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Exp Clin Endocrinol Diabetes 2023; 131(11): 605-614
DOI: 10.1055/a-2105-0799
Article

Aerobic Training Increases Hippocampal Volume and Protects Cognitive Function for Type 2 Diabetes Patients with Normal Cognition

Ying Wang
1   The First Affiliated Hospital of Hainan Medical University, Hainan Clinical Research Center for Metabolic Disease, Haikou, Hainan Province, China
,
Liping Wang
2   Department of Geriatrics, Affiliated Nanjing Brain Hospital, Nanjing Medical University, Nanjing, Jiangsu Province, China
,
Juan Yan
3   Jiangsu college of nursing, Huaian, Jiangsu Province, China
,
Xiaodan Yuan
4   Affiliated Hospital of Integrated Traditional Chinese and Western Medicine, Nanjing, University of Chinese Medicine, Nanjing, Jiangsu Province, China
,
Qing Q. Lou
1   The First Affiliated Hospital of Hainan Medical University, Hainan Clinical Research Center for Metabolic Disease, Haikou, Hainan Province, China
› Author Affiliations Funding Information the Six Talent Peaks Project – (2014-WSN-025)

Clinical Trials Registration: ClinicalTrials.gov NCT04489966
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Abstract

Aim To evaluate the effects of aerobic training on hippocampal volume and cognitive function in patients with type 2 diabetes mellitus (T2DM) with normal cognition.

Materials and methods One hundred patients with T2DM aged 60–75 years who met inclusion criteria were randomized into the aerobic training group (n=50) and control group (n=50). The aerobic training group received 1 year of aerobic training, while the control group maintained their lifestyle without additional exercise intervention. The primary outcomes were hippocampal volume measured by MRI and Mini-mental State Examination (MMSE) score or Montreal Cognitive Assessment scale (MoCA) scores.

Results Eighty-two participants completed the study (aerobic training group, n=40; control group, n=42). There was no significant difference between the two groups at baseline (P>0.05). After one year of moderate aerobic training, increase in total and right hippocampal volume in the aerobic training group were significantly higher than in the control group (P=0.027, P=0.043, respectively). In the aerobic group, total hippocampal volume significantly increased after the intervention compared with baseline (P=0.034). The between-group difference in the change of MMSE and MoCA scores was statistically significant (P=0.015, P=0.027, respectively). Logistic regression showed strong correlations between aerobic training and increase in total hippocampal volume (OR:1.091, [95%CI 0.969, 1.228], P=0.002), improvement of MMSE scores (OR:1.127, [95%CI 1.005, 1.263], P=0.041) or MoCA scores (OR:2.564, [95%CI 2.098.2.973], P=0.045).

Conclusions One-year moderate aerobic training increased total and right hippocampal volume and protected cognitive function for T2DM patients with normal cognition. Early intervention focusing on cognition protection should be considered for T2DM patients in clinical settings.

Key words

aerobic training - hippocampal volume - cognitive function - type 2 diabetes


Publication History

Received: 22 December 2022
Received: 25 May 2023

Accepted: 01 June 2023

Accepted Manuscript online:
02 June 2023

Article published online:
14 November 2023

© 2023. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Li W, Risacher SL, Huang E. et al. Type 2 diabetes mellitus is associated with brain atrophy and hypometabolism in the ADNI cohort. Neurology 2016; 87: 595-600
    CrossrefPubMedGoogle Scholar
  • 2 Kivipelto M, Uusitupa M, Soininen H. et al. History of medically treated diabetes and risk of Alzheimer disease in a nationwide case-control study. Diabetes Care 2013; 36: 2015-2019
    CrossrefPubMedGoogle Scholar
  • 3 Bohlken J, Jacob L, Kostev K. Progression of mild cognitive impairment to dementia in German specialist practices. Dementia (London) 2019; 18: 380-390
    CrossrefPubMedGoogle Scholar
  • 4 Alam MJ, Kitamura T, Saitoh Y. et al. Adult neurogenesis conserves hippocampal memory capacity. J Neurosci 2018; 38: 6854-6863
    CrossrefPubMedGoogle Scholar
  • 5 Mungas D, Harvey D, Reed BR. et al. Longitudinal volumetric MRI change and rate of cognitive decline. Neurology 2015; 65: 565-571
    CrossrefPubMedGoogle Scholar
  • 6 Woo H, Hong CJ, Jung S. et al. Chronic restraint stress induces hippocampal memory deficits by impairing insulin signaling. Mol Brain 2018; 11: 37
    CrossrefPubMedGoogle Scholar
  • 7 Van Harten B, Oosterman J, Muslimovic D. et al. Cognitive impairment and MRI correlates in the elderly patients with type 2 diabetes mellitus. Age Ageing 2007; 36: 164-170
    CrossrefPubMedGoogle Scholar
  • 8 Erickson KI, Voss MW, Prakash RS. et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA 2011; 108: 3017-3022
    CrossrefPubMedGoogle Scholar
  • 9 Anderson-Hanley C, Arciero PJ, Westen SC. et al. Neuropsychological benefits of stationary bike exercise and a cyber cycle exergame for older adults with diabetes: An exploratory analysis. J Diabetes Sci Technol 2012; 6: 849-857
    CrossrefPubMedGoogle Scholar
  • 10 Chang YK, Huang CJ, Chen KF. et al. Physical activity and working memory in healthy older adults: An ERP study. Psychophysiology 2013; 50: 1174-1182
    CrossrefPubMedGoogle Scholar
  • 11 Weng J, Ji L, Jia W. et al. Standards of care for type 2 diabetes in China. Diabetes Metab Res Rev 2016; 32: 442-458
    CrossrefPubMedGoogle Scholar
  • 12 Karvonen MJ, Kentala E, Mustala O. The effects of training on heart rate: A longitudinal study. Ann Med Exper Fenn 1957; 35: 307-315
    PubMedGoogle Scholar
  • 13 Robergs RA, Landwehr R. The surprising history of the' HRmax= 220-age' equation. J Exerc Physiol Online 2002; 5: 1-10
    PubMedGoogle Scholar
  • 14 Tanaka H, Monahan KG, Seals DS. Age – predicted maximal heart rate revisited. J Am Coll Cardiol 2001; 37: 153-156
    CrossrefPubMedGoogle Scholar
  • 15 Cuingnet R, Gerardin E, Tesieras J. et al. Automatic classification of patients with Alzheimer's disease from structural MRI: A comparison of ten methods using the ADNI database. Neuroimage 2011; 56: 766-781
    CrossrefPubMedGoogle Scholar
  • 16 Winblad B, Palmer kKivipelto M. et al. Mild cognitive impairment--beyond controversies, towards a consensus: Report of the international working group on mild cognitive impairment. J Intern Med 2004; 256: 240-246
    CrossrefPubMedGoogle Scholar
  • 17 Malykhin NV, Bouchard TP, Ogilvie CJ. et al. Three-dimensional volumetric analysis and reconstruction of amygdala and hippocampal head, body and tail. Psychiatry Res 2007; 155: 155-165
    CrossrefPubMedGoogle Scholar
  • 18 Agarwal N, Port JD. Neuroimaging: Anatomy Meets Function. Cham: Springer; 2017
    Google Scholar
  • 19 Frisoni GB, Jack CR, Bocchetta M. et al. The EADC-ADNI Harmonized Protocol form anual hippocampal segmentation on magnetic resonance: Evidence of validity. Alzheimers Dementia 2015; 11: 111-125
    CrossrefPubMedGoogle Scholar
  • 20 Folstein MF, Folstein SE, McHugh PR. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12: 189-198
    CrossrefPubMedGoogle Scholar
  • 21 Schrag A, Siddiqui UF, Anastasiou Z. et al. Clinical variables and biomarkers in prediction of cognitive impairment in patients with newly diagnosed Parkinson's disease: A cohort study. Lancet Neurol 2016; 16: 66-75
    CrossrefPubMedGoogle Scholar
  • 22 Li MY, Huang MM, Li SZ. et al. The effects of aerobic exercise on the structure and function of DMN-related brain regions: A systematic review. Int J Neurosci 2016; 127: 634-649
    CrossrefPubMedGoogle Scholar
  • 23 Stomby A, Otten J, Ryberg M. et al. A paleolithic diet with and without combined aerobic and resistance exercise increases functional brain responses and hippocampal volume in subjects with type 2 diabetes. Front Aging Neurosci 2017; 9: 391
    CrossrefPubMedGoogle Scholar
  • 24 Ten Brinke LF, Bolandzadeh N, Nagamatsu LS. et al. Aerobic exercise increases hippocampal volume in older women with probable mild cognitive impairment: A 6-month randomised controlled trial. Br J Sports Med 2015; 49: 248-254
    CrossrefPubMedGoogle Scholar
  • 25 Colcombe S, Kramer AF. Fitness effects on the cognitive function of older adults: A meta-analytic study. 2003; Psychol Sci 14: 125-130
    CrossrefPubMedGoogle Scholar
  • 26 Reske-Nielsen E, Lundbæk K, Rafaelsen OJ. Pathological changes in the central and peripheral nervous system of young long-term diabetics: I. Diabetic encephalopathy. Diabetologia 1966; 1: 233-241
    CrossrefPubMedGoogle Scholar
  • 27 Moran C, Phan TG, Chen J. et al. Brain atrophy in type 2 diabetes: Regional distribution and influence on cognition. Diabetes Care 2013; 36: 4036-4042
    CrossrefPubMedGoogle Scholar
  • 28 Neeper SA, Gómez-Pinilla F, Choi J. et al. Exercise and brain neurotrophins. Nature 1955; 373: 109
    CrossrefPubMedGoogle Scholar
  • 29 Mehta BK, Singh KK, Banerjee S. Effect of exercise on type 2 diabetes-associated cognitive impairment in rats. Int J Neurosci 2019; 129: 252-263
    CrossrefPubMedGoogle Scholar
  • 30 Adlard PA, Perreau VM, Engesser-Cesar C. et al. The timecourse of induction of brain-derived neurotrophic factor mRNA and protein in the rat hippocampus following voluntary exercise. Neurosci Lett 2004; 363: 43-48
    CrossrefPubMedGoogle Scholar
  • 31 Baker LD, Frank LL, Foster-Schubert K. et al. Effects of aerobic exercise on mild cognitive impairment: A controlled trial. Arch Neurol 2010; 67: 71-79
    CrossrefPubMedGoogle Scholar
  • 32 Ding Q, Vaynman S, Akhavan M. et al. Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 2016; 140: 823-833
    CrossrefPubMedGoogle Scholar
  • 33 Liu-Ambrose T, Donaldson MG. Exercise and cognition in older adults: Is there a role for resistance training programmes?. Br J Sports Med 2009; 43: 25-27
    CrossrefPubMedGoogle Scholar
  • 34 Teppala S, Shankar A. Association between serum IGF-1 and diabetes among U.S. adults. Diabetes Care 2009; 33: 2257-2259
    CrossrefPubMedGoogle Scholar
  • 35 Cassilhas RC, Lee KS, Fernandes J. et al. Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms. Neuroscience 2012; 202: 309-317
    CrossrefPubMedGoogle Scholar
  • 36 Frederiksen KS, Larsen CT, Hasselbalch SG. et al. A 16-week aerobic exercise intervention does not affect hippocampal volume and cortical thickness in mild to moderate Alzheimer's disease. Front Aging Neurosci 2018; 10: 293
    CrossrefPubMedGoogle Scholar
  • 37 Callisaya ML, Daly RM, Sharman JE. et al. Feasibility of a multi-modal exercise program on cognition in older adults with Type 2 diabetes – a pilot randomised controlled trial. BMC Geriatr 2017; 17: 237
    CrossrefPubMedGoogle Scholar
  • 38 Fiocco AJ, Scarcello S, Marzolini S. et al. The effects of an exercise and lifestyle intervention program on cardiovascular, metabolic factors and cognitive performance in middle-aged adults with type II diabetes: A pilot study. Can J Diabetes 2013; 37: 214-219
    CrossrefPubMedGoogle Scholar
  • 39 Woods SP, Delis DC, Scott JC. et al. The California Verbal Learning Test--second edition: Test-retest reliability, practice effects, and reliable change indices for the standard and alternate forms. Arch Clin Neuropsychol 2006; 21: 413-420
    CrossrefPubMedGoogle Scholar
  • 40 Siqueira GSA, Hagemann PMS, Coelho DS. et al. Can MoCA and MMSE be interchangeable cognitive screening tools? A systematic review. Gerontologist 2019; 59: e743-e763
    CrossrefPubMedGoogle Scholar
  • 41 De SRAL, Improta-Caria AC, Cassilhas RC. et al. Effects of physical exercise on memory in type 2 diabetes: A brief review. Metab. Brain Dis 2021; 1-5
    PubMedGoogle Scholar