The Acute Effects of Aerobic and Resistance Exercise on Blood Glucose Levels in Type 1 Diabetes

256 Pages·2011·4.56 MB·English

The Acute Effects of Aerobic and Resistance Exercise on
Blood Glucose Levels in Type 1 Diabetes

Jane Elizabeth Yardley

Thesis submitted to the
Faculty of Graduate and Postdoctoral Studies
In partial fulfillment of the requirements
For the PhD in Population Health

Institute of Population Health
University of Ottawa

© Jane Elizabeth Yardley, Ottawa, Canada, 2011
Abstract
Aerobic exercise interventions involving individuals with type 1 diabetes have had little
positive effect on blood glucose control as reflected by hemoglobin A . The few existing
1c
interventions involving resistance exercise, either alone or combined with aerobic exercise,
while small in sample size, have had better outcomes. The purpose of this research
program was to examine the changes in blood glucose levels during activity and for 24
hours post-exercise (as measured by continuous glucose monitoring) when resistance
exercise is performed, either on its own or combined with aerobic exercise, as compared to
aerobic exercise alone or no exercise. Twelve physically active individuals with type 1
diabetes performed 5 separate exercise sessions in random order separated by at least five
days: 1) no exercise/control; 2) aerobic exercise (45 minutes of treadmill running at 60%

VO ); 3) resistance exercise (45 minutes of weight lifting – 3 sets of 8 repetitions of 7
2peak
different exercises); 4) aerobic then resistance exercise (2 and 3 combined with the aerobic
exercise first); 5) resistance then aerobic exercise (2 and 3 combined with the resistance
exercise first). We found that resistance exercise was associated with a lower risk of
hypoglycemia during exercise, less carbohydrate intake during exercise, less post-exercise
hyperglycemia and more frequent (but less severe) nocturnal hypoglycemia than aerobic
exercise. When aerobic and resistance exercise were combined, performing resistance
exercise prior to aerobic exercise (rather than the reverse) resulted in attenuated declines in
blood glucose during aerobic exercise, accompanied by a lower need for carbohydrate
supplementation during exercise and a trend towards milder post-exercise nocturnal

hypoglycemia.
ii
Acknowledgements

I am extremely grateful for the support of both of my supervisors, Drs. Ronald Sigal and
Glen Kenny who have provided me with invaluable knowledge, guidance, support and
opportunities for personal growth throughout this project. I would also like to thank Dr.
Denis Prud’Homme for his input in the development of the project, Dr. Pierre Boulay for
his guidance and technical assistance, and Dr. Francois Haman for his advice, support, and
sharing of laboratory resources.

I was fortunate enough throughout my studies to have financial support from the Canadian
Diabetes Association in the form of a Doctoral Student Research Award, the Ottawa
Hospitals Research Institute Research Chair in Lifestyle Research, and the University of
Ottawa (Excellence Scholarship and Entrance Scholarship).

I would also like to express my gratitude to Drs. Michael Riddell, Bruce Perkins, Janine
Malcolm, Pascal Imbeault, and Mary-Ellen Harper who frequently made themselves
available to share their advice and expertise with me.

For their assistance in the laboratory, I would like to acknowledge Dr. Heather Wright, Ms.
Jerilee Barnett, Ms. Ghazal Bahman, and Ms. Nadia Balaa.

Finally, I would like to thank my family and friends who supported me both physically and
emotionally throughout my doctoral studies.
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TABLE OF CONTENTS

Table of Contents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . iv

List of Tables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . viii

List of Figures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . x

List of Appendices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xi

1.0 INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

1.1 Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

1.2 Objectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

1.3 Research Questions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

1.4 Research Hypotheses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

2.0 REVIEW OF THE LITERATURE . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

2.1 Glucose Homeostasis in Healthy Individuals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

2.1.1 Fasting Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

2.1.2 Postprandial Metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

2.1.3 Acute Effects of Aerobic Exercise on Glucose Homeostasis . . . . . . . . . . . . 11

2.1.4 Acute Effects of Anaerobic Exercise on Glucose Homeostasis . . . . . . . . . . 12

2.1.5 Acute Effects of Resistance Exercise on Glucose Homeostasis . . . . . . . . . . 13

2.2 Type 1 Diabetes Mellitus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

2.2.1 Management of Type 1 Diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15

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2.2.2 Insulin Therapy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

2.2.3 Diet . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

2.2.4 Physical Activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19

2.2.4a General Considerations for Exercise in Type 1 Diabetes . . . . . . . . . . . 19

2.3 Physical Activity in Type 1 Diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22

2.3.1 Potential Benefits of Physical Activity in Individuals with
Type 1 Diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23

2.4 The Chronic and Acute Effects of Exercise in Type 1 Diabetes . . . . . . . . . . . . 25

2.4.1 Aerobic Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25

2.4.1a General Adaptations to Aerobic Exercise Training . . . . . . . . . . . . . . . 25

2.4.1b Studies Examining Aerobic Exercise Training in Type 1
Diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

2.4.1c Acute Effects of Aerobic Exercise on Blood Glucose in
Type 1 Diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

2.4.2 Anaerobic Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29

2.4.2a General Adaptations to Anaerobic Exercise Training . . . . . . . . . . . . . 29

2.4.2b Studies Examining Anaerobic Exercise Training in Type 1
Diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30

2.4.2c Acute Effects of Anaerobic Exercise in Type 1 Diabetes . . . . . . . . . . 31

2.4.3 Resistance Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33

2.4.3a General Adaptations to Resistance Exercise Training . . . . . . . . . . . . . 33

2.4.3b Studies Examining Resistance Exercise Training in Type 1
Diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34

2.4.3c Acute Effects of Resistance Exercise in Type 1 Diabetes . . . . . . . . . . 37

2.5 Continuous Glucose Monitoring Systems (CGMS) . . . . . . . . . . . . . . . . . . . . . . 37

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3.0 PAPER 1

Aerobic exercise causes greater decreases in glycemia than resistance
exercise in type 1 diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41

Title Page . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45
Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53
Discussion/Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66
Tables and Figures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68

4.0 PAPER 2

Resistance exercise attenuates declines in blood glucose during subsequent
aerobic exercise in type 1 diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77

Title Page . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78
Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
Tables and Figures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104

5.0 PAPER 3

Effects on glycemia of performing resistance exercise before versus
after aerobic exercise in type 1 diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 110

Title Page . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 111
Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 112
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 114
Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115
Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122
Discussion/Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134
Tables and Figures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137

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6.0 GENERAL DISCUSSIONS AND CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . 147
6.1 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 148
6.2 Limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150
6.3 Relevance to Population Health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155
6.4 Future Research Considerations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 156
6.5 Summary and Recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158
6.6 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160

7.0 STATEMENT OF CONTRIBUTIONS OF CO-AUTHORS AND
COLLABORATORS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161

8.0 REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164

9.0 APPENDICES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 176
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LIST OF TABLES

REVIEW OF THE LITERATURE

Table 2.1 – Types of insulin and their characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
Table 2.2 – Responses to aerobic exercise in individuals with and without
type 1 diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
Table 2.3 – Responses to anaerobic exercise in individuals with and without
type 1 diabetes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31

PAPER 1

Table 1. Participant characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69
Table 2. Changes in glucose, non-esterified fatty acids, cortisol, insulin and growth
hormone throughout exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
Table 3. Changes in glucose, non-esterified fatty acids, cortisol, insulin and growth
hormone throughout recovery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71
Table 4. Summary of overnight continuous glucose monitoring data for the
night following exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
Table 5. Carbohydrate and insulin intake calculated from patient food and insulin
diaries. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .73

PAPER 2

Table 1. Changes in glucose, non-esterified fatty acids, cortisol, insulin and growth
hormone throughout exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 105
Table 2. Changes in glucose, non-esterified fatty acids, cortisol, insulin and growth
hormone throughout recovery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 106
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PAPER 3

Table 1. Participant characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 138
Table 2. Changes in glucose, non-esterified fatty acids, cortisol, insulin and growth
hormone throughout exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 139
Table 3. Changes in glucose, non-esterified fatty acids, cortisol, insulin and growth
hormone throughout recovery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141
Table 4. Carbohydrate intake and total daily insulin doses . . . . . . . . . . . . . . . . . . . . . . 142
Table 5. Summary of overnight continuous glucose monitoring data for the night
after exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143
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LIST OF FIGURES

PAPER 1

Figure 1. Plasma glucose during 45 minutes of exercise and 60 minutes of recovery . . . 74
Figure 2. Effect of 45 minutes of exercise and 60 minutes of recovery on mean
(±SE) non-esterified fatty acids (NEFA) (A), cortisol (B), insulin (C), and
growth hormone (D) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
Figure 3. Mean glucose as measured by continuous glucose monitoring from
1 to 12 hours post-exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76

PAPER 2

Figure 1. Plasma glucose during 45 minutes of aerobic exercise on its own or
after resistance exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 107
Figure 2. Effect of 45 minutes of aerobic exercise on its own or after resistance
exercise on (A) non-esterified fatty acids (NEFA), (B) growth hormone, (C)
insulin and (D) cortisol. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108
Figure 3. Mean glucose as measured by continuous glucose monitoring during the 12
hours post-exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 109

PAPER 3

Figure 1. Plasma glucose during exercise and recovery for aerobic exercise
performed before resistance exercise and resistance exercise performed
before aerobic exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 144
Figure 2. Effect of 90 minutes of exercise on (A) non-esterified fatty acids (NEFA),
(B) growth hormone, (C) insulin, and (D) cortisol . . . . . . . . . . . . . . . . . . . . . 145
Figure 3. Mean glucose as measured by continuous glucose monitoring from 1 to
12 hours post-exercise following aerobic exercise performed before
resistance exercise and resistance exercise performed before aerobic
exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146
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