American Medical Society for Sports Medicine Position Statement on the Care of the Athlete and Athletic Person With Diabetes

Abstract

The American Medical Society for Sports Medicine (AMSSM) developed this position statement to assist physicians and other health professionals in managing athletes and active people with diabetes. The AMSSM selected the author panel through an application process to identify members with clinical and academic expertise in the care of active patients with diabetes. This article reviews the current knowledge and gaps regarding the benefits and risks of various types of exercise and management issues for athletes and physically active people with diabetes, including nutrition and rehabilitation issues. Resistance exercises seem to be beneficial for patients with type 1 diabetes, and the new medications for patients with type 2 diabetes generally do not need adjustment with exercise. In preparing this statement, the authors conducted an evidence review and received open comment from the AMSSM Board of Directors before finalizing the recommendations.

INTRODUCTION

The American Medical Society for Sports Medicine (AMSSM) has developed this scientific statement to assist physicians and other health professionals in the management of athletes and active people with diabetes. This article reviews the current knowledge of the benefits and risks of various types of exercise and management issues for athletes and physically active people with diabetes, including nutrition and rehabilitation issues. The statement is a consensus of the authors after review of the medical literature that is supported by an editorial review by the AMSSM Board of Directors.

Athletes and active people (henceforth referred to as “athletes” in this statement) with diabetes participate in all levels of activity from youth sports to weekend warriors to professional and Olympic athletes. People with diabetes have conquered even Mount Everest.^1,2 The American Diabetes Association advocates that people with type 1 diabetes mellitus (T1DM) should be encouraged and educated by medical professionals “to allow safe participation in all forms of physical activity consistent with an individual's desires and goals.”³ The sports medicine physician should be aware that proper medical management should remove limitations to participation for most athletes with diabetes.

Physical activity provides many benefits for those athletes with diabetes. However, barriers to exercise can exist for people with diabetes, including a fear of hypoglycemia, loss of glycemic control, insufficient time, facilities or motivation, and a general scarcity of knowledge around exercise management.⁴ Diabetes does pose definite management challenges for both the athletes and for healthcare providers. Athletes with diabetes are at risk for hypoglycemia and hyperglycemia (with the potential for diabetic ketoacidosis) and chronic health issues, including microvascular and macrovascular disease. Thus, there are many questions the medical professional caring for the athlete with diabetes should ask: Does the athlete notice performance changes at different levels of blood glucose? What are the attitudes, abilities, and willingness of the athlete's teammates and coaches to assist them in diabetes management? Do athletes routinely monitor their blood glucose, or do they use general gestalt of how their body feels? How does blood glucose level vary with different life stresses, such as variation in meal times, changes in training regimens and intensity, around times of competitions, and other stressors (examinations, relationships, etc.)?⁵ This scientific statement addresses these questions and more. Our goal is to assist sports medicine physicians and other healthcare professionals in giving appropriate guidance to active individuals with any type of diabetes.

Key Points

1. The number of athletes with type 1 diabetes participating in high school and college sport is not well known but seems to be the same as the percentage of individuals with type 1 diabetes in the general population.
2. Medical evaluation is not needed before low to moderate exercise in patients with diabetes who receive regular care.
3. Resistance exercise for patients with type 1 diabetes lowers A1C levels.
4. Reduction in basal insulin is needed with vigorous exercise.
5. Newer medications for type 2 diabetes generally do not need an adjustment with exercise.
6. Every school should have an emergency action plan (EAP) for athletes with diabetes and possible hypoglycemia. A sample EAP is available in the Appendix 1, Supplemental Digital Content 1, https://links.lww.com/JSM/A254.

BENEFITS AND RISKS OF EXERCISE WITH DIABETES

Physical activity has both acute and chronic benefits and risks. Providers should be aware of these to assist athletes in being active both safely and effectively.

Benefits

Aerobic, resistance, and other types of training provide many benefits to individuals with diabetes of either type.

Aerobic training increases insulin sensitivity, mitochondrial density and oxidative enzymes, blood vessel compliance and reactivity, endothelial function, lung function, immune defenses, and cardiac output.¹⁶ Physical activity reduces cardiovascular and overall mortality risk in people with diabetes.¹⁷ Activity has also been shown to have small-to-moderate beneficial effects on lipid levels, blood pressure, and overall glycemic management.^18,19

High-intensity interval training (HIIT) promotes skeletal muscle oxidative capacity, insulin sensitivity, and glycemic control in adults with T2DM^20,21 and can be effective at minimizing the risk of a hypoglycemic episode.^22,23 Athletes with T2DM who undertake HIIT can expect benefits similar to those achieved from moderate-intensity continuous training.²⁴

Resistance training provides more benefits for improved muscular strength and functional status,^25,26 although it can also enhance body composition, bone mineral density, cardiovascular health, and insulin sensitivity.¹⁶ Any effects on long-term glycemia (as measured by glycated hemoglobin A1C) in T1DM are less specific than in adults with T2DM.^23,27 Resistance training may reduce the acute risk of exercise-related hypoglycemia in T1DM.^28,29

Flexibility and balance training (including yoga and tai chi) may enhance mobility and lower fall risk in older adults with diabetes as well in those with peripheral neuropathy.^30,31 In most instances, flexibility and balance training have a lesser impact on glycemic management.^32,33

Risks

Being physically active does carry some risks. The biggest concern for anyone using insulin (or insulin secretagogues) is the potential for exercise-related hypoglycemia.³⁴ Although most hypoglycemic events occur during, immediately after, or 6 to 15 hours after exercise,³⁵ the risk can extend out to 48 hours.³⁶ Appropriate regimen changes can and should be made to minimize this risk.^37–40

Exercise-induced hyperglycemia can also occur, more commonly in those with T1DM than T2DM.⁴¹ Overconsumption of carbohydrates before or during exercise, relative insulin deficiency, and intense exercise may lead to hyperglycemia during exercise,^37,42–45 especially if starting blood glucose levels are elevated. Individuals with T1DM who have hyperglycemia (≥250 mg/dL) and elevated ketones (≥1.5 mmol/L) should test for blood or urine ketones and postpone exercise until ketones are lower or absent, glucose is less than 180 mg/dL, and euhydration is present.³

Another concern is that skin perfusion and sweating may be impaired in adults with T1DM.^46,47 There is an increased risk of heat-related illness during exercise in patients with T2DM, who are older, have poorer blood glucose management, or have neuropathy.⁴⁸ Chronic hyperglycemia also increases the risk for dehydration, and some blood pressure medications may negatively impact hydration status and electrolyte balance.¹⁵ Older adults with diabetes or any athlete with diabetes and any of the following: autonomic neuropathy, cardiovascular complications, or pulmonary disease should avoid exercising outdoors on days with excessive heat or humid days. Also, various complications associated with long-term diabetes can result in physical limitations and disability that may be worsened by physical activity unless appropriate precautions are taken.^3,49,50

PRE-EXERCISE SCREENING

The rationale for pre-exercise screening in patients with diabetes has historically been based on reducing the risks of an acute cardiac event, hypoglycemia, or hyperglycemia.^3,51 Recent literature has shown, however, that the risk of these events is low and that the benefits of exercise outweigh the risks for most individuals with diabetes. Screening of individuals without symptoms of cardiovascular disease (CVD) undergoing low-to-moderate intensity exercise has not been shown to reduce the risk of cardiac events.^3,52,53

There are some variations in the guidelines for screening. The American Diabetic Association guidelines state that pre-exercise medical clearance is not necessary for asymptomatic individuals who are receiving diabetes care consistent with the current guidelines who wish to begin a low or moderate-intensity physical activity that does not exceed the demands of brisk walking or everyday living.³ The American College of Sports Medicine guidelines state that physically inactive individuals with known metabolic disorders or those with signs or symptoms suggestive of cardiovascular, renal, or metabolic diseases should seek medical clearance before starting any exercise program, regardless of the intensity.⁵¹ When screening is performed, evaluation often includes electrocardiogram, echocardiogram, and exercise stress testing at the discretion of the clinician. Although the risk stratification in this group of individuals is more complex, per current clinical guidelines, the workup should be the same as in any individual with symptoms of CVD.^51,54

Indications for Pre-exercise Screening

1. Patients with symptoms of CVD, regardless of exercise-intensity level.
2. Individuals attempting to begin a vigorous exercise program.³
3. Individuals who are increasing from a relatively sedentary level of activity to a more vigorous level of exercise.

RECOMMENDED TYPES OF EXERCISE TRAINING

Although aerobic, resistance, and HIIT exercise all have roles in diabetes management, the optimal amounts or types of exercise have not been fully elucidated.^55–57 Individuals can benefit from doing aerobics or HIIT training, as well as combined aerobic and strength conditioning.⁵⁸ Resistance exercise may be especially beneficial for lowering glycemia in adults with newly diagnosed diabetes and those with higher baseline A1C values.⁵⁹

Exercise Recommendations by Type

Aerobic exercise is defined as repeated, continuous movement of large muscle groups that depend primarily on the aerobic energy system. Examples include cycling, rowing, running or jogging, swimming, and walking. Resistance exercise can be defined by purposeful movements against an external load to improve muscular strength and muscular endurance. Such exercises generally target the phosphagenic and anaerobic metabolic pathways and can be performed using body mass as resistance, resistance bands, free weights, or weight-training machines. High-intensity interval training is an exercise strategy that alternates brief periods of high-intensity work with recovery periods of low or no intensity work. High-intensity interval training puts a greater emphasis on the use of the phosphagenic metabolic energy pathways. Some examples of HIIT exercise include sprint interval training (30 seconds of maximal sprint with 30 seconds of rest) and circuit training (a series of exercises performed in rotation with minimal rest, often using different pieces of apparatus).

Recommended Activities for Adults with Diabetes

Consistent with recommendations for the general population, the current guidelines for people with diabetes call for a weekly minimum of 150 minutes of accumulated aerobic, moderate-intensity physical activity (or 75 minutes of vigorous-intensity training) and 2 to 3 days of resistance training. For children and young adults with diabetes, 60 minutes of physical activity is recommended per day,³ three the same as for nondiabetic youth.

Vigorous exercise lasting 75 minutes weekly may substitute for the minimum 150 minutes given that 1 minute of vigorous activity is considered equivalent to 2 minutes of moderate activity.^3,60 Exercise should ideally be performed a minimum of 10 minutes per activity. Training programs should be individualized based on an athlete's overall goals, such as improvements in blood glucose levels, fitness, strength, or body composition.

IMPACT OF EXERCISE ON BLOOD GLUCOSE

The limiting step in blood glucose metabolism is glucose transport into cells, which is primarily mediated by the insulin-sensitive GLUT4 glucose transporter.⁶¹ There are 2 pathways to increase glucose uptake by skeletal muscles. The first pathway is stimulated by insulin, and muscle contractions stimulate the second pathway during exercise.⁶² Skeletal muscle is the primary tissue responsible for insulin-stimulated glucose disposal of serum glucose and the major site of peripheral insulin resistance. Impaired glucose transport (ie, insulin resistance in muscle) may lead to T2DM. Because exercise stimulates insulin-independent mechanisms to increase glucose uptake into skeletal muscle, physical activity is especially important for anyone with peripheral insulin resistance.

Studies have shown that obese patients and those with T2DM usually have appropriate muscle GLUT4 protein levels that allow for an expected increase in peripheral glucose utilization through insulin-independent mechanisms during exercise.^63,64 Exercise participation can have both an acute and a chronic impact on blood glucose management. The effect can also vary with the type of training undertaken.

Acute Glycemic Responses to Exercise

Aerobic Exercise

A meta-analysis examining the acute effect of physical activity on glycemic control in a group with T1DM showed that continuous, moderate-intensity aerobic exercise was associated with a significant and rapid reduction in glucose levels during exercise, followed by a slight rise after exercise cessation.⁶⁵ In athletes with T1DM, hypoglycemia usually occurs within 45 minutes of starting aerobic exercise unless regimen adjustments are made to prevent it. The exact glycemic response to aerobic activity may vary by session based on several factors, including the amount of circulating insulin, starting blood glucose level, recent food intake and its composition, time of day (especially prebreakfast vs later in the day), previous hypoglycemia or activity, and exercise duration and intensity.^3,4 Frequent fingerstick or continuous glucose monitoring is recommended to assist athletes in establishing their usual glycemic responses and maintaining euglycemia with appropriate regimen changes (insulin reduction and carbohydrate ingestion).

Resistance Exercise and High-Intensity Intervals

Resistance exercise is short duration, high intensity, and predominantly anaerobic that generally does not cause acute hypoglycemia. Resistance exercise can, however, cause hyperglycemia because of catecholamine release leading to rapid mobilization of liver and muscle glycogen. Hyperglycemia from such training may also be related to the release of growth hormone that attenuates glucose uptake by cells. This short-term hyperglycemia generally does not result in significant hypoglycemia after exercise, but clinicians should continue to monitor athletes for individual responses to exercise. Relevant to those with either T1DM or T2DM, resistance exercise increases insulin signaling and increases glucose and glycogen uptake during and after exercise.⁶⁶ Like a bout of resistance exercise, HIIT exercise may also result in hyperglycemia acutely and less hypoglycemia after exercising due to slower glycogen breakdown.^23,67 For both activities, athletes with diabetes should be prepared for the possibility of delayed-onset hypoglycemia, which may occur many hours after an intense training session.

Strategies for the Team Physician

In general, prolonged aerobic exercises that deplete glycogen stores will cause hypoglycemia. Increasing carbohydrate intake before and during prolonged exercise while decreasing insulin levels can mitigate the hypoglycemic response. Also, for those with T1DM, leveraging resistance exercise, short sprints, or more vigorous HIIT before more extended aerobic exercises can attenuate the hypoglycemic response.^4,20,29

Finally, the clinician must be aware of the potential hyperglycemic response of both more laborious resistance exercise and HIIT when advising athletes on how to optimize the management of glycemia. Despite these generalities, individual responses vary, and the clinician must be prepared for hypoglycemia after any exercise, mainly when undertaken by athletes using insulin.

In individuals with T1DM, strategies to reduce the risk of hypoglycemia with activity include consuming extra carbohydrates or other macronutrients⁶⁸ and altering insulin dosage.^69,70 Appropriate counseling by a healthcare provider with knowledge of insulin dosing regimens and adjustments reduces the risk of hypoglycemia. In addition, resistance training before aerobic exercise has been shown to reduce hypoglycemia during the latter activity.²⁹ Finally, time-of-day adjustments are essential to consider when dosing insulin because exercise performed later in the day can be associated with an increased risk of overnight hypoglycemia.³⁸

High-Altitude Effects

People with diabetes can take part in activities at high altitude and even extreme altitude.^2,71 However, blood glucose regulation is affected by altitude exposure in people with and without diabetes,⁷² likely because of changes in levels of counterregulatory hormones. The combination of high-altitude–induced anorexia and increased energy expenditure at altitude may develop abnormal glycemia levels in a person with diabetes unless careful adjustments in medication are performed.^71,73 Because of this and because acute mountain sickness may mimic the signs of hypoglycemia,¹ it is important to frequently monitor blood glucose levels and be aware that glucose monitors and continuous glucose monitoring (CGM) may not work as well at altitude or in severe cold.^1,73 Planning and preparation are the key to exercise at high altitudes.

Long-Term Glycemic Effects of Exercise

Aerobic Training

Two meta-analyses about adults with T1DM have shown decreases in A1C with regular aerobic training, and the more significant effects occur in those starting exercise who have less effective management (A1C > 8%).^23,74,75 Many studies have shown that aerobic exercise improves glycemic control in those with T2DM. A meta-analysis that included 848 patients who participated in structured aerobic exercise showed a decrease in absolute A1C reduction of 0.73%. Those who performed structured exercise for more than 150 minutes per week showed the most significant reduction.⁷⁶ In a second meta-analysis, of 1372 T2DM participants, 737 who performed aerobic exercise training also experienced a decrease in A1C; the longer the length of weeks of the program, the greater the benefit. Improvements were also seen in V̇o₂max and were more significant for those who exercised at a vigorous intensity.⁷⁷ Better glycemic management is not the only improvement; however, aerobic exercise training also decreases visceral fat in patients with T2DM who are overweight or obese⁷⁸ and improves their quality of life.⁷⁹ In addition to benefits to glycemia, cardiorespiratory fitness and lipid profiles improve potentially leading to a reduction in morbidity and mortality related to CVD, especially in adults with T1DM.⁸⁰

Resistance Training

The main effects of resistance exercise training involve increases in lean muscle mass and strength, leading to enhanced glucose uptake and restoration of glycogen stores, enhanced athletic performance, heightened insulin sensitivity, and improved A1C after 6 months.⁵⁶ Other known effects include an increase in mitochondrial oxidation capacity⁸¹ and reduction of inflammation.⁸² In addition, such training has been shown to increase bone density, reduce body fat, and increase resting metabolic rate,^3,83 all of which are beneficial for overall body composition and general health and fitness.

Combined Aerobic and Resistance Training

A Cochrane review demonstrated that exercise (moderate-intensity aerobic and resistance training) decreased A1C by 0.6% (95% CI, −0.9 to −0.3; P < 0.05),⁸⁴ consistent with a 30% improvement toward a target value of 7% A1C for a person starting with a 9% A1C. Studies have investigated the benefits of combining aerobic and resistance training. Participants who did combined training compared with just aerobic exercise had more significant improvement in A1C (mean difference = −0.17%; 95% CI, −0.31 to −0.03; P = 0.02; 9 trials, 493 participants) and improved A1C, fasting glucose, and triglyceride levels compared with just resistance training.⁵⁸ Combined training programs also show a superior benefit in decreasing visceral adiposity (effect size −0.21; 95% CI, −0.037 to −0.05; P = 0.01).⁷⁸ When examining self-directed exercise programs (as opposed to supervised ones), combined training also leads to a more significant reduction in A1C than aerobic exercise alone.⁸⁵

For the best long-term glycemic management and cardiorespiratory fitness gains, a combination of the 3 different exercise types (aerobic, resistance, and HIIT) seems to show more significant benefits than any single type of exercise. A meta-analysis that included 323 patients with T1DM who did aerobic, resistance, and HIIT training showed that their A1C decreased more than controls.⁸⁶ Subgroup analysis showed a more significant decrease in those participants with a baseline A1C >8.5%.⁸⁷

High-Intensity Interval Training

Various types of HIIT rapidly increase mitochondrial oxidation, lower insulin resistance, and improve glycemic management more than continuous aerobic training.²⁰ Circuit training, HIIT, and other forms of functional fitness training often incorporate resistance exercises. These programs are challenging to study because of the multidomain aspects. However, literature shows the potential of HIIT in both types of diabetes,^23,75 Higher-intensity exercise is generally more effective in improving metabolism, physical characteristics, and physical fitness,⁸⁵ as well as chronic blood glucose levels. A meta-analysis of 8 studies with 235 participants showed a weighted mean difference in A1C of −0.22% (-0.38 to −0.06) or −2.4 mmol/mol (−4.2 to −0.7, P = 0.007) with higher-intensity training compared with lower-intensity training.⁸⁸ High-intensity interval training induces cardiometabolic adaptations similar to those of aerobic training in prediabetes and T2DM and provides more significant benefits to functional capacity in those with T2DM.⁸⁹

Yoga

Yoga practices may promote significant improvements in several indices of importance in T2DM, including overall glycemia, lipid levels, body composition, and diabetes medication use.³² Compared with controls, yoga participants were successful in improving their A1C by −0.36, (95% CI, 0.16-0.56) in one meta-analysis⁹⁰ and A1C standardized mean difference = −0.64 (95% CI, −0.97 to −0.30) in another⁹¹; the latter article did note that there was a high risk of reporting bias in the studies that met their inclusion criteria. Among leisure recreational activities, yoga was found to produce the best reduction in A1C in adults with T2DM,⁹² but further quality research is needed.⁹³

IMPACT OF LIFESTYLE MANAGEMENT ON TYPE 2 DIABETES

Although healthcare providers do not consider T1DM to be preventable, T2DM may be preventable in high-risk individuals (those with prediabetes) with improvements in physical activity levels and dietary quality. Lifestyle management can improve insulin sensitivity in anyone with diabetes of either type. However, lifestyle changes are most frequently used for adults with T2DM to manage blood glucose and to assist with weight loss or maintenance. In adults at high risk for T2DM, structured lifestyle interventions including at least 150 minutes of weekly physical activity and dietary restriction to achieve a loss of 5% to 7% have demonstrated reductions of 40% to 70% in the risk of progressing to diabetes.⁹⁴ A recent systematic review and a meta-analysis found that diet and physical activity lifestyle programs reduced T2DM incidence, body mass, and fasting blood glucose in at-risk individuals and improved other cardiometabolic risk factors.^95,96 Greater adherence to lifestyle improvements generally results in more substantial weight loss.⁹⁷ Furthermore, intensive lifestyle management can benefit the health of adults who already have T2DM, including sustained weight loss, increased physical fitness, improved glycemic control, and reduced blood pressure and lipids with fewer medications, along with a reduced incidence of sleep apnea, kidney and eye disease, depression, and knee pain.^98,99

NUTRITIONAL PRACTICES AND PERFORMANCE

Coordination of care among athletic trainers, physicians, nutritionists, and athletes with diabetes becomes imperative because most competitive athletes learn to manage their diabetes during training and competition by trial and error and by sharing personal experiences with other athletes.¹⁰⁰ Providers should be familiar with the different motivations for athletes to participate in athletics, thus have a better understanding of their goals, especially those with diabetes. These individual goals may be more important than blood glucose management; however, they also can be in direct conflict with the physician's goals of preventing short-term and long-term complications of diabetes.⁵ Certain dietary practices, such as restricting carbohydrates or foods with a low GI, may have an impact on blood glucose management and performance.

Glycemic Index and Diabetes

The type of food eaten affects blood glucose levels; however, there is no universal approach to the optimal diabetic diet, and the usefulness of the low–glycemic index (GI) diet is controversial.^101,102 Glycemic index describes the blood glucose response after consumption of a carbohydrate-containing food relative to a reference food. There are many charts and guidelines for GI, but an example is that white potatoes have a higher GI than black beans.^101,103 Low GI use by athletes with diabetes is intended to prevent spikes in postprandial glucose.¹⁰⁴ There are many variables involved in response to the effects of food intake on blood glucose beyond the GI.¹⁰⁵ Although as a positive, one meta-analysis found that implementing a low-GI diet lowered A1C values by 0.43% when compared with a high-GI diet.¹⁰⁶ Caring for athletes with diabetes, one should be aware of the potential benefits of low-GI foods in the treatment of diabetes.¹⁰⁷

Ketogenic Diets and Training

Because of the very low-carbohydrate nature of ketogenic diets (KDs), they deserve special mention here. Fasting and very low-carbohydrate diets lead to what is known as “physiological ketosis,” a state in which ketone body levels can rise to 7 to 8 mmol/L without any change in blood pH. A KD contrasts with diabetic ketoacidosis when ketones can exceed 20 mmol/L and lower arterial pH. Through gluconeogenesis, blood glucose levels decrease but remain at a physiological level while on a ketogenic diet.¹⁰⁸ A KD seems to enhance fat metabolism and oxidation,¹⁰⁹ with at least maintenance of athletic performance in highly aerobic athletes (such as ultraendurance ones) after full adaptation.¹¹⁰

Sustained nutritional ketosis for the management of insulin resistance and T2DM is being examined, and initial results demonstrate significant weight loss and a lesser requirement for diabetes medications to manage blood glucose.¹¹¹ Studies suggest that some athletes with T1DM are intentionally not achieving adequate blood glucose levels before their competitive event¹¹² and have enhanced lipid utilization that potentially prevents exercise-induced hypoglycemia.¹¹³

Weight Loss and Diabetes Management in the Athlete

Calorie restriction and increased physical activity can lead to significant weight loss and A1C reduction in those with T2DM.¹¹⁴ Meta-analyses of studies estimate that for each kilogram of mean weight loss, there is a mean A1C reduction of 0.1 percentage points.¹¹⁵ Weight reduction resulting from interventions other than lifestyle management can also be useful in the management of T2DM. Two meta-analyses of studies looking at bariatric surgery and weight loss for people with T2DM show that bariatric surgery leads to more significant body mass loss and higher remission rates of T2DM.^116,117 These studies show promise for people that fail to achieve weight loss maintenance (WLM) with diet and exercise or diet alone. The studies further showed a reduction of A1C by a mean difference of between −1.1¹¹⁶ to −1.3.¹¹⁷ These meta-analyses show that bariatric surgery for T2DM can be a successful method of weight reduction and remission of T2DM. Weight loss maintenance after bariatric surgery can be difficult, and exercise is a critical factor for long-term WLM and lasting remission of T2DM after bariatric surgery.¹¹⁸ There are no known restrictions to exercise once the postsurgery healing has occurred. After bariatric surgery, exercise seems to be associated with a more significant weight loss of more than 4% of BMI (95% CI, 0.26-8.11), although a causal relationship cannot be excluded because findings are from observational data.¹¹⁹ However, exercise is likely to be an effective strategy for WLM for those individuals who can implement and maintain a regular regimen, further work is needed to determine modes and duration of exercise for successful WLM.¹²⁰

Unsafe Weight Loss Practices

The athletic trainer and physician should be aware of athletes practicing unsafe dietary habits and patterns, manipulating medications, using nutritional supplements with no known beneficial (or even detrimental) effects, and be able to recognize potential nutritional problems in the athlete. In sports with weight categories (eg, weightlifting and combative sports such as wrestling and boxing), a common practice is the omission of insulin.¹²¹ By withholding insulin, athletes can lose weight before their weigh-ins due to diuresis but doing so may lead to hyperglycemia and risk of diabetic ketoacidosis.¹²² Athletes may attempt other rapid weight loss approaches to “make weight” and compensate by consuming excessive calories, thereby causing large fluctuations in serum glucose.

BLOOD GLUCOSE TARGETS FOR ATHLETIC PARTICIPATION

Blood glucose levels need to be monitored closely during physical activity, especially in athletes with T1DM. Even when blood glucose levels are acceptable before competition, psychological stress can lead to increases in blood glucose from elevated counterregulatory hormones causing increased hepatic glucose production and decreased peripheral glucose uptake. The increase in counterregulatory hormones results in the athlete being susceptible to hyperglycemia during competition. For athletes participating in team sports that necessitate breaks in play (eg, baseball, basketball, and hockey), the periods of physical inactivity coupled with elevations in stress hormones may cause unusually large increases in glucose concentration.¹²³

Also, training or competing in warm and humid environments can elevate glucose levels because of increases in circulating catecholamines, glucagon, cortisol, and growth hormone.¹²⁴ The combination of psychological stress and warm, humid environments sets the stage for hyperglycemia, dehydration, and potential heat illness. Frequent glucose monitoring, coupled with small boluses of rapid-acting insulin, may be required to recover from these fluctuations and to prevent complications.

The athlete, athletic trainer, and team physician should have an agreed upon predetermined blood glucose level that dictates when the athlete can and cannot participate.⁵ Athletes should be educated and questioned about the frequency of their blood glucose monitoring. It is recommended that blood should be sampled 2 to 3 times at 30 minutes intervals before exercise to ascertain any directional trends. An athlete can start exercise if blood glucose is higher than 90 mg/dL; a pre-exercise blood glucose level between 100 and 250 mg/dL is generally a safe range.¹²⁵Table 1 shows recommended guidelines. Above 250 mg/dL, there is significant osmotic diuresis present and a higher risk for dehydration and development of blood ketones.

TABLE 1. - General Guidelines for Pre-exercise Glucose and Activity Level⁴

The carbohydrate intakes showed here aim to stabilize glycemia at the start of exercise. Blood glucose at the start of exercise must also be viewed within a wider context. Factors to consider include directional trends in glucose and insulin concentrations, patient safety, and individual patient preferences based on experience. Carbohydrate intake will need to be higher if circulating insulin concentrations are high at the onset of exercise

Starting glycemia below target (<5 mmol/L; <90 mg/dL)

Ingest 10-20 g of glucose before starting exercise

Delay exercise until blood glucose is more than 5 mmol/L (>90 mg/dL) and monitor closely for hypoglycemia

Starting glycemia near target (5-6.9 mmol/L; 90-124 mg/dL)

Ingest 10 g of glucose before starting aerobic exercise

Anaerobic exercise and high-intensity interval training sessions can be started

Starting glycemia at target levels (7-10 mmol/L; 126-180 mg/dL)

Aerobic exercise can be started

Anaerobic exercise and high-intensity interval training sessions can be started, but glucose concentrations could rise

Starting glycemia slightly above target (10.1-15.0 mmol/L; 182-270 mg/dL)

Aerobic exercise can be started

Anaerobic exercise can be started, but glucose concentrations could rise

Starting glycemia above target (>15 mmol/L; >270 mg/dL)

If the hyperglycemia is unexplained (not associated with a recent meal), check blood ketones. If blood ketones are modestly elevated (up to 1.4 mmol/L), exercise should be restricted to a light intensity for only a brief duration (<30 min) and a small corrective insulin dose might be needed before starting exercise. If blood ketones are elevated (≥1.5 mmol/L), exercise is contraindicated and glucose management should be initiated rapidly as per the advice of the healthcare professional team

Mild-to-moderate aerobic exercise can be started if blood ketones are low (<0.6 mmol/L) or the urine ketone dipstick is less than 2+ (or <4.0 mmol/L). Blood glucose concentrations should be monitored during exercise to help detect whether glucose concentrations increase further. Intense exercise should be initiated only with caution because it could promote further hyperglycemia

https://www.thelancet.com/journals/landia/article/PIIS2213-8587(17)30014-1/abstract.

During exercise, blood glucose levels should ideally be checked every 30 minutes. For every 30 minutes of exercise, 15 to 30 g of carbohydrate may be needed (depending on circulating insulin levels and type of physical activity). Adequate fluid replacement needs to be maintained. Exercise sessions lasting more than 35 to 45 minutes begin to deplete glucose stores in the muscles and liver, which need to be replenished. Replenishing the glucose stores can be achieved with 40 to 80 g of carbohydrate intake after exercise cessation, depending on the duration and intensity of the activity and level of depletion. After the event, glucose monitoring should occur every 2 hours and up to 4 hours to assess for delayed hypoglycemia.¹²⁶

DIABETES MEDICATIONS AND EXERCISE

People with diabetes often rely on the use of medications for the management of blood glucose and any other medical conditions. Those with T1DM primarily use intensive insulin therapy, whereas those with T2DM may use a lifestyle modification program, oral medication, noninsulin injectable, or insulin therapy.

Hypoglycemia remains a primary concern for all insulin users, and fear of hypoglycemia continues to be the number one barrier to exercise in those with T1DM.¹²⁷ Indeed, exercise-induced hypoglycemia is common in people with T1DM and, to a lesser extent, in those with T2DM who use insulin or secretagogues (sulfonylureas and meglitinides).¹²⁸ It is important to avoid hypoglycemia because of the increased risk for further hypoglycemic episodes during the next 48 hours.³⁹

The appropriate changes to medications to reduce the risk of hypoglycemia during exercise must be individualized and based on the experience of both the patient and the healthcare provider with exercise. Recommendations for normalizing glycemic control during and after exercise consist of adjustments to the bolus insulin therapy based on food composition only produce short-term results. By reducing a basal insulin dose in combination with prandial bolus insulin and eating low-GI carbohydrates, exercise-induced hypoglycemia can potentially be avoided for 24 hours after evening exercise without hyperglycemia.³⁷

Manipulating the athlete's insulin regimen and carbohydrate intake should be undertaken to prevent exercise-related hypoglycemia. No dose adjustments are necessary for users of metformin, thiazolidinediones, or dipeptidyl peptidase 4 inhibitors.³ However, when these medications are used in conjunction with insulin or oral insulin secretagogues (such as sulfonylureas and meglitinides) and a new activity is initiated, the dose of insulin and secretagogues may need to be lowered to reduce the risk of hypoglycemia¹²⁹ (Table 2). Glucagon-like peptide 1 (GLP-1) agonists are noninsulin injectable medications that work through multiple mechanisms, including a slowing of gut transit that may result in multiple gastrointestinal complaints that could potentially delay absorption. There are no recommended dose adjustments for GLP-1 agonists for exercise, but concomitant use of insulin or sulfonylureas may necessitate a lowering of these medications to prevent hypoglycemia, particularly as an athlete is initiating a new activity or level of exercise.¹³⁰

TABLE 2. - Diabetes Medications, Exercise Considerations, and Dose Adjustments

Type/Class of Medication	Exercise Considerations	Safety/Dose Adjustments
Diabetes
Insulin	Deficiency: hyperglycemia, ketoacidosis Excess: hypoglycemia during and after exercise	Increase insulin dose pre-exercise and post-exercise for deficiency Decrease prandial and/or basal doses for excess insulin
Insulin secretagogues	Exercise-induced hypoglycemia	If exercise-induced hypoglycemia has occurred, decrease dose on exercise days to reduce hypoglycemia risk
Metformin	None	Generally safe; no dose adjustment for exercise
Thiazolidinediones	Fluid retention	Generally safe; no dose adjustment for exercise
Dipeptidyl peptidase 4 inhibitors	Slight risk of congestive heart failure with saxagliptin and alogliptin	Generally safe; no dose adjustment for exercise
Glucagon-like peptide 1 receptor agonists	May increase risk of hypoglycemia when used with insulin or sulfonylureas but not when used alone	Generally safe; no dose adjustment for exercise but may need to lower insulin or sulfonylurea dose
Sodium–glucose cotransporter 2 inhibitors	May increase risk of hypoglycemia when used with insulin or sulfonylureas but not when used alone	Generally safe; no dose adjustment for exercise

From the ADA position statement.³

Sodium–glucose cotransporter 2 (SGLT2) inhibitors, the newest class of therapeutics, promote glucosuria and have a modest diuretic effect. Dehydration is a potential concern with the introduction of new physical activities, but no dose adjustments are recommended before initiating an exercise routine.¹³¹ It may be prudent to ensure normal fluid balance before initiating exercise. Their use is associated with an increased risk of ketoacidosis and bone fractures,¹³¹ especially when taken by adults with T1DM (a practice that is becoming more frequent). Sodium–glucose cotransporter 2 inhibitors alone do not increase the risk for hypoglycemia but may when used in conjunction with insulin or sulfonylureas.

USE OF NEWER TECHNOLOGIES

Insulin Pumps

Multiple daily injections (MDIs) and insulin pump therapy are both methods to deliver intensive insulin therapy. Multiple daily injection uses a long-acting basal insulin and rapid-acting insulin with meals. Pump therapy delivers rapid-acting insulin to provide both basal and bolus insulin. Athletes in consultation with their healthcare provider can work together in making the decision regarding MDI versus pump therapy.¹³² Many athletes with T1DM do not make the proper adjustments to their insulin doses around exercise,¹³³ and a careful and thorough discussion with the athlete about dosing insulin is needed.

Some advantages of insulin pumps include: (1) the use of a single rapid-acting insulin to achieve a more physiologic insulin profile; (2) ability to alter the basal rate before, during, or after exercise; (3) options to suspend or disconnect; and (4) availability of “smart pumps” that use internal calculators and settings to determine the estimated amount of insulin in circulation and suggest appropriate dosing.¹³⁴

Few people (about 4%) discontinue using the pump and return to MDIs, with 70% of those quitting citing difficulties in doing sports.¹³⁵ With the most novel of insulin pumps, the threshold suspend of insulin delivery may offer additional protection against exercise-induced hypoglycemia,⁷⁰ and the hybrid closed-loop system allows CGM data to drive the basal insulin infusion rate while the pump is in auto mode. In this system, a temporary higher blood glucose target offers some protection from hypoglycemia risk. The greater flexibility in adjusting basal insulin levels within 1 to 2 hours may limit postexercise hypoglycemia. It is a recommended disconnection of the insulin pump during contact or collision sports, as well as some other sports (eg, diving).¹²³ Damage in contact sports is one of the disadvantages of an insulin pump therapy as well as risk of hyperglycemia or ketosis with malfunction or inadvertent disconnection, infusion set adhesive problems, irritation at the infusion site, and potential for extreme ambient temperatures (<36°F and >86°F) to interfere with insulin action.¹³⁶

For those on MDIs, limited data and clinical experience suggest that reductions in long-acting insulin may reduce the risk of hypoglycemia during and after activity but with the potential for hyperglycemia during other points of the day.¹³⁴ The advantages of MDI include the absence of a connection to a device and a lower cost. Peoples on pump therapy do better with postexercise glucose management than MDI treatment.¹³⁷

Continuous Glucose Monitoring

Continuous glucose monitoring devices provide valuable information on glucose concentrations, rates of change, and patterns of change, which athletes can use to prevent hypoglycemia during exercise.¹³⁸ Although existing sensors are reasonably accurate for exercise, the lag time in glucose equilibrium with the interstitial space and a rapid turnover of glucose during exercise may affect that accuracy, overestimating blood glucose levels when they are dropping and underestimating them when they are rising.^3,139 The Clarke Error Grid Analysis is a method to compare glucose levels between a device and a gold standard. Zone A is clinically the same values; zone B device is clinically different from the gold standard but safe, with zone C, D, and E being clinically relevant differences. In multiple studies, the CGM is 99% to 100% in zones A and B during high-intensity exercise or continuous aerobic exercise, with zone A accounting for 75% to 80% of these measurements.^140,141,142 Despite these limitations, CGM use may decrease the fear of hypoglycemia in insulin users by providing trend analysis,¹⁴² and it is conceivable that this benefit would apply to noninsulin users with T2DM as well. Continued improvements to existing technologies, plus the introduction of new technologies, will be aided by better algorithms to optimize blood glucose and performance during and following exercise, enhanced closed-loop systems that use additional inputs, and machine learning, which allow the device to meet the needs of the athletic person with diabetes.¹³⁸

REHABILITATION CONSIDERATIONS

In addition to the common sports injuries of ligament tears and stress fractures that occur to all athletes, other conditions associated with diabetes that occur at higher rates include tendinopathy,¹⁴³ adhesive capsulitis of the shoulder, and articular cartilage disease.¹⁴⁴ Diabetes can have a significant impact on the function of tendons due to the accumulation of advanced glycation end-products during hyperglycemia that impact load-bearing collagen. Besides, tendon vascularity and reduced healing may be due to diabetes-induced changes in the peripheral vascular system and impaired synthesis of collagen and glycosaminoglycan.¹⁴⁵ The presence of certain complications, such as nerve damage in the extremities, may also impact healing and rehabilitation of injuries.

Diabetic Peripheral Neuropathy

Diabetes potentially leads to health complications as the duration of the disease progresses, and diabetic peripheral neuropathy (DPN) is one of the most common complications. Diabetic peripheral neuropathy occurs in more than 50% of individuals with diabetes and is a significant risk factor for pathologic consequences such as ulceration, reduced physical mobility, infection, and even amputations. In previous recommendations, walking and running in people with DPN was contraindicated. Fortunately, a growing body of evidence suggests that physical activity and exercise may improve DPN (and diabetic foot) outcomes.¹⁴⁶ Rehabilitation therapy that includes a large portion of balance training can help with neuro-retraining.^146,147 In patients with DPN, diminished peripheral blood flow and decreased local angiogenesis result from abnormalities in the production of collagen, inflammatory mediators, angiogenic and growth factors, and also contribute to lack of healing in damaged tissue.¹⁴⁸ Longer time to respond to usual rehabilitation techniques, including working on balance and proprioception training, is necessary.^145,148

Postinjury Rehabilitation Considerations

The approach to the postmusculoskeletal injury rehabilitation of the athlete with diabetes should be slightly different than athletes without diabetes. To effectively treat the athlete with diabetes, it is essential first to understand the physiological response after trauma. After the initial injury, stress hormones in the body will increase, leading to a hyperglycemic response and the need for more optimal blood glucose levels to promote healing.¹⁴⁴

Diabetes is associated with increased rates of complications from sports medicine operative procedures, such as infection, delayed healing, and failure of the procedure.¹⁴⁴ Postoperative anterior cruciate ligament reconstruction has higher rates of infections as other procedures and, worse, short but equal long-term outcomes.¹⁴⁹ The athlete and clinician need to take special consideration to ensure the best environment to regain full function and ability after injury.

Hypoglycemia and hyperglycemia can lead to problems with proprioception, spatial awareness, coordination, strength/muscle gains, wound and tissue healing rates, and a higher instance of DPN, and symptoms, such as blurry vision, fatigue, headache, shaking, dizziness, and trouble concentrating. These symptoms could impair their ability to perform rehabilitation exercises effectively, decrease their attention to form, and possibly create more harm due to balance and dizziness complications. Therefore, monitoring glucose levels during rehabilitation therapy is recommended.¹⁵⁰

The use of rehabilitation modalities may have different effects on athletes. Massage therapy and thermal modalities could contribute to increased or decreased absorption rates based on insulin administration and timing. There is insufficient research on ultrasound and electric stimulation modalities to determine the effects, but their thermodynamic and stimulating properties may affect the absorption rate of insulin, if performed near the injection site. The clinician needs to be aware and prepared to address these issues and concerns to provide the athlete with diabetes the best environment to recover from injury.

SPECIAL POPULATIONS

Master Athletes

“Master athletes” is a class of athletics often found in track and field, road running, cross country running, and swimming. These events feature athletic competitions in 5-year age groups beginning at age 35 years. As athletes age, medical comorbidities such as diabetes are more commonly present than in younger athletes but often less common than in sedentary peers.^151,152 One study showed that master athletes with an average age of 60 years had similar blood glucose and insulin levels as athletes in their mid-20s. Age-related decline in mitochondrial oxidative capacity was absent in endurance-trained individuals.^153,154 In addition, endurance-trained master athletes had higher insulin sensitivity than age-matched peers.¹⁵⁵

Parisi and Baggish recommend for master athletes with T2DM maximal-effort limited exercise testing as well as for patients with T2DM and other CV risk factors who wish to or who counseled by their healthcare provider to engage in moderate-to-vigorous intensity exercise. Other studies only recommend this level of pre-exercise testing if patients are previously sedentary or want to move from moderate-to-vigorous exercise.^3,156 For master athletes, the recommendations are for closer monitoring of blood glucose during and after physical activity.¹⁵⁷ Wearing a medical alert identification is also recommended to assist with care if an emergency occurs. Nutritional needs change during aging, and older athletes have a lower lean body mass, which on average requires a lower amount of energy intake than in younger athletes.¹⁵⁷

National Collegiate Athletic Association Student Athletes

The AMSSM endorsed the National Collegiate Athletic Association Sports Science Institute's INTERASSOCIATION RECOMMENDATIONS: PREVENTING CATASTROPHIC INJURY AND DEATH IN COLLEGIATE ATHLETES.¹⁵⁸ Each institution should adopt requirements for the education and training of athletics personnel, including as a minimum, but not limited to, strength and conditioning professionals, sports coaches, and primary athletics healthcare providers on diabetic emergencies annually. The recommendations state that schools should develop well-rehearsed and venue-specific emergency action plans for a diabetic emergency. We have included a sample diabetic emergency action plan (see Appendix 1, Supplemental Digital Content 1, https://links.lww.com/JSM/A254)¹⁵⁹ to help schools comply.

SUMMARY

A collaboration of exercise scientists, family medicine physicians, sport medicine physicians, and endocrinology physicians developed this AMSSM Scientific Statement. This statement provides an overview of athletes and active people with diabetes, including the benefits of exercise in preventing and treating diabetes, potential risks for those with diabetes, recommended activities, nutrition and exercise practices, and injuries, rehabilitation, and other concerns for athletes with type 1 and type 2 diabetes. The document also discusses strategies for the team physician for managing blood glucose levels during various athletic activities, both competitive and recreational, and the use of new technologies in the management of diabetes.

DIABETES PREVALENCE IN ATHLETES

Although athletes with diabetes can be active at any age, many participate in organized sports and teams when they are youth or young adults. It is estimated that the number of people in the United States with diabetes aged 19 years and younger is 192,000 with about 167 000 T1DM, 20 000 type 2 diabetes mellitus (T2DM), and 5000 other types.⁶ The T1DM prevalence for the general population younger than 40 years is estimated to be 3.4 [95% confidence interval (CI), 2.7-4.3] per 1000 persons.⁷ The ratio of T1DM and T2DM changes with age. The Center for Disease Control and Prevention estimates 13.7 million people 18 to 64 years have diabetes, 90% of whom have type 2 diabetes.⁸ The prevalence of T1DM in sports is not well defined. The prevalence of T1DM in individuals 19 years and younger is 3.22 (95% CI, 3.11-3.34) per 1000 and 0.46 (95% CI, 0.43-0.49) per 1000 for those with T2DM.⁹ Recently, a pilot study showed that the prevalence among college-age student athletes is 3.42 (±2.36 SD) per 1000.¹⁰ This pilot study supports that T1DM is not limiting to the participation in Division 1 college athletics.

Type 1 Diabetes

Type 1 diabetes mellitus is a chronic metabolic disease characterized by a relative or absolute insulin deficiency. Most often diagnosed in children or adolescents, it can occur at any age. The typical development of T1DM is a gradual process occurring over months with the gradual onset of symptoms (fatigue, muscle soreness, polydipsia, polyuria, and polyphagia). Type 1 diabetes mellitus is an autoimmune disease characterized by cellular antibodies that may form against islet cells, insulin and glutamic acid decarboxylase.^11,12

Type 2 Diabetes

Type 2 diabetes mellitus, by far the more prevalent type (comprising 90%-95% of people with the disease), is primarily defined by a state of increased insulin resistance accompanied by elevated yet insufficient insulin production. Insulin resistance results in an elevation in blood glucose levels (fasting, postprandial, or both). Athletes with T2DM face many challenges, previously listed, to perform optimally during physical exercise. Therefore, they often limit or stop participation because of these challenges. The healthcare provider needs to address these things because physical activity is an integral part of the management of T2DM.¹³ The risk of T2DM is inversely related to obesity and central fat distribution, particularly visceral obesity, which can be altered with exercise.¹⁴ This is an example of why exercise plays an essential role in the prevention and treatment of T2DM.¹⁵

DATA SOURCE

The authors searched PubMed with the following terms: (Prevalence[TI] AND ((“Diabetes Mellitus, Type 2/epidemiology”[Mesh]) OR “Diabetes Mellitus, Type 1/epidemiology”[Mesh])) AND (“United States/epidemiology”[MeSH]) Diabetes[TI] AND exercise[TI] AND ("POSITION STATEMENT" or “CONSENSUS”) Diabetes AND exercise Filters: Meta-Analysis, Randomized Controlled Trial, Systematic Review diabetic AND medication and exercise “Insulin Pump” AND exercise “Continuous Glucose Monitoring” AND exercise Diabetes AND rehabilitation.