Abstract
Exercise plays an important role in the management of diabetes and is associated with many benefits such as decreased morbidity and mortality. For people exhibiting signs and symptoms of cardiovascular disease, pre-exercise medical clearance is warranted; however, requiring broad screening requirements can lead to unnecessary barriers to initiating an exercise program. Robust evidence supports the promotion of both aerobic and resistance training, with evidence emerging on the importance of reducing sedentary time. For people with type 1 diabetes, there are special considerations, including hypoglycemia risk and prevention, exercise timing (including prandial status), and differences in glycemic responses based on biological sex.
Physical activity has long been considered an important component of diabetes management (1). Regular exercise (planned, structured physical activity) provides substantial health benefits to individuals with diabetes, and practice guidelines (2–7) consistently call for exercise training to be part of standard therapy for diabetes. Nevertheless, 50–79% of this population remains insufficiently active (8–11), and many who begin a regular exercise program do not continue over the long term (11). Common barriers include perceived lack of time, low motivation, lack of social support, cost, and health concerns (12). Health care professionals (HCPs) and community exercise programs can play an important role in supporting people with diabetes. This article gives an overview of considerations and suggestions on where to start when recommending and discussing physical activity with people with diabetes.
Pre-Exercise Evaluation
Although strong evidence supports the promotion of physical activity in adults with diabetes, the most appropriate way to screen and evaluate people with diabetes ahead of exercise participation has remained somewhat controversial. Although people with diabetes who are middle-aged or older tend to have higher cardiovascular disease (CVD) risk than their peers without diabetes, it is important to put the risks into perspective, as the barriers and risks of inactivity in this population are also considerable. For most people with diabetes, the risks of morbidity and mortality associated with being sedentary are considerably greater than the risks associated with exercise.
Medical Clearance
Traditionally, several professional organizations have promoted survey questionnaires to screen and identify at-risk individuals who should be medically evaluated before initiating an exercise training program (13–16). However, given the high prevalence of CVD risk factors and use of antihypertensive medications and statins in people with diabetes, this approach has proven to be too inclusive (17), with virtually all people with diabetes required to obtain medical clearance ahead of participating in an exercise program, according to these algorithms. Accordingly, updated American College of Sports Medicine (ACSM) guidelines (4) and consensus statements (3) have slightly relaxed this guidance by discontinuing the need for medical clearance before participation in moderate activity for people with diabetes who are currently active. However, these recommendations still suggest that all individuals with diabetes who are currently sedentary, which is a large portion of people with diabetes of any type, obtain medical clearance ahead of participation in moderate, or even light, exercise training.
These available screening surveys and guideline algorithms result in a high number of medical referrals and can create another barrier for sedentary adults to become more physically active. Programs that require a “pre-participation form” to be completed by a medical HCP place the burden of completing this administrative task, and any associated costs, on participants. If HCPs in turn require a physical examination and/or exercise stress testing before completing these forms, individuals may have to coordinate time off of work, child care, and transportation to a medical visit, at which they may be responsible for a copayment and related costs. In some populations, access to a primary care clinician can also be a significant barrier. Because habitually sedentary individuals with diabetes often perceive numerous barriers to the initiation and maintenance of a physical activity program (18), being judicious regarding the need for medical clearance may help to reduce this barrier.
Pre-Participation Exercise Stress Testing
Controversy also remains regarding the use of pre-participation exercise stress testing for screening purposes. Although exercise stress testing can be valuable in the development of an exercise prescription, measurement of cardiorespiratory fitness, and assessment of long-term prognosis (19), concerns about costs, barriers, follow-up with expensive/invasive tests, and potential low yield suggest that it may be impractical to screen asymptomatic individuals with diabetes who want to begin a moderate-intensity exercise training program. Several trials investigating screening for coronary artery disease (CAD) in asymptomatic people with diabetes found that such screening did not reduce cardiac event rates at follow-up (20–22). Accordingly, guidelines (23,24) do not recommend routine CAD screening in people with diabetes.
However, this evidence does not necessarily apply to individuals who wish to initiate exercise. Although recommended by ACSM (4), the utility of pre-participation exercise stress testing in asymptomatic adults with diabetes is unclear. A study (25) in 1,705 people with type 2 diabetes who were referred for supervised exercise reported that the rate of major cardiovascular outcomes was very low (<1%), with no difference between those who underwent stress testing and those who did not, over a follow-up period of 3.4 years. Adverse events were more likely to occur during the follow-up period in participants who reported symptoms of chest pain, had experienced a previous cardiovascular event, or had known CAD, arrhythmias, congestive heart failure (CHF), and/or microvascular complications. No evidence currently exists on the usefulness of pre-participation screening for resistance exercise training.
Where to Start?
We suggest that required medical clearance for exercise participation be reserved for individuals who report signs and symptoms suggestive of CVD (Table 1) and for middle-aged and older individuals with diabetes who are not already exercising regularly and who want to begin a very-high-intensity exercise program. Because people with long-term or complicated diabetes who are not appropriately managed medically may be at an increased risk of silent ischemia, ensuring that participants have been medically evaluated within the past 12 months may be good practice. Furthermore, HCPs may want to consider pre-participation exercise stress testing for individuals who are symptomatic or have known CAD, arrhythmias, CHF, and/or microvascular complications and for those planning very vigorous exercise, such as racing, long-distance running, or high-intensity interval training (HIIT). HCPs may also want to consider a stress test for anyone they suspect may be ignoring symptoms or not giving an accurate history.
Table 1.
CVD Status
Signs and symptoms suggestive of CVD include:
|
Known CVD includes a history of:
|
Because these suggestions limit the need for medical clearance, it is important that HCPs and exercise program staff have an understanding of this approach. The reduced need for medical clearance does put the impetus on these professionals to be especially vigilant about screening for and educating participants about the warning signs and symptoms suggestive of CVD, particularly at the time an exercise program is started and/or when the exercise intensity is increased.
Exercise Recommendations
As discussed above, “exercise” is planned, structured physical activity. These recommendations are focused on these activities rather than on unstructured physical movement, with the exception of reducing sedentary time.
Aerobic and Resistance Exercise
Aerobic exercise, such as walking, bicycling, swimming, or jogging, involves continuous, rhythmic movements of large muscle groups. When performed regularly, aerobic exercise training increases cardiorespiratory fitness. Resistance exercise training, or strength training, involves brief repetitive exercises with free weights, weight machines, resistance bands, or one’s own body weight. When performed regularly, resistance exercise training increases muscular strength and endurance.
Both aerobic and resistance training decrease insulin resistance, and randomized trials have shown that both training types reduce A1C in individuals with type 2 diabetes (26–28), and their combination is likely to be more effective than either type of exercise alone (29). Large, long-term cohort studies have shown that people with diabetes who exercise more have lower cardiovascular and overall mortality rates than those who exercise less (30–34). For these reasons, both regular aerobic and resistance exercise are recommended for people with diabetes. Several professional organizations, including the American Diabetes Association (2), ACSM (3), and Diabetes Canada (5) recommend the accumulation of a minimum of 150 minutes of aerobic exercise per week, spread over at least 3 days and with no more than 2 days without aerobic exercise, and at least two (but preferably three) sessions per week of resistance exercise on nonconsecutive days.
However, many people with diabetes perform very little physical activity and would find it daunting to attempt to meet these goals right away. For very sedentary middle-aged and older people, it may be advisable to begin with very modest goals, such as walking for 5–10 minutes/day, and to gradually increase these amounts every week over a period of several months. Many people prefer to perform several shorter sessions of exercise each day rather than a single longer session (e.g., three 10-minute sessions rather than a single 30-minute session), and the glycemic benefits of doing either may be similar (35).
Strength training is particularly beneficial for people with diabetes. Muscle strength and muscle mass tend to decline with age, especially after the age of 60 years, and these age-related declines tend to be more marked in older adults with diabetes than in those without diabetes (36). Reductions in muscle strength and bulk can result in reduced function, disability, and difficulty with activities of daily living (37).
Pain from osteoarthritis can be a barrier to physical activity (38). Water-based activities, such as walking in a pool, swimming, or aquatic exercise classes, can be recommended for people with osteoarthritis pain (39,40). In adults with type 2 diabetes, a meta-analysis found that aquatic exercise training reduces A1C by about the same amount as nonaquatic aerobic exercise (41). Using exercise equipment such as a recumbent bike or elliptical machine that reduce impact and shear force can also be helpful.
HIIT
HIIT involves alternating between periods of higher- and lower-intensity exercise in a single session. This type of training results in larger gains in cardiorespiratory fitness than continuous moderate-intensity training (42,43). Some trials have found that HIIT causes greater reductions in A1C than continuous moderate-intensity aerobic training in people with type 2 diabetes (44,45). In type 1 diabetes, some studies have found that HIIT results in less hypoglycemia during exercise compared with continuous aerobic training (46–48).
Supervised Exercise Training
Although not always feasible or affordable, supervised exercise training is particularly beneficial in people with diabetes. A systematic review and meta-analysis found that, for both aerobic and resistance training in people with type 2 diabetes, supervised exercise programs resulted in reduced A1C regardless of whether there was a dietary cointervention, whereas unsupervised programs reduced A1C only if there was also a dietary intervention (26). A meta-analysis of resistance exercise intervention trials in type 2 diabetes found that programs with less supervision showed less favorable changes in A1C, insulin resistance, and body composition than programs with more supervision (49). A randomized trial compared 12 months of twice-weekly supervised aerobic and resistance exercise plus exercise counseling versus exercise counseling alone in people with type 2 diabetes and metabolic syndrome (50). The group receiving the supervised exercise training had significantly greater reductions in A1C, blood pressure, BMI, and waist circumference and greater increases in cardiorespiratory fitness, strength, and HDL cholesterol compared with the group receiving exercise counseling alone (50). Although expensive, supervised exercise training can be cost-effective in type 2 diabetes (51).
Reduced Sedentary Time
Sedentary behavior involves prolonged sitting or reclining while awake, such as when using a computer, watching TV or videos, or driving. Observational studies have shown associations between larger amounts of sedentary time and higher mortality in people with and without diabetes, even after adjusting for time spent doing physical activity (52–55). Small trials have shown that interrupting sitting time with light walking or light resistance exercise for several minutes at a time over the course of a day can reduce postprandial increases in glucose, insulin, and triglycerides (56–58). Therefore, reducing sedentary time is an important goal, in addition to increasing physical activity. A suggested initial activity plan for a person new to exercise is provided in Table 2 (5).
Table 2.
Suggested Initial Activity Plan for a Person New to Exercise
| Aerobic exercise: |
|
| Resistance exercise: |
|
| Sedentary time: |
|
Adapted from ref. 5.
Special Considerations for People With Type 1 Diabetes
Three main areas worthy of discussion related to becoming and staying physically active—especially for anyone with type 1 diabetes or anyone who takes mealtime insulin—are hypoglycemia risk and prevention, exercise timing (including prandial status), and differences in glycemic responses based on biological sex. These areas should be addressed when planning where to start with being active and overcoming barriers to participation. Additional strategies to support greater exercise participation in all adults with diabetes are given in Table 3.
Table 3.
Sample Strategies to Help Support Exercise in People With Diabetes
|
Hypoglycemia Risk and Prevention Around Activities
Fear of hypoglycemia has long been reported as a barrier to regular physical activity in individuals with type 1 diabetes of various ages (59–62), for good reason. A number of factors increase the risk of hypoglycemia around physical activity, and hypoglycemia risk can vary according to the type, intensity, and duration of the activity (63–65). In many studies, most aerobic exercise appeared to lower blood glucose, whereas intense activity (such as interval training or heavy resistance exercise) raised it, at least temporarily (66–68). However, glycemic responses can also vary based on prandial status (69), time of day, sex, and the total volume of activity (70).
The exogenous insulin on board during physical activities can also affect hypoglycemia risk, with higher insulin levels raising hypoglycemia risk, possibly related in part to the later peaks and longer durations of action of higher doses of rapid-acting insulin types (71). Increases in blood flow related to physical activity can lead to faster insulin absorption from subcutaneous depots, increasing circulating insulin levels and, consequently, raising the risk for exercise-induced hypoglycemia (72), although hypoglycemia frequently can be prevented by lowering insulin doses before activities or insulin delivery via an insulin pump during activities (73–77). Moreover, other factors such as inadequate or restricted carbohydrate intake (78–80), failure to monitor glucose levels, and exercising in the heat may, in some cases, increase the risk of hypoglycemia. Even undertaking new or unfamiliar activities presents a higher risk because of greater blood glucose use until a training effect increases fat utilization as an alternate fuel (81).
To further compound hypoglycemia risk, not all exercise-related events occur during activities. In some cases, the risk has been shown to be biphasic, occurring both immediately after the cessation of activity and again 7–11 hours later and up to 24 hours or more after exercising (82,83). When substantial amounts of muscle glycogen are used during an activity of any type, the risk for later-onset hypoglycemia appears to be greater. In particular, repeated interval workouts or intense resistance training can result in substantial glycogen depletion, thereby increasing hypoglycemia risk (84) and suggesting that post-exercise vigilance and possible insulin reductions and increased carbohydrate intake may be warranted to prevent hypoglycemia (85,86).
Finally, it has long been reported that individuals with type 1 diabetes may have multiple impairments in their counterregulatory hormone response to hypoglycemia, placing them at high risk for severe hypoglycemia, especially during subsequent hypoglycemia or exercise (87). Most individuals with type 1 diabetes eventually develop a diminished glucagon response to hypoglycemia (88), and their epinephrine release may also be blunted during both exercise and hypoglycemia. Exercise itself may also reduce their subsequent counterregulatory responses to hypoglycemia on the same day or the next day (89,90).
Exercise Timing and Prandial Status
For individuals with type 1 diabetes, it may be that exercise timing and prandial status (e.g., exercising after an overnight fast and before eating breakfast) has a bigger impact on keeping blood glucose levels stable or higher during activity than the type of exercise undertaken (69). Performing exercise training first thing in the morning usually results in different glycemic outcomes than doing the same activity in a fed state later in the day. In 35 adults with type 1 diabetes using sensor-augmented insulin pumps, 60 minutes of moderate aerobic exercise on a treadmill before breakfast resulted in less hypoglycemia and more time in the target glycemic range than the same exercise performed in the afternoon on another day (91).
Similarly, in a small study involving 12 active participants with type 1 diabetes who undertook sprint interval training before breakfast or before dinner, the morning activity raised their blood glucose during and after the activity, whereas activity later in the day caused a decline both during the activity and the hour following it (92). Likewise, pre-breakfast resistance exercise increased blood glucose in eight participants with type 1 diabetes (93), but afternoon resistance exercise decreased blood glucose in 12 others (94). Conversely, in another group of 12 habitually active adult participants with type 1 diabetes using continuous glucose monitoring, overall glycemia, time in range, and other glycemic variables were largely unchanged during the 24-hour period after either aerobic or resistance exercise performed in the late afternoon, suggesting that both types of activity undertaken at that time of day had a similar glycemic impact (95). Thus, undertaking fasted exercise in the morning may help to prevent hypoglycemia.
Impact of Biological Sex
Biological sex has long been investigated as a basis for differences in counterregulatory hormonal responses to exercise (96–98), with reduced responses in males with type 1 diabetes likely leading to a higher risk of hypoglycemia after recent exercise (99) and a blunted hormonal response to exercise after hypoglycemia (100) compared with females with type 1 diabetes. In adults without diabetes, sex-related differences in hormonal responses to exercise may result in altered fuel metabolism during exercise (101,102). In individuals with type 1 diabetes, the advent of attempted closed-loop insulin delivery systems has raised this question again because hormonal fluxes could potentially impact insulin dosing (103). In females with type 1 diabetes, at least one study has suggested that they may experience smaller declines in blood glucose during exercise and a lower risk of late-onset hypoglycemia after acute resistance exercise compared with males (104), perhaps due to higher estrogen levels after resistance exercise, resulting in higher lipid and lower blood glucose use. Also, in females with type 1 diabetes, blood glucose levels are generally higher during the luteal phase of the menstrual cycle, when estradiol and other hormones surge (105). In a cross-sectional study, more males than females with type 1 diabetes reported consuming extra carbohydrates, both before and during physical activity, as a strategy to prevent hypoglycemia (106). More investigation into the potential impact of these differences in exercise responses and hypoglycemia risk related to biological sex is warranted (107).
Conclusion
When recommending exercise for, or even discussing activity with, people with any type of diabetes, it is important to know where to start. In most cases, requiring pre-participation screening, exercise stress testing, or medical clearance creates a barrier to increased exercise that poses more of a risk for individuals than starting activity would. Use such requirements judiciously and mainly for people with signs and symptoms of CVD or those who want to undertake very vigorous exercise. Most individuals will benefit from regular aerobic and resistance exercise training, although starting levels may need to be much lower than recommended daily and weekly target amounts. Reducing sedentary time should be recommended to all. Finally, individuals with type 1 diabetes and other insulin users require consideration of hypoglycemia risk and prevention, exercise timing, and differences in glycemic responses when planning where to start with being active and overcoming barriers to participation.
References
- 1. Joslin EP. The Treatment of Diabetes Mellitus. Philadelphia, PA, and New York, Lea & Febiger, 1917 [Google Scholar]
- 2. Colberg SR, Sigal RJ, Yardley JE, et al. Physical activity/exercise and diabetes: a position statement of the American Diabetes Association. Diabetes Care 2016;39:2065–2079 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Kanaley JA, Colberg SR, Corcoran MH, et al. Exercise/physical activity in individuals with type 2 diabetes: a consensus statement from the American College of Sports Medicine. Med Sci Sports Exerc 2022;54:353–368 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. Liguori G, Feito Y, Fountaine C, Roy B. ACSM’s Guidelines for Exercise Testing and Prescription. 11th ed. Philadelphia, PA, Wolters Kluwer, 2022 [Google Scholar]
- 5. Diabetes Canada Clinical Practice Guidelines Expert Committee; Sigal RJ, Armstrong MJ, Bacon SL, et al. Physical activity and diabetes. Can J Diabetes 2018;42(Suppl. 1):S54–S63 [DOI] [PubMed] [Google Scholar]
- 6. Hordern MD, Dunstan DW, Prins JB, Baker MK, Singh MA, Coombes JS. Exercise prescription for patients with type 2 diabetes and pre-diabetes: a position statement from Exercise and Sport Science Australia. J Sci Med Sport 2012;15:25–31 [DOI] [PubMed] [Google Scholar]
- 7. Nagi D, Gallen I. The Association of British Clinical Diabetologists position statement on physical activity and exercise in diabetes. Pract Diabetes Int 2010;27:158a–163a [Google Scholar]
- 8. Zhang X, Geiss LS, Caspersen CJ, et al. Physical activity levels and differences in the prevalence of diabetes between the United States and Canada. Prev Med 2010;50:241–245 [DOI] [PubMed] [Google Scholar]
- 9. Blackwell DL, Lucas JW, Clarke TC. Summary health statistics for U.S. adults: National Health Interview Survey, 2012. Vital Health Stat 10 2014;260:1–161 [PubMed] [Google Scholar]
- 10. Johnson PJ, Ghildayal N, Rockwood T, Everson-Rose SA. Differences in diabetes self-care activities by race/ethnicity and insulin use. Diabetes Educ 2014;40:767–777 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Morrato EH, Hill JO, Wyatt HR, Ghushchyan V, Sullivan PW. Physical activity in U.S. adults with diabetes and at risk for developing diabetes, 2003. Diabetes Care 2007;30:203–209 [DOI] [PubMed] [Google Scholar]
- 12. Korkiakangas EE, Alahuhta MA, Laitinen JH. Barriers to regular exercise among adults at high risk or diagnosed with type 2 diabetes: a systematic review. Health Promot Int 2009;24:416–427 [DOI] [PubMed] [Google Scholar]
- 13. Warburton DE, Jamnik VK, Bredin SS, Gledhill N. The Physical Activity Readiness Questionnaire for Everyone (PAR-Q+) and Electronic Physical Activity Readiness Medical Examination (ePARmed-X+). Health and Fitness Journal of Canada 2011;4:3–17 [Google Scholar]
- 14. Bredin SS, Gledhill N, Jamnik VK, Warburton DE. PAR-Q+ and ePARmed-X+: new risk stratification and physical activity clearance strategy for physicians and patients alike. Can Fam Physician 2013;59:273–277 [PMC free article] [PubMed] [Google Scholar]
- 15. Grundy SM, Stone NJ, Bailey AL, et al. 2018 AHA/ACC/AACVPR/AAPA/ABC/ACPM/ADA/AGS/APhA/ASPC/NLA/PCNA guideline on the management of blood cholesterol: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Am Coll Cardiol 2019;73:e285–e350 [DOI] [PubMed] [Google Scholar]
- 16. Balady GJ, Chaitman B, Driscoll D, et al. Recommendations for cardiovascular screening, staffing, and emergency policies at health/fitness facilities. Circulation 1998;97:2283–2293 [DOI] [PubMed] [Google Scholar]
- 17. Whitfield GP, Pettee Gabriel KK, Rahbar MH, Kohl HW 3rd. Application of the American Heart Association/American College of Sports Medicine adult preparticipation screening checklist to a nationally representative sample of US adults aged ≥40 years from the National Health and Nutrition Examination Survey 2001 to 2004. Circulation 2014;129:1113–1120 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Bauman AE, Sallis JF, Dzewaltowski DA, Owen N. Toward a better understanding of the influences on physical activity: the role of determinants, correlates, causal variables, mediators, moderators, and confounders. Am J Prev Med 2002;23(Suppl. 2):5–14 [DOI] [PubMed] [Google Scholar]
- 19. Ashley EA, Myers J, Froelicher V. Exercise testing in clinical medicine. Lancet 2000;356:1592–1597 [DOI] [PubMed] [Google Scholar]
- 20. Muhlestein JB, Lappé DL, Lima JA, et al. Effect of screening for coronary artery disease using CT angiography on mortality and cardiac events in high-risk patients with diabetes: the FACTOR-64 randomized clinical trial. JAMA 2014;312:2234–2243 [DOI] [PubMed] [Google Scholar]
- 21. Young LH, Wackers FJT, Chyun DA, et al.; DIAD Investigators . Cardiac outcomes after screening for asymptomatic coronary artery disease in patients with type 2 diabetes: the DIAD study: a randomized controlled trial. JAMA 2009;301:1547–1555 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Lièvre MM, Moulin P, Thivolet C, et al.; DYNAMIT investigators . Detection of silent myocardial ischemia in asymptomatic patients with diabetes: results of a randomized trial and meta-analysis assessing the effectiveness of systematic screening. Trials 2011;12:23. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Jonas DE, Reddy S, Middleton JC, et al. Screening for cardiovascular disease risk with resting or exercise electrocardiography: evidence report and systematic review for the US Preventive Services Task Force. JAMA 2018;319:2315–2328 [DOI] [PubMed] [Google Scholar]
- 24. American Diabetes Association Professional Practice Committee . Introduction: Standards of Medical Care in Diabetes—2022. Diabetes Care 2021;45(Suppl. 1):S1–S2 [DOI] [PubMed] [Google Scholar]
- 25. Armstrong MJ, Rabi DM, Southern DA, Nanji A, Ghali WA, Sigal RJ. Clinical utility of pre-exercise stress testing in people with diabetes. Can J Cardiol 2019;35:185–192 [DOI] [PubMed] [Google Scholar]
- 26. Umpierre D, Ribeiro PA, Kramer CK, et al. Physical activity advice only or structured exercise training and association with HbA1c levels in type 2 diabetes: a systematic review and meta-analysis. JAMA 2011;305:1790–1799 [DOI] [PubMed] [Google Scholar]
- 27. Umpierre D, Ribeiro PA, Schaan BD, Ribeiro JP. Volume of supervised exercise training impacts glycaemic control in patients with type 2 diabetes: a systematic review with meta-regression analysis. Diabetologia 2013;56:242–251 [DOI] [PubMed] [Google Scholar]
- 28. Liubaoerjijin Y, Terada T, Fletcher K, Boulé NG. Effect of aerobic exercise intensity on glycemic control in type 2 diabetes: a meta-analysis of head-to-head randomized trials. Acta Diabetol 2016;53:769–781 [DOI] [PubMed] [Google Scholar]
- 29. Sigal RJ, Kenny GP, Boulé NG, et al. Effects of aerobic training, resistance training, or both on glycemic control in type 2 diabetes: a randomized trial. Ann Intern Med 2007;147:357–369 [DOI] [PubMed] [Google Scholar]
- 30. Gregg EW, Gerzoff RB, Caspersen CJ, Williamson DF, Narayan KM. Relationship of walking to mortality among US adults with diabetes. Arch Intern Med 2003;163:1440–1447 [DOI] [PubMed] [Google Scholar]
- 31. Hu FB, Stampfer MJ, Solomon C, et al. Physical activity and risk for cardiovascular events in diabetic women. Ann Intern Med 2001;134:96–105 [DOI] [PubMed] [Google Scholar]
- 32. Hu G, Jousilahti P, Barengo NC, Qiao Q, Lakka TA, Tuomilehto J. Physical activity, cardiovascular risk factors, and mortality among Finnish adults with diabetes. Diabetes Care 2005;28:799–805 [DOI] [PubMed] [Google Scholar]
- 33. Moy CS, Songer TJ, LaPorte RE, et al. Insulin-dependent diabetes mellitus, physical activity, and death. Am J Epidemiol 1993;137:74–81 [DOI] [PubMed] [Google Scholar]
- 34. Tikkanen-Dolenc H, Wadén J, Forsblom C, et al.; FinnDiane Study Group . Frequent and intensive physical activity reduces risk of cardiovascular events in type 1 diabetes. Diabetologia 2017;60:574–580 [DOI] [PubMed] [Google Scholar]
- 35. Eriksen L, Dahl-Petersen I, Haugaard SB, Dela F. Comparison of the effect of multiple short-duration with single long-duration exercise sessions on glucose homeostasis in type 2 diabetes mellitus. Diabetologia 2007;50:2245–2253 [DOI] [PubMed] [Google Scholar]
- 36. Jang HC. Sarcopenia, frailty, and diabetes in older adults. Diabetes Metab J 2016;40:182–189 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37. Omura T, Araki A. Skeletal muscle as a treatment target for older adults with diabetes mellitus: the importance of a multimodal intervention based on functional category. Geriatr Gerontol Int 2022;22:110–120 [DOI] [PubMed] [Google Scholar]
- 38. Bolen J, Hootman J, Helmick CG, Murphy L, Langmaid G; Centers for Disease Control and Prevention (CDC) . Arthritis as a potential barrier to physical activity among adults with diabetes: United States, 2005 and 2007. MMWR Morb Mortal Wkly Rep 2008;57:486–489 [PubMed] [Google Scholar]
- 39. Lu M, Su Y, Zhang Y, et al. Effectiveness of aquatic exercise for treatment of knee osteoarthritis: systematic review and meta-analysis. Z Rheumatol 2015;74:543–552 [DOI] [PubMed] [Google Scholar]
- 40. Waller B, Ogonowska-Slodownik A, Vitor M, et al. Effect of therapeutic aquatic exercise on symptoms and function associated with lower limb osteoarthritis: systematic review with meta-analysis. Phys Ther 2014;94:1383–1395 [DOI] [PubMed] [Google Scholar]
- 41. Rees JL, Johnson ST, Boulé NG. Aquatic exercise for adults with type 2 diabetes: a meta-analysis. Acta Diabetol 2017;54:895–904 [DOI] [PubMed] [Google Scholar]
- 42. Weston KS, Wisløff U, Coombes JS. High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis. Br J Sports Med 2014;48:1227–1234 [DOI] [PubMed] [Google Scholar]
- 43. Jelleyman C, Yates T, O’Donovan G, et al. The effects of high-intensity interval training on glucose regulation and insulin resistance: a meta-analysis. Obes Rev 2015;16:942–961 [DOI] [PubMed] [Google Scholar]
- 44. Curry M, Mehta SP, Chaffin JC, Duran E, Washington B, Bose SS. The effect of low-volume, high-intensity interval training on blood glucose markers, anthropometric measurements, and cardiorespiratory fitness in patients with type 2 diabetes. Crit Rev Phys Rehabil Med 2015;27:19–35 [Google Scholar]
- 45. Francois ME, Little JP. Effectiveness and safety of high-intensity interval training in patients with type 2 diabetes. Diabetes Spectr 2015;28:39–44 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46. Bally L, Zueger T, Buehler T, et al. Metabolic and hormonal response to intermittent high-intensity and continuous moderate intensity exercise in individuals with type 1 diabetes: a randomised crossover study. Diabetologia 2016;59:776–784 [DOI] [PubMed] [Google Scholar]
- 47. Moser O, Tschakert G, Mueller A, et al. Effects of high-intensity interval exercise versus moderate continuous exercise on glucose homeostasis and hormone response in patients with type 1 diabetes mellitus using novel ultra-long-acting insulin. PLoS One 2015;10:e0136489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48. Iscoe KE, Riddell MC. Continuous moderate-intensity exercise with or without intermittent high-intensity work: effects on acute and late glycaemia in athletes with type 1 diabetes mellitus. Diabet Med 2011;28:824–832 [DOI] [PubMed] [Google Scholar]
- 49. Gordon BA, Benson AC, Bird SR, Fraser SF. Resistance training improves metabolic health in type 2 diabetes: a systematic review. Diabetes Res Clin Pract 2009;83:157–175 [DOI] [PubMed] [Google Scholar]
- 50. Balducci S, Zanuso S, Nicolucci A, et al.; Italian Diabetes Exercise Study (IDES) Investigators . Effect of an intensive exercise intervention strategy on modifiable cardiovascular risk factors in subjects with type 2 diabetes mellitus: a randomized controlled trial: the Italian Diabetes and Exercise Study (IDES). Arch Intern Med 2010;170:1794–1803 [DOI] [PubMed] [Google Scholar]
- 51. Coyle D, Coyle K, Kenny GP, et al. Cost-effectiveness of exercise programs in type 2 diabetes. Int J Technol Assess Health Care 2012;28:228–234 [DOI] [PubMed] [Google Scholar]
- 52. Biswas A, Oh PI, Faulkner GE, et al. Sedentary time and its association with risk for disease incidence, mortality, and hospitalization in adults: a systematic review and meta-analysis. Ann Intern Med 2015;162:123–132 [DOI] [PubMed] [Google Scholar]
- 53. Wilmot EG, Edwardson CL, Achana FA, et al. Sedentary time in adults and the association with diabetes, cardiovascular disease and death: systematic review and meta-analysis. Diabetologia 2012;55:2895–2905 [DOI] [PubMed] [Google Scholar]
- 54. Loprinzi PD, Sng E. The effects of objectively measured sedentary behavior on all-cause mortality in a national sample of adults with diabetes. Prev Med 2016;86:55–57 [DOI] [PubMed] [Google Scholar]
- 55. Glenn KR, Slaughter JC, Fowke JH, et al. Physical activity, sedentary behavior and all-cause mortality among Blacks and Whites with diabetes. Ann Epidemiol 2015;25:649–655 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56. Dunstan DW, Kingwell BA, Larsen R, et al. Breaking up prolonged sitting reduces postprandial glucose and insulin responses. Diabetes Care 2012;35:976–983 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57. Dempsey PC, Larsen RN, Sethi P, et al. Benefits for type 2 diabetes of interrupting prolonged sitting with brief bouts of light walking or simple resistance activities. Diabetes Care 2016;39:964–972 [DOI] [PubMed] [Google Scholar]
- 58. Duvivier BM, Schaper NC, Hesselink MK, et al. Breaking sitting with light activities vs structured exercise: a randomised crossover study demonstrating benefits for glycaemic control and insulin sensitivity in type 2 diabetes. Diabetologia 2017;60:490–498 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59. Brazeau AS, Rabasa-Lhoret R, Strychar I, Mircescu H. Barriers to physical activity among patients with type 1 diabetes. Diabetes Care 2008;31:2108–2109 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 60. Jabbour G, Henderson M, Mathieu ME. Barriers to active lifestyles in children with type 1 diabetes. Can J Diabetes 2016;40:170–172 [DOI] [PubMed] [Google Scholar]
- 61. Cigrovski Berkovic M, Bilic-Curcic I, La Grasta Sabolic L, Mrzljak A, Cigrovski V. Fear of hypoglycemia, a game changer during physical activity in type 1 diabetes mellitus patients. World J Diabetes 2021;12:569–577 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62. Martyn-Nemeth P, Quinn L, Penckofer S, Park C, Hofer V, Burke L. Fear of hypoglycemia: influence on glycemic variability and self-management behavior in young adults with type 1 diabetes. J Diabetes Complications 2017;31:735–741 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63. Hasan S, Shaw SM, Gelling LH, Kerr CJ, Meads CA. Exercise modes and their association with hypoglycemia episodes in adults with type 1 diabetes mellitus: a systematic review. BMJ Open Diabetes Res Care 2018;6:e000578. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64. Rempel M, Yardley JE, MacIntosh A, et al. Vigorous intervals and hypoglycemia in type 1 diabetes: a randomized cross over trial. Sci Rep 2018;8:15879. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65. Roy-Fleming A, Taleb N, Messier V, et al. Timing of insulin basal rate reduction to reduce hypoglycemia during late post-prandial exercise in adults with type 1 diabetes using insulin pump therapy: a randomized crossover trial. Diabetes Metab 2019;45:294–300 [DOI] [PubMed] [Google Scholar]
- 66. Yardley JE, Sigal RJ, Riddell MC, Perkins BA, Kenny GP. Performing resistance exercise before versus after aerobic exercise influences growth hormone secretion in type 1 diabetes. Appl Physiol Nutr Metab 2014;39:262–265 [DOI] [PubMed] [Google Scholar]
- 67. Yardley JE, Kenny GP, Perkins BA, et al. Resistance versus aerobic exercise: acute effects on glycemia in type 1 diabetes. Diabetes Care 2013;36:537–542 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68. Yardley J, Mollard R, MacIntosh A, et al. Vigorous intensity exercise for glycemic control in patients with type 1 diabetes. Can J Diabetes 2013;37:427–432 [DOI] [PubMed] [Google Scholar]
- 69. Yardley JE. Reassessing the evidence: prandial state dictates glycaemic responses to exercise in individuals with type 1 diabetes to a greater extent than intensity. Diabetologia 2022;65:1994–1999 [DOI] [PubMed] [Google Scholar]
- 70. Steineck IIK, Ranjan AG, Schmidt S, Norgaard K. Time spent in hypoglycemia is comparable when the same amount of exercise is performed 5 or 2 days weekly: a randomized crossover study in people with type 1 diabetes. BMJ Open Diabetes Res Care 2021;9:e001919. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 71. Nosek L, Roggen K, Heinemann L, et al. Insulin aspart has a shorter duration of action than human insulin over a wide dose-range. Diabetes Obes Metab 2013;15:77–83 [DOI] [PubMed] [Google Scholar]
- 72. Koivisto VA, Felig P. Effects of leg exercise on insulin absorption in diabetic patients. N Engl J Med 1978;298:79–83 [DOI] [PubMed] [Google Scholar]
- 73. Bracken RM, West DJ, Stephens JW, Kilduff LP, Luzio S, Bain SC. Impact of pre-exercise rapid-acting insulin reductions on ketogenesis following running in type 1 diabetes. Diabet Med 2011;28:218–222 [DOI] [PubMed] [Google Scholar]
- 74. West DJ, Morton RD, Bain SC, Stephens JW, Bracken RM. Blood glucose responses to reductions in pre-exercise rapid-acting insulin for 24 h after running in individuals with type 1 diabetes. J Sports Sci 2010;28:781–788 [DOI] [PubMed] [Google Scholar]
- 75. West DJ, Stephens JW, Bain SC, et al. A combined insulin reduction and carbohydrate feeding strategy 30 min before running best preserves blood glucose concentration after exercise through improved fuel oxidation in type 1 diabetes mellitus. J Sports Sci 2011;29:279–289 [DOI] [PubMed] [Google Scholar]
- 76. Riddell MC, Gallen IW, Smart CE, et al. Exercise management in type 1 diabetes: a consensus statement. Lancet Diabetes Endocrinol 2017;5:377–390 [DOI] [PubMed] [Google Scholar]
- 77. Franc S, Daoudi A, Pochat A, et al. Insulin-based strategies to prevent hypoglycaemia during and after exercise in adult patients with type 1 diabetes on pump therapy: the DIABRASPORT randomized study. Diabetes Obes Metab 2015;17:1150–1157 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 78. Scott S, Kempf P, Bally L, Stettler C. Carbohydrate intake in the context of exercise in people with type 1 diabetes. Nutrients 2019;11:3017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 79. Scott SN, Anderson L, Morton JP, Wagenmakers AJM, Riddell MC. Carbohydrate restriction in type 1 diabetes: a realistic therapy for improved glycaemic control and athletic performance? Nutrients 2019;11:1022. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80. Scott SN, Fontana FY, Cocks M, et al.; Study of Integrative Biology of Exercise in Diabetes . Post-exercise recovery for the endurance athlete with type 1 diabetes: a consensus statement. Lancet Diabetes Endocrinol 2021;9:304–317 [DOI] [PubMed] [Google Scholar]
- 81. Dubé JJ, Broskey NT, Despines AA, et al. Muscle characteristics and substrate energetics in lifelong endurance athletes. Med Sci Sports Exerc 2016;48:472–480 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 82. Davey RJ, Howe W, Paramalingam N, et al. The effect of midday moderate-intensity exercise on postexercise hypoglycemia risk in individuals with type 1 diabetes. J Clin Endocrinol Metab 2013;98:2908–2914 [DOI] [PubMed] [Google Scholar]
- 83. 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 [DOI] [PubMed] [Google Scholar]
- 84. Joy NG, Tate DB, Davis SN. Counterregulatory responses to hypoglycemia differ between glimepiride and glyburide in non diabetic individuals. Metabolism 2015;64:729–737 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 85. Cermak NM, van Loon LJ. The use of carbohydrates during exercise as an ergogenic aid. Sports Med 2013;43:1139–1155 [DOI] [PubMed] [Google Scholar]
- 86. Campbell MD, Walker M, Bracken RM, et al. Insulin therapy and dietary adjustments to normalize glycemia and prevent nocturnal hypoglycemia after evening exercise in type 1 diabetes: a randomized controlled trial. BMJ Open Diabetes Res Care 2015;3:e000085. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 87. Davis SN, Tate D, Hedrington MS. Mechanisms of hypoglycemia and exercise-associated autonomic dysfunction. Trans Am Clin Climatol Assoc 2014;125:281–291; discussion 291–292 [PMC free article] [PubMed] [Google Scholar]
- 88. Cryer PE. Hypoglycemia-associated autonomic failure in diabetes. Handb Clin Neurol 2013;117:295–307 [DOI] [PubMed] [Google Scholar]
- 89. Galassetti P, Mann S, Tate D, Neill RA, Wasserman DH, Davis SN. Effect of morning exercise on counterregulatory responses to subsequent, afternoon exercise. J Appl Physiol (1985) 2001;91:91–99 [DOI] [PubMed] [Google Scholar]
- 90. Galassetti P, Mann S, Tate D, et al. Effects of antecedent prolonged exercise on subsequent counterregulatory responses to hypoglycemia. Am J Physiol Endocrinol Metab 2001;280:E908–E917 [DOI] [PubMed] [Google Scholar]
- 91. Gomez AM, Gomez C, Aschner P, et al. Effects of performing morning versus afternoon exercise on glycemic control and hypoglycemia frequency in type 1 diabetes patients on sensor-augmented insulin pump therapy. J Diabetes Sci Technol 2015;9:619–624 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 92. Yardley JE. Fasting may alter blood glucose responses to high-intensity interval exercise in adults with type 1 diabetes: a randomized, acute crossover study. Can J Diabetes 2020;44:727–733 [DOI] [PubMed] [Google Scholar]
- 93. Turner D, Luzio S, Gray BJ, et al. Impact of single and multiple sets of resistance exercise in type 1 diabetes. Scand J Med Sci Sports 2015;25:e99–e109 [DOI] [PubMed] [Google Scholar]
- 94. Toghi-Eshghi SR, Yardley JE. Morning (fasting) vs afternoon resistance exercise in individuals with type 1 diabetes: a randomized crossover study. J Clin Endocrinol Metab 2019;104:5217–5224 [DOI] [PubMed] [Google Scholar]
- 95. Brockman NK, Sigal RJ, Kenny GP, Riddell MC, Perkins BA, Yardley JE. Afternoon aerobic and resistance exercise have limited impact on 24-h CGM outcomes in adults with type 1 diabetes: a secondary analysis. Diabetes Res Clin Pract 2021;177:108874. [DOI] [PubMed] [Google Scholar]
- 96. Devries MC, Hamadeh MJ, Phillips SM, Tarnopolsky MA. Menstrual cycle phase and sex influence muscle glycogen utilization and glucose turnover during moderate-intensity endurance exercise. Am J Physiol Regul Integr Comp Physiol 2006;291:R1120–R1128 [DOI] [PubMed] [Google Scholar]
- 97. Devries MC, Samjoo IA, Hamadeh MJ, Tarnopolsky MA. Effect of endurance exercise on hepatic lipid content, enzymes, and adiposity in men and women. Obesity (Silver Spring) 2008;16:2281–2288 [DOI] [PubMed] [Google Scholar]
- 98. Amiel SA, Maran A, Powrie JK, Umpleby AM, Macdonald IA. Gender differences in counterregulation to hypoglycaemia. Diabetologia 1993;36:460–464 [DOI] [PubMed] [Google Scholar]
- 99. Galassetti P, Neill AR, Tate D, Ertl AC, Wasserman DH, Davis SN. Sexual dimorphism in counterregulatory responses to hypoglycemia after antecedent exercise. J Clin Endocrinol Metab 2001;86:3516–3524 [DOI] [PubMed] [Google Scholar]
- 100. Galassetti P, Tate D, Neill RA, Morrey S, Wasserman DH, Davis SN. Effect of sex on counterregulatory responses to exercise after antecedent hypoglycemia in type 1 diabetes. Am J Physiol Endocrinol Metab 2004;287:E16–E24 [DOI] [PubMed] [Google Scholar]
- 101. Davis SN, Shavers C, Costa F. Gender-related differences in counterregulatory responses to antecedent hypoglycemia in normal humans. J Clin Endocrinol Metab 2000;85:2148–2157 [DOI] [PubMed] [Google Scholar]
- 102. Hedrington MS, Davis SN. Sexual dimorphism in glucose and lipid metabolism during fasting, hypoglycemia, and exercise. Front Endocrinol (Lausanne) 2015;6:61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 103. Yardley JE, Brockman NK, Bracken RM. Could age, sex and physical fitness affect blood glucose responses to exercise in type 1 diabetes? Front Endocrinol (Lausanne) 2018;9:674. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 104. Brockman NK, Sigal RJ, Kenny GP, Riddell MC, Perkins BA, Yardley JE. Sex-related differences in blood glucose responses to resistance exercise in adults with type 1 diabetes: a secondary data analysis. Can J Diabetes 2020;44:267–273.e1 [DOI] [PubMed] [Google Scholar]
- 105. Barata DS, Adan LF, Netto EM, Ramalho AC. The effect of the menstrual cycle on glucose control in women with type 1 diabetes evaluated using a continuous glucose monitoring system. Diabetes Care 2013;36:e70. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 106. Prévost MS, Rabasa-Lhoret R, Talbo MK, Yardley JE, Curry EG, Brazeau AS. Gender differences in strategies to prevent physical activity-related hypoglycemia in patients with type 1 diabetes: A BETTER Study. Diabetes Care 2022;45:e51–e53 [DOI] [PubMed] [Google Scholar]
- 107. Brockman NK, Yardley JE. Sex-related differences in fuel utilization and hormonal response to exercise: implications for individuals with type 1 diabetes. Appl Physiol Nutr Metab 2018;43:541–552 [DOI] [PubMed] [Google Scholar]
