline; Hyperglycemia; Hypoglycemia

Indexed keywords

C PEPTIDE;

ADULT DISEASE; ARTICLE; CHILDHOOD DISEASE; CHRONIC DISEASE; COGNITION; COGNITIVE DEFECT; DISEASE ASSOCIATION; DISEASE SEVERITY; EXECUTIVE FUNCTION; GLYCEMIC CONTROL; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; INSULIN DEFICIENCY; INSULIN DEPENDENT DIABETES MELLITUS; INTELLIGENCE QUOTIENT; MENTAL PERFORMANCE; META ANALYSIS; MOTOR ACTIVITY; ONSET AGE; PSYCHIATRIC TREATMENT; RECURRENT DISEASE; SPATIAL MEMORY; VELOCITY; VERBAL COMMUNICATION; ADULT; AGE; CHILD; COGNITION DISORDERS; COMPLICATION; MEMORY; NEUROPSYCHOLOGICAL TEST; PSYCHOLOGY; SEVERITY OF ILLNESS INDEX;

ADULT; AGE FACTORS; CHILD; COGNITION; COGNITION DISORDERS; DIABETES MELLITUS, TYPE 1; HUMANS; MEMORY; NEUROPSYCHOLOGICAL TESTS; SEVERITY OF ILLNESS INDEX;

EID: 84912019369     PISSN: 17530393     EISSN: 17530407     Source Type: Journal    
DOI: 10.1111/1753-0407.12193     Document Type: Article

References (97)

1. Brands AM, Biessels GJ, de Haan EH, Kappelle LJ, Kessels RP. The effects of type 1 diabetes on cognitive performance: A meta-analysis. Diabetes Care. 2005; 28: 726-735.
2. Miles WR, Root HF. Psychologic tests applied in diabetic patients. Arch Intern Med. 1922; 30: 767-770.
3. Mijnhout GS, Scheltens P, Diamant M etal. Diabetic encephalopathy: A concept in need of a definition. Diabetologia. 2006; 49: 1447-1448.
4. Gaudieri PA, Chen R, Greer TF, Holmes CS. Cognitive function in children with type 1 diabetes: A meta-analysis. Diabetes Care. 2008; 31: 1892-1897.
5. Blasetti A, Chiuri RM, Tocco AM etal. The effect of recurrent severe hypoglycemia on cognitive performance in children with type 1 diabetes: A meta-analysis. J Child Neurol. 2011; 26: 1383-1391.
6. Auer RN. Hypoglycemic brain damage. Metab Brain Dis. 2004; 19: 169-175.
7. Malone JI, Hanna S, Saporta S etal. Hyperglycemia not hypoglycemia alters neuronal dendrites and impairs spatial memory. Pediatr Diabetes. 2008; 9: 531-539.
8. Wrighten SA, Piroli GG, Grillo CA, Reagan LP. A look inside the diabetic brain: Contributors to diabetes-induced brain aging. Biochim Biophys Acta. 2009; 1792: 444-453.
9. Li ZG, Zhang W, Sima AA. The role of impaired insulin/IGF action in primary diabetic encephalopathy. Brain Res. 2005; 1037: 12-24.
10. Li ZG, Zhang W, Sima AA. C-Peptide prevents hippocampal apoptosis in type 1 diabetes. Int J Exp Diabetes Res. 2002; 3: 241-245.
11. Sima AA, Kamiya H, Li ZG. Insulin, C-peptide, hyperglycemia, and central nervous system complications in diabetes. Eur J Pharmacol. 2004; 490: 187-197.
12. Perantie DC, Wu J, Koller JM etal. Regional brain volume differences associated with hyperglycemia and severe hypoglycemia in youth with type 1 diabetes. Diabetes Care. 2007; 30: 2331-2337.
13. Stargardt T, Gonder-Frederick L, Krobot KJ, Alexander CM. Fear of hypoglycaemia: Defining a minimum clinically important difference in patients with type 2 diabetes. Health Qual Life Outcomes. 2009; 7: 91-99.
14. Chaytor N, Schmitter-Edgecombe M. The ecological validity of neuropsychological tests: A review of the literature on everyday cognitive skills. Neuropsychol Rev. 2003; 13: 181-197.
15. Aye T, Reiss AL, Kesler S etal. The feasibility of detecting neuropsychologic and neuroanatomic effects of type 1 diabetes in young children. Diabetes Care. 2011; 34: 1458-1462.
16. Crawford SG, Kaplan BJ, Field LL. Absence of an association between insulin-dependent diabetes mellitus and developmental learning difficulties. Hereditas. 1995; 122: 73-78.
17. Hannonen R, Tupola S, Ahonen T, Riikonen R. Neurocognitive functioning in children with type-1 diabetes with and without episodes of severe hypoglycemia. Dev Med Child Neurol. 2003; 45: 262-268.
18. Hannonen R, Komulainen J, Riikonen R etal. Academic skills in children with early-onset type 1 diabetes: The effects of diabetes-related risk factors. Dev Med Child Neurol. 2012; 54: 457-463.
19. Hershey T, Bhargava N, Sadler M, White NH, Craft S. Conventional versus intensive diabetes therapy in children with type 1 diabetes: Effects on memory and motor speed. Diabetes Care. 1999; 22: 1318-1324.
20. Hershey T, Lillie R, Sadler M, White NH. Severe hypoglycemia and long-term spatial memory in children with type 1 diabetes mellitus: A retrospective study. J Int Neuropsychol Soc. 2003; 9: 740-750.
21. Hershey T, Lillie R, Sadler M, White NH. A prospective study of severe hypoglycemia and long-term spatial memory in children with type 1 diabetes. Pediatr Diabetes. 2004; 5: 63-71.
22. Hershey T, Perantie DC, Warren SL, Zimmerman EC, Sadler M, White NH. Frequency and timing of severe hypoglycemia affects spatial memory in children with type 1 diabetes. Diabetes Care. 2005; 28: 2372-2377.
23. Holmes CS, Dunlap WP, Chen RS, Cornwell JM. Gender differences in the learning status of diabetic children. J Consult Clin Psychol. 1992; 60: 698-704.
24. Kaufman FR, Epport K, Engilman R, Halvorson M. Neurocognitive functioning in children diagnosed with diabetes before age 10 years. J Diabetes Complications. 1999; 13: 31-38.
25. Northam EA, Anderson PJ, Jacobs R, Hughes M, Warne GL, Werther GA. Neuropsychological profiles of children with type 1 diabetes 6 years after disease onset. Diabetes Care. 2001; 24: 1541-1546.
26. Ohmann S, Popow C, Rami B etal. Cognitive functions and glycemic control in children and adolescents with type 1 diabetes. Psychol Med. 2009; 40: 95-103.
27. Patino-Fernandez AM, Delamater AM, Applegate EB etal. Neurocognitive functioning in preschool-age children with type 1 diabetes mellitus. Pediatr Diabetes. 2010; 11: 424-430.
28. Perantie DC, Lim A, Wu J etal. Effects of prior hypoglycemia and hyperglycemia on cognition in children with type 1 diabetes mellitus. Pediatr Diabetes. 2008; 9: 87-95.
29. Rovet JF, Ehrlich RM, Hoppe M. Specific intellectual deficits in children with early onset diabetes mellitus. Child Dev. 1988; 59: 226-234.
30. Ryan C, Vega A, Drash A. Cognitive deficits in adolescents who developed diabetes early in life. Pediatrics. 1985; 75: 921-927.
31. Shehata G, Eltayeb A. Cognitive function and event-related potentials in children with type 1 diabetes mellitus. J Child Neurol. 2010; 25: 469-474.
32. Blackman JD, Towle VL, Sturis J, Lewis GF, Spire JP, Polonsky KS. Hypoglycemic thresholds for cognitive dysfunction in IDDM. Diabetes. 1992; 41: 392-399.
33. Brands AM, Kessels RP, Hoogma RP etal. Cognitive performance, psychological well-being, and brain magnetic resonance imaging in older patients with type 1 diabetes. Diabetes. 2006; 55: 1800-1806.
34. Deary IJ, Crawford JR, Hepburn DA etal. Severe hypoglycemia and intelligence in adult patients with insulin-treated diabetes. Diabetes. 1993; 42(2): 341-344.
35. Franceschi M, Cecchetto R, Minicucci F, Smizne S, Baio G, Canal N. Cognitive processes in insulin-dependent diabetes. Diabetes Care. 1984; 7: 228-231.
36. Geddes J, Deary IJ, Frier BM. Effects of acute insulin-induced hypoglycaemia on psychomotor function: People with type 1 diabetes are less affected than non-diabetic adults. Diabetologia. 2008; 51: 1814-1821.
37. Kramer L, Fasching P, Madl C etal. Previous episodes of hypoglycemic coma are not associated with permanent cognitive brain dysfunction in IDDM patients on intensive insulin treatment. Diabetes. 1998; 47: 1909-1914.
38. Lawson JS, Erdahl DL, Monga TN etal. Neuropsychological function in diabetic patients with neuropathy. Br J Psychiatry. 1984; 145: 263-268.
39. 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.
40. Maran A, Lomas J, Macdonald IA, Amiel SA. Lack of preservation of higher brain function during hypoglycaemia in patients with intensively-treated IDDM. Diabetologia. 1995; 38: 1412-1418.
41. Ryan CM, Williams TM, Orchard TJ, Finegold DN. Psychomotor slowing is associated with distal symmetrical polyneuropathy in adults with diabetes mellitus. Diabetes. 1992; 41: 107-113.
42. Ryan CM, Williams TM. Effects of insulin-dependent diabetes on learning and memory efficiency in adults. J Clin Exp Neuropsychol. 1993; 15: 685-700.
43. Ryan CM, Williams TM, Finegold DN, Orchard TJ. Cognitive dysfunction in adults with type 1 (insulin-dependent) diabetes mellitus of long duration: Effects of recurrent hypoglycaemia and other chronic complications. Diabetologia. 1993; 36: 329-334.
44. Sachon C, Grimaldi A, Digy JP, Pillon B, Dubois B, Thervet F. Cognitive function, insulin-dependent diabetes and hypoglycaemia. J Intern Med. 1992; 231: 471-475.
45. Wright RJ, Frier BM, Deary IJ. Effects of acute insulin-induced hypoglycemia on spatial abilities in adults with type 1 diabetes. Diabetes Care. 2009; 32: 1503-1506.
46. Wessels AM, Rombouts SA, Remijnse PL etal. Cognitive performance in type 1 diabetes patients is associated with cerebral white matter volume. Diabetologia. 2007; 50: 1763-1769.
47. Jacobson AM, Musen G, Ryan CM etal. Long-term effect of diabetes and its treatment on cognitive function. N Engl J Med. 2007; 356: 1842-1852.
48. Kelly D, Hamilton JK, Riddell MC. Blood glucose levels and performance in a sports cAMP for adolescents with type 1 diabetes mellitus: A field study. Int J Pediatr. 2010; 1: 1-8.
49. Knight S, Northam E, Donath S etal. Improvements in cognition, mood and behaviour following commencement of continuous subcutaneous insulin infusion therapy in children with type 1 diabetes mellitus: A pilot study. Diabetologia. 2009; 52: 193-198.
50. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med. 1993; 329: 977-986.
51. Draelos MT, Jacobson AM, Weinger K etal. Cognitive function in patients with insulin-dependent diabetes mellitus during hyperglycemia and hypoglycemia. Am J Med. 1995; 98: 135-144.
52. Ewing FM, Deary IJ, McCrimmon RJ, Strachan MW, Frier BM. Effect of acute hypoglycemia on visual information processing in adults with type 1 diabetes mellitus. Physiol Behav. 1998; 64: 653-660.
53. Gold AE, Deary IJ, MacLeod KM, Thomson KJ, Frier BM. Cognitive function during insulin-induced hypoglycemia in humans: Short-term cerebral adaptation does not occur. Psychopharmacology (Berl). 1995; 119: 325-333.
54. Howorka K, Pumprla J, Saletu B, Anderer P, Krieger M, Schabmann A. Decrease of vigilance assessed by EEG-mapping in Type I diabetic patients with history of recurrent severe hypoglycemia. Psychoneuroendocrinology. 2000; 25: 85-105.
55. McAulay V, Deary IJ, Sommerfield AJ, Frier BM. Attentional functioning is impaired during acute hypoglycaemia in people with type 1 diabetes. Diabet Med. 2005; 2005: 26-31.
56. McCrimmon RJ, Frier BM. Symptomatic and physiological responses to hypoglycaemia induced by human soluble insulin and the analogue Lispro human insulin. Diabet Med. 1997; 14: 929-936.
57. Musen G, Jacobson AM, Ryan CM etal. Impact of diabetes and its treatment on cognitive function among adolescents who participated in the Diabetes Control and Complications Trial. Diabetes Care. 2008; 31: 1933-1938.
58. Reichard P, Pihl M, Rosenqvist U, Sule J. Complications in IDDM are caused by elevated blood glucose level: The Stockholm Diabetes Intervention Study (SDIS) at 10-year follow up. Diabetologia. 1996; 39: 1483-1488.
59. Sommerfield AJ, Deary IJ, McAulay V, Frier BM. Short-term, delayed, and working memory are impaired during hypoglycemia in individuals with type 1 diabetes. Diabetes Care. 2003; 26: 390-396.
60. Strachan MW, Ewing FM, Frier BM, McCrimmon RJ, Deary IJ. Effects of acute hypoglycaemia on auditory information processing in adults with Type I diabetes. Diabetologia. 2003; 46: 97-105.
61. Wredling R, Levander S, Adamson U, Lins PE. Permanent neuropsychological impairment after recurrent episodes of severe hypoglycemia in man. Diabetologia. 1990; 33: 152-157.
62. Blakemore SJ, Choudhury S. Development of the adolescent brain: Implications for executive function and social cognition. J Child Psychol Psychiatry. 2006; 47: 296-312.
63. Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970; 45: 13-23.
64. Lezak MD, Howieson DB, Loring DW. Neuropsychological Assessment, 4th edn. Oxford University Press, Oxford, 2004.
65. Strauss E, Sherma EMS, Spreen O. A Compendium of Neuropsychological Tests, 3rd edn. Oxford University Press, Oxford, 2006.
66. Cohen J. Statistical Power Analysis for the Behavioral Sciences, 2nd edn. Lawrence erlbaum Associates, Hillsdale, NJ, 1988.
67. SIGNS. Critical appraisal: Notes and checklists. Available from: http://www.sign.ac.uk/methodology/checklists.html (accessed 12 January 2012).
68. Northam EA, Lin A. Hypoglycaemia in childhood onset type 1 diabetes: Part villain, but not the only one. Pediatr Diabetes. 2010; 11: 134-141.
69. Wysocki T, Harris MA, Mauras N etal. Absence of adverse effects of severe hypoglycemia on cognitive function in school-aged children with diabetes over 18 months. Diabetes Care. 2003; 26: 1100-1105.
70. Deary IJ, Crawford JR, Hepburn DA, Langan SJ, Blackmore LM, Frier BM. Severe hypoglycemia and intelligence in adult patients with insulin-treated diabetes. Diabetes. 1993; 42: 341-344.
71. Clausen TD, Mortensen EL, Schmidt L etal. Cognitive function in adult offspring of women with Type 1 diabetes. Diabet Med. 2011; 28: 838-844.
72. Gschwend S, Ryan C, Atchison J, Arslanian S, Becker D. Effects of acute hyperglycemia on mental efficiency and counterregulatory hormones in adolescents with insulin-dependent diabetes mellitus. J Pediatr. 1995; 126: 178-184.
73. Fanelli CG, Pampanelli S, Porcellati F etal. Rate of fall of blood glucose and physiological responses of counterregulatory hormones, clinical symptoms and cognitive function to hypoglycaemia in Type I diabetes mellitus in the postprandial state. Diabetologia. 2003; 46: 53-64.
74. Group TDCaCR. Effects of intensive diabetes therapy on neuropsychological function in adults in the Diabetes Control and Complications Trial. Ann Intern Med. 1996; 124: 379-388.
75. Jacobson AM, Ryan CM, Cleary PA etal. Biomedical risk factors for decreased cognitive functioning in type 1 diabetes: An 18 year follow-up of the Diabetes Control and Complications Trial (DCCT) cohort. Diabetologia. 2010; 54: 245-255.
76. Wessels AM, Scheltens P, Barkhof F, Heine RJ. Hyperglycaemia as a determinant of cognitive decline in patients with type 1 diabetes. Eur J Pharmacol. 2008; 585: 88-96.
77. Ferguson SC, Blane A, Perros P etal. Cognitive ability and brain structure in type 1 diabetes: Relation to microangiopathy and preceding severe hypoglycemia. Diabetes. 2003; 52: 149-156.
78. Li ZG, Sima AA. C-peptide and central nervous system complications in diabetes. Exp Diabesity Res. 2004; 5: 79-90.
79. Warren RE, Allen KV, Sommerfield AJ, Deary IJ, Frier BM. Acute hypoglycemia impairs nonverbal intelligence: Importance of avoiding ceiling effects in cognitive function testing. Diabetes Care. 2004; 27: 1447-1448.
80. Pramming S, Thorsteinsson B, Stigsby B, Binder C. Glycaemic threshold for changes in electroencephalograms during hypoglycaemia in patients with insulin dependent diabetes. Br Med J (Clin Res Ed). 1988; 296: 665-667.
81. Puente EC, Silverstein J, Bree AJ etal. Recurrent moderate hypoglycemia ameliorates brain damage and cognitive dysfunction induced by severe hypoglycemia. Diabetes. 2010; 59: 1055-1062.
82. Faraco CC, Unsworth N, Langley J etal. Complex span tasks and hippocampal recruitment during working memory. Neuroimage. 2011; 55: 773-787.
83. Park CR. Cognitive effects of insulin in the central nervous system. Neurosci Biobehav Rev. 2001; 25: 311-323.
84. Musen G, Lyoo IK, Sparks CR etal. Effects of type 1 diabetes on gray matter density as measured by voxel-based morphometry. Diabetes. 2006; 55(2): 326-333.
85. Thomas J, Garg ML, Smith DW. Altered expression of histone and synaptic plasticity associated genes in the hippocampus of streptozotocin-induced diabetic mice. Metab Brain Dis. 2013; 28: 613-618.
86. Lubin FD, Gupta S, Parrish RR, Grissom NM, Davis RL. Epigenetic mechanisms: Critical contributors to long-term memory formation. Neuroscientist. 2011; 17: 616-632.
87. Castellano V, White LJ. Serum brain-derived neurotrophic factor response to aerobic exercise in multiple sclerosis. J Neurol Sci. 2008; 269: 85-91.
88. Sanchez-Carrion R, Gomez PV, Junque C etal. Frontal hypoactivation on functional magnetic resonance imaging in working memory after severe diffuse traumatic brain injury. J Neurotrauma. 2008; 25: 479-494.
89. Bolo NR, Musen G, Jacobson AM etal. Brain activation during working memory is altered in patients with type 1 diabetes during hypoglycemia. Diabetes. 2011; 60: 3256-3264.
90. Barnea-Goraly N, Raman M, Mazaika P etal. Alterations in white matter structure in young children with type 1 diabetes. Diabetes Care. 2014; 37: 332-340.
91. Gonder-Frederick LA, Zrebiec JF, Bauchowitz AU etal. Cognitive function is disrupted by both hypo- and hyperglycemia in school-aged children with type 1 diabetes: A field study. Diabetes Care. 2009; 32: 1001-1006.
92. Chaytor N, Schmitter-Edgecombe M, Burr R. Improving the ecological validity of executive functioning assessment. Arch Clin Neuropsychol. 2006; 21: 217-227.
93. Rajashree R, Kholkute SD, Goudar SS. Effects of duration of diabetes on behavioural and cognitive parameters in streptozotocin-induced juvenile diabetic rats. Malays J Med Sci. 2011; 18: 26-31.
94. Tang M, Donaghue KC, Cho YH, Craig ME. Autonomic neuropathy in young people with type 1 diabetes: A systematic review. Pediatr Diabetes. 2013; 14: 239-248.
95. Ryan CM. Why is cognitive dysfunction associated with the development of diabetes early in life? The diathesis hypothesis. Pediatr Diabetes. 2006; 7(5): 289-297.
96. Musen G. Cognition and brain imaging in type 1 diabetes. Curr Diab Rep. 2008; 8(2): 132-137.
97. Kodl CT, Franc DT, Rao JP etal. Diffusion Tensor Imaging Identifies Deficits in White Matter Microstructure in Subjects With Type 1 Diabetes That Correlate With Reduced Neurocognitive Function. Diabetes. 2008; 57(11): 3083-3089.