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diabetes and vigorous exercise diabetes and vigorous exercise

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CANADIAN JOURNAL OF DIABETES20063016371 pecial considerations are needed for the physically active individual with type 1 diabetes mellitusAlthough regular activityis beneficial for all patie ID: 453688

CANADIAN JOURNAL DIABETES.2006;30(1):63-71. pecial considerations

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diabetes and vigorous exercise CANADIAN JOURNAL OF DIABETES.2006;30(1):63-71. pecial considerations are needed for the physically active indi-vidual with type 1 diabetes mellitus.Although regular activityis beneficial for all patients,vigorous exercise can cause majordisturbances in blood glucose.The glycemic response dependslargely on the type,intensity and duration of the activity,asell as the circulating insulin and glucose counterregulatoryhormone concentrations.This review highlights a number ofstrategies to optimize blood glucose levels in patients withtype 1 diabetes who exercise vigorously. Il faut prendre des mesures particulires chez une personneteinte de diabte de type 1 qui est physiquement active.ÕactivitŽ rŽgulire profite ˆ tous les patients,mais les exer-cices violents peuvent provoquer de graves dŽsŽquilibres dela glycŽmie.La rŽponse glycŽmique dŽpend largement de lanature,de lÕintensitŽ et de la durŽe de lÕactivitŽ,de mmeque des concentrations circulantes dÕinsuline et dÕhormonesde la contre-rŽgulation glycŽmique.Ce compte renduprŽsente plusieurs stratŽgies visant ˆ optimiser la glycŽmiehez les patients atteints de diabte de type 1 qui font desexercices violents.ype 1 Diabetes and Vigorous Exercise:Applications of Exercise Physiology to Michael C.RiddellPhD,Bruce A.PerkinsDepartment ofKinesiology and Health Science,York University,Toronto,Ontario,Canada Division of Endocrinology and Metabolism,Department of Medicine,University ofToronto,Toronto,Ontario,CanadaThis manuscript is based in part on a presentation given at the 8th Annual Canadian Diabetes Association Professional Conferencand Annual Meetings,October 27Ð30,2004,Quebec City,Quebec,Canada ABSTRACT Address for correspondence:Michael C.Riddell Department of Kinesiology and Health ScienceUniversity347 Bethune College4700 Keele Streetoronto,Ontarioelephone:(416) 736-2100,ext.40493ax:(416) 736-5774E-mail:mriddellebsite:http://www.yorku.ca/mriddell/index.html Keywords:aerobic exercise,anaerobic exercise,yperglycemia,hypoglycemia 64 INTRODUCTIONDespite decades of improved insulin therapy and significantadvancements in blood glucose (BG) monitoring,largeexcursions in BG concentration remain a major challenge forthe active person with type 1 diabetes mellitus.The purposethis review is to highlight the benefits and risks associatedwith vigorous exercise,discuss the possible metabolic respons-es to various forms of exercise and suggest managementstrategies for patients who participate in vigorous exercise.BENEFITS AND RISKS OF EXERCISE INDIABETES MANAGEMENTEven before the 19th century,it was known that BG concen-trations typically decrease with endurance-type exercise inmost individuals with diabetes (1).In the 1950s,theAmerican physician E.P.Joslin emphasized the importance ofegular physical activity to effectively manage his patientsÕsymptoms.His idea of ÔvictoryÕwas the triad of nutrition,insulin and regular exercise to properly manage BG levelsnd thus provide a life free from complications from diabetes.or patients with either type 1 or type 2 diabetes,thereare both benefits and risks of regular exercise (Table 1).AnindividualÕs unique characteristics (e.g.age,sex,psychosocialmilieu),comorbid medical conditions and medications needto be considered by healthcare providers when prescribing atraining program.In fact,target work rates,used to deter-mine training intensity,require modification and definedlimits in the presence of coronary heart disease,hyperten-sion or microvascular complications.In particular,the typeand intensity of exercise may need to be limited in somepatients with retinopathy and neuropathy.Given the demonstrated benefits of low- to moderate-intensity exercise,with its minimal associated risks,the ben-efits of regular physical activity almost certainly outweigh thepotential side effects in the majority of individuals with dia-betes,even those with some complications from the disease.Unfortunately,training and competition are frequently asso-ciated with either hypo- or hyperglycemia in active peoplewith diabetes and very little is known about the effects of dia-betes on athletic performance.AEROBIC VS.ANAEROBIC EXERCISEExercise can be classified into 2 formsÑanaerobic and aero-during the activity.activities are characterized byhigher intensities of muscular contraction.Contractions aresustained by the phosphagen and anaerobic glycolytic systemsto produce lactic acid and energy in the form of adenosinetriphosphate.activities include sprinting,powerlifting,hockey and some motions during basketball and rac-quet sports.efers to the ability to work at ahigh level during these activities for relatively shortperiods (5 to 30 s).activities are characterized bylower rates of muscular contraction.These contractions usually have more prolonged durations and use carbohy-drates,fats and some protein for oxidation by mitochondriawithin the muscle.metabolism is the primary methodof energy production during endurance activities such asunning,cycling,rowing,swimming,soccer and ultra-endurance events.indicates the endurancecapacity (VO) of the individualÕs heart,lungs and musclesthat allows him/her the ability to offset fatigue over thecourse of an activity (game,practise,competition,etc.).It iscrucial to note that these and similar activities often includeshort bursts of anaerobic metabolism.The distinctionbetween the 2 types of exercise is important because of theirdistinct effects on BG concentration.For example,manyindividuals find that aerobic-type exercise causes BG todecrease both during and post-activity.On the other hand,anaerobic activities,which may only last for seconds,tend tocause dramatic increases in BG levels.MECHANISMS OF GLUCOSE REGULATIONDURING AEROBIC EXERCISEunderstand the possible metabolic responses to exercisein diabetes,it is useful to first describe the mechanisms ofglucose regulation in people without diabetes.eople without diabetesThe increased metabolic demand of exercise requires a dra-matic increase in fuel mobilization from sites of storage andan increase in fuel oxidation within the working muscle.Normally,the increase in fuel mobilization for oxidation isunder neuroendocrine control.During the transition fromest to exercise,the working muscles shift from using pre-dominantly free fatty acids released from adipose tissue to acomplex mixture of circulating fats,muscle triglycerides(TG),muscle glycogen and BG derived from liver glycogen. le 1.Benefits and risks of regular ercise in diabetes Benefits € Potentially lower A1C in€ Reduced risk of CVD,ypertension,colon cancer,obesity and osteoporosis€ Increased overall life€ Increased CV endurance,uscle fitness and flexibility€ Enhanced self-esteem andsense of well-being € Hyperglycemia€ Hypoglycemia€ Musculoskeletal injury€ CV accident (angina,dysrhythmia,sudden death)€ Deterioration of underlyingretinopathy and nephropathy A1C = glycosylated hemoglobinCVD = cardiovascular disease 65 During the initial stages of exercise,muscle glycogen is themain source of energy,but the reliance on this limited fuelsource decreases as the duration of exercise increases.As aesult,contributions from circulating free fatty acids and glu-cose in the blood stream increase to replace diminishinguscle glycogen stores.This greater reliance on liver glyco-gen can have dramatic effects on BG levels.The mixture of fuel utilization differs markedly depend-ing on the intensity of exercise.During low to moderateintensities,plasma-derived free fatty acids make up themajority of oxidized substrate.As the intensity increases,there is a greater reliance on carbohydrates.During heavy exercise,BG utilization may be as great as 1 to 1.5 g/min andthis fuel source must be continuously replaced at an equalrate or hypoglycemia will ensue (2).The mix of fuel utiliza-tion during exercise in people with type 1 diabetes appearsto be similar to that of people without diabetes,except thatindividuals with diabetes may have a slightly greater relianceon fat as an energy source and a slightly lower rate of carbo-ydrate oxidation (3,4).facilitate the changes in glucose delivery during exer-cise,pancreatic insulin secretion decreases and circulating lev-els of glucagon,growth hormonecortisol and catecholaminesincrease.The primary role of these hormonal changes is todiabetes and vigorous exercise CANADIAN JOURNAL OF DIABETES.2006;30(1):63-71. Figure 1.Schematic illustration of the BG response to exercise in non-diabetic or ideallycontrolled persons with diabetes (panel A),overinsulinized patients (panel B)or underinsulinized patients (panel C) BG balance is primarily a function of circulating insulin levels,counterregulatory hormone levels,parameters related to the exeitself (mode,duration,intensity) and characteristics of the individual.In this schema,the thickness of the block arrows represeflux.In panel A,glucose production matches glucose utilization and BG concentration is maintained in a euglycemic state.In panel B,a relatively high insulin concentration lowers hepatic glucose production and may further enhance glucose uptake resulting in adecrease in BG concentration.In panel C,a relatively low insulin concentration or an elevation in glucose counterregulatory hormone levels increase hepatic glucose production and lower glucose uptake resulting in an increase in BG concentration.BG = blood glucose 66 ensure an adequate supply of glucose for the exercising mus-cles (Figure 1A).Usually,the magnitude of change in thesehormones is greater with increasing exercise duration andintensity.That is,during prolonged heavy aerobic exercise(i.e.exercising for over 30 min at 60 to 80% of VO),theeduction in insulin secretion is more pronounced,while theelease of the other glucose counterregulatory hormones isincreased to a greater extent.eople with type 1 diabetesIn the individual with type 1 diabetes,the pancreas does notegulate insulin levels in response to exercise,making nor-mal fuel regulation nearly impossible.Moreover,there maybe deficiencies in the release of glucose counterregulatoryhormones that would normally help facilitate glucose pro-duction and release by the liver.As patients quickly discover,they may have either increases or decreases in BG levels dur-ing exercise.The inability to regulate the delivery of exoge-nous insulin into the bloodstream based on Òreal-timeÓglucose measurements and the failure to reduce insulin lev-els during exercise severely hampers the ability to exercise ina euglycemic state.The following sections outline the typicalproblems of over- and underinsulinization during exercisethat cause hypo- and hyperglycemia,respectively.VERINSULINIZATION AND HYPOGLYCEMIAThe results of the Diabetes Control and Complications Trialclearly show that near-normal and normal glycosylatedhemoglobin (A1C) levels limit the progression of long-termcomplications from diabetes (5).Indeed,most competitivethletes with diabetes may find that intensive insulin therapy,particularly insulin pump therapy,helps with BG manage-ment during exercise,since it allows for frequent changes ininsulin dosages.Although tight metabolic control is desirable,the movetoward more aggressive insulin therapy increases the risk ofexercise-associated hypoglycemia for some active peoplewith diabetes.Simply stated,hypoglycemia is the most severeacute complication of intensive insulin treatment,and exer-cise is a common behaviour that causes hypoglycemia (2).Intensive insulin therapy,whether it occurs via subcuta-neous injection or via insulin pump,frequently causeserinsulinization and hypoglycemia in active individualswith type 1 diabetes.Several factors contribute to overin-sulinization and hypoglycemia during exercise:1) The absorption of subcutaneously injected insulin may beincreased with exercise.The increase in subcutaneous andskeletal muscle blood flow resulting from exercise can beassociated with a concurrent increase in insulin absorption andaccelerated hypoglycemia (6).In addition,a rise in body tem-perature may increase insulin absorption rate and the inci-dence of hypoglycemia.It is important to note that exercisedoes not appear to alter insulin glargine absorption rate (7). Plasma insulin levels do not decrease during exercise.Theinability to decrease insulin levels during exercise afterinjection causes a relative hyperinsulinemia that impairshepatic glucose production and initiates hypoglycemia,usu-ally within 20 to 60 min after the onset of exercise (8,9).3) There is an exercise-induced increase in skeletal muscleinsulin sensitivity.During exercise there is a dramaticincrease in non-insulin-mediated muscle glucose uptakethat considerably reduces the need for circulating insulinlevels (2).Even when insulin dose is decreased prior toexercise,there is often a relative overinsulinization inpatients,as the pharmacokinetics of injected insulin do notprecisely meet the bodyÕs requirements for a prolongeddecrement of insulin secretion.Since the increase in insulinaction persists for several hours after the end of exercise(likely to help replenish muscle and liver glycogen stores),patients are at increased risk of hypoglycemia for severalhours after the cessation of exercise (Figure 1B) (10).Counterregulatory failureHypoglycemia during exercise may result from impairedelease of glucose-counterregulatory hormones caused by pre-vious exposure to either exercise or hypoglycemia (Figure 1B).Normally,both hypoglycemia and exercise cause similarincreases in glucagon secretion,reductions in insulin secre-tion,sympathetic nervous system activity and activation of theypothalamic-pituitary-adrenal axis.Neuropathic complica-tions of diabetes and poor glycemic control reduce the coun-terregulatory responses to either exercise or hypoglycemia(2).Not surprisingly,this finding of a blunted counterregula-tory response to exercise is similar to the scenario that occursin intensively treated patients with diabetes who developdefects in counterregulatory responses to hypoglycemia (11).or those pursuing vigorous aerobic activity,a vicious cyclemay be created whereby an episode of prior hypoglycemia mayeduce counterregulatory responses to subsequent exercise,thereby predisposing the individual to hypoglycemia.This,inturn,could blunt counterregulatory responses to additionalepisodes of exercise and/or hypoglycemia.As a result,indi-viduals with type 1 diabetes who experience hypoglycemia ondays preceding competition may have an elevated risk of hypo-glycemia and autonomic counterregulatory failure duringexercise.It should also be noted that the energy expenditureitself will predispose the individual to hypoglycemia for ~24 hafter the end of exercise,as insulin sensitivity remains elevat-ed (see point 3 above) (10).UNDERINSULINIZATION AND HYPERGLYCEMIAIn individuals with poor metabolic control,exercise can causean additional increase in BG concentration and ketoacidosis.he rise in BG is caused by exaggerated hepatic glucose production and impairment in exercise-induced glucose utilization (Figure 1C).Hyperglycemia and excessive ketosis 67 during exercise are particularly undesirable since they causedehydration and may decrease blood pH,both of whichimpair exercise performance.Intense exercise (i.e.�60 to70% VO�or 75 to 85% of maximal heart rate) may par-ticularly aggravate this condition,since increases in cate-holamines and glucocorticoids will further exaggerate theelevations in BG concentrations and ketone production (12).HIGH-INTENSITY EXERCISE AND HYPERGLYCEMIAHigh-intensity exercise may be defined as activities above theÒlactate threshold,Ówhich is approximatel�y 60 to 70%or 85 to 90% maximal heart rate.This thresholdcoincides with dramatic elevations in catecholamines,freefatty acids and ketone bodies,all of which impair muscle glu-cose utilization.Even those individuals on multiple dailyinsulin injections or those on pump therapy may haveincreases in BG levels during and after high-intensity exercise(13),likely due to a failure in insulin release to offset theincreases in counterregulatory hormones (Figure 1C).Thisise in BG concentration is usually transient and tends to lastonly as long as there are elevations in counterregulary hormones (i.e.30 to 60 min).Although some individuals can easily correct the elevations with an insulin bolus,particular-if they take rapid-acting insulin analogues,others may be resistant to taking additional insulin following exercise,since there will be greater risk of late-onset post-exercise hypoglycemia in the next several hours (particular-if the prior exercise bout w�as 30 min).COMPETITION STRESS,HEAT STRESSAND HYPERGLYCEMIAThe psychological stress of competition is frequently associ-ted with increases in BG levels even if the pre-exercise BGconcentrations are normal.Those pursuing vigorous aerobicexercise may find that on regular training or practice daysthey become hypoglycemic,but on the day of competitionthey develop hyperglycemia.Although empirical data do notexist for patients with type 1 diabetes,excessive increases incounterregulatory hormones likely occur just prior to exer-cise,when anticipatory stress is high.It is also probable thatthe stress during competition can further increase BG levels.The elevated levels of these stress hormones are known toincrease hepatic glucose production dramatically anddecrease peripheral glucose uptake.In people with diabetes,the bodyÕs failure to compensate for the ÒstressÓassociateddiabetes and vigorous exercise CANADIAN JOURNAL OF DIABETES.2006;30(1):63-71. le 2.Practical guidelines to limit BG excursions before,during and after exercise Before exercise € Determine the timing,mode,duration and intensity of exercise€ Eat a carbohydrate meal 1…3 h prior to exercise€ Assess metabolic control:… If BG is els are decreasing,extra calories may be needed… If BG is 5…13.9 mmol/L,extra calories may not be needed,depending on the duration of exercise and individual response to exercise14.0 mmol/L and urine or blood ketones are present,delay exercise until levels are normalizedwith insulin administration€ If the activity is aerobic,estimate energy expenditure and determine if insulin or additional carbohydrate will… If insulin dose is to be adjusted for long-duration and/or moderate- to high-intensity activities,try a 50% pre-meal insulin dose reduction 1 h prior to exercise.Dosages can be altered on subsequent exercise days,based on the measured individual response.Insulin should be injected into a site distal tothe exercising muscles and into subcutaneous tissue.… If carbohydrate intake is to be increased,try 1 g/kg body weight/hour of moderate- to high-intensityexercise performed during peak insulin activity and less carbohydrate as the time since insulin injectionincreases.The amount of carbohydrate can be altered on subsequent exercise days,based on the measured individual responses.The total dose of carbohydrate should be divided equally and consumedat 20-min intervals.€ If the exercise is anaerobic or occurring during heat or accompanied by competition stress,an increase ininsulin may be needed.€ Consider fluid intake to maintain hydration (~250 mL 20 min prior to exercise) During exercise € Monitor BG every 30 min€ Continue fluid intake (250 mL every 20…30 min)€ If required,consume carbohydrate at 20…30-min intervals (see above) After exercise € Monitor BG,including overnight,if amount of exercise is not habitual€ Consider adjusting insulin therapy to decrease immediate and delayed insulin action€ Consider consuming additional slow-acting carbohydrate to protect against post-exercise late-onset ypoglycemia BG = blood glucose 68 with exercise by increasing insulin secretion may make themparticularly susceptible to hyperglycemia during some formsof competition (Figure 1C).Some patients may find thisyperglycemic response to stressful competition frustrating,particularly when they are participating in team sports thatnecessitate breaks in play (e.g.baseball,basketball,hockey).In these instances,periods of physical inactivity coupled withelevations in stress hormones may cause particularly largeincreases in BG concentration.Again,frequent BG monitor-ing and small boluses of rapid-acting insulin may be requiredto recover from these fluctuations.Individuals may find that training or competing in warmand humid environments also elevates BG levels,likelybecause of excessive increases in circulating plasma cate-holamines,glucagon,cortisol and growth hormone (14).PRACTICAL CONSIDERATIONS FORPREVENTING HYPOGLYCEMIA ORHYPERGLYCEMIA DURING EXERCISEThere are a number of strategies available to help stabilizeBG concentrations during exercise (Table 2).Unfortunately,it is impossible to give precise guidelines for diet and insulintherapy that will be suitable for all individuals who wish to bephysically active.The factors most affecting BG fluctuationsduring exercise appear to be circulating plasma insulin levels,intensity and duration of exercise and the type of exercise(aerobic vs.anaerobic).Other variables that influence themetabolic responses to exercise,albeit to a lesser extent,include age,gender,level of metabolic control,level of aer-obic fitness and prevailing concentrations of the glucosecounterregulatory hormones.Although highly specific guide-lines are not possible,some general strategies can be appliedto help prevent dramatic BG excursions during exercise.MonitoringFrequent self-monitoring of BG and information about theexercise,insulin administration and carbohydrate intakeshould be recorded so that immediate risks of hypoglycemiaand hyperglycemia may be identified.First,it is helpful tohave an exercise-training log that documents the type,timingand duration of exercise performed.Second,it is best to have2 or 3 pre-exercise glucose measurements at 30-min inter-als so that directions of change in BG can be determinedprior to the activity.Making insulin and/or carbohydrateadjustments based solely on 1 glucose measurement is risky,as the individual is aware of neither the direction nor the rateof this change.Third,individuals ery 30 min during exercise and every 2 h after the end ofexercise for up to 2 readings.Monitoring this frequently priorto,during and after exercise is recommended,particularly ifthe individual is undertaking a new training regimen or exer-cise activity.Additional post-exercise measurements may beneeded for up to 24 hours after the end of exercise to guardagainst post-exercise late-onset hycemia.Both patients and healthcare providers should be aware that although someindividuals may claim to know or ÒfeelÓtheir BG levels dur-ing exercise,there is no evidence to support this.Exercisemay mask many of the symptoms of changes in BG,and indi-viduals tend to overestimate their levels when they are hypo-glycemic and underestimate levels when they areyperglycemic (15).Finally,there should also be documenta-tion of the estimated carbohydrate intake prior to,duringand after exercise as well as the location,dose and timing ofinsulin injection.Self-monitoring of BG and accurate recordeeping of all these variables provide feedback for bothpatients and healthcare professionals that will form the basisfor implementing insulin and/or nutritional strategies forsubsequent exercise bouts.Although exercise conditions vary,evidence suggests thatBG responses to exercise have some degree of reproducibility(16),making individualized therapeutic recommendations pos-sible.Ideally,for maximal metabolic control and performance,thletes may consider newly developed continuous glucosemonitoring devices and insulin pump therapy,since changes inBG concentration can be particularly rapid during exercise andthe risk of post-exercise late-onset hypoglycemia is high.Pre-exercise BGIf pre-exercise BG readings are not rising andthe activity is primarily aerobic (e.g.prolonged running,cling,soccer),the risk of exercise-associated hypoglycemiais substantial (2).In these cases,it is suggested that exercisenot be initiated without the ingestion of at least 15 g of carbo-ydrate.On the other hand,if fasting BG is and ketone bodies are present in the urine,patients are gen-erally advised to administer more insulin and delay exercis-ing (2).The knowledge of ketone production may beparticularly important since it is common for individuals toexercise post-meal with starting BG levels between 10 and15 mmol/L,although not ketotic.These individuals mayexperience dramatic decreases in BG,likely due to risinginsulin levels during the activity.Again,it is important toknow the direction and rate of change in BG,both prior toand during exercise,so that diet and/or insulin regimens canbe modified to prevent hypo- or hyperglycemia.For exam-ple,a BG level of 5.5 mmol/L may be considered safe forexercise if the previous measurement was 5 mmol/L,where-as the same reading of 5.5 mmol/L indicates a potentiallydangerous imbalance of glucose production and utilization ifthe preceding measurement was 7 mmol/L.Clearly,in thelatter situation,carbohydrate intake would be necessary toprevent hypoglycemia.Some individuals may wish to allowBG levels to be slightly higher just prior to and during exer-cise as a further safeguard against hypoglycemia.Insulin adjustments for exerciseIt is clear that reducing insulin dosage in anticipation of exer-cise decreases the risk of hypoglycemia and is the best way to 69 mimic the normal physiological response to exercise.This isparticularly important if the exercise is performed postpran-dially when insulin levels are generally the highest.Individuals treated with intensive insulin therapy can becomeypoglycemic within 45 min of strenuous exercise per-formed 2 h after a standard meal and their usual insulin dose(8,9).A 30 to 50% reduction in bolus insulin deliveryeduces the likelihood of developing hypoglycemia in thesesame patients (9).It is important to note that it may not benecessary to reduce the insulin dose if the start of exerciseoccurs several hours after a meal,when insulin levels are low.or prolonged exercise (i.e.90 min),a greater reduc-tion in insulin dosage may be needed.For example,it hasbeen shown that cross-country skiers with type 1 diabetesare able to exercise for several hours without becomingypoglycemic if the insulin dose is reduced by 80% com-pared with only 90 min if the dose is reduced by only 50%(17).In general,higher aerobic exercise intensities that lastfor prolonged periods elicit a greater drop in BG and aeater need for reduced insulin dosage (17-20).Injecting insulin in a subcutaneous depot well away froman exercising muscle may minimize the risk of hypoglycemiato some degree (21),although the effects of exercise on thekinetics of rapid-acting insulin analogues are not well under-stood.Individuals should be cautious about injecting insulininto the muscle tissue itself,since it may dramaticallyincrease the insulin absorption rate (22).Further considera-tions for quantifying insulin pump adjustments during exer-cise are provided in the companion paper (23).Carbohydrate adjustments for exerciseBecause exercise is often spontaneous,it is not always possi-le to anticipate the need to decrease the insulin dosage.Inaddition,some patients find that lowering their insulin dosethe meal prior to exercise causes an initial hyperglycemicesponse that impairs their exercise performance (see ÒBGlevels and exercise performanceÓbelow).In these instances,carbohydrate ingestion is a viable option,and possibly theonly alternative to maintain BG levels during exercise (24).Recommendations for the amounts and forms of carbohy-drate intake during competition are discussed below.MACRONUTRIENT ADJUSTMENTS FORTRAINING AND COMPETITIONor the endurance athlete,nutritional strategies to optimizecarbohydrate stores in muscle and liver are essential to opti-mize training and performance.Nutritional strategies can bedivided into 4 categories:1) daily caloric intake during train-ing;2) caloric intake hours prior to exercise;3) nutrientintake during exercise;and 4) intake following exercise.Daily macronutrient intakeThe recommended distribution of macronutrients for thethlete with diabetes is 55 to 60% of total energy intake as arbohydrate:25 to 30% as fat,and 12 to 15% as protein (25).It is important to note that intense daily training will acutelyeduce the bodyÕs stores of carbohydrate.If carbohydratestores are not replenished after each exercise session,endurance capacity will be impaired and the individual maybe at increased risk of hypoglycemia.It is generally recom-mended that the majority of carbohydrates be complex (e.g.whole grains,beans) to limit post-meal hyperglycemia andelevated needs for insulin.Endurance athletes should consumeapproximately 8 to 10 g carbohydrate/kg body weight/day(25).Although protein is not a major fuel source oxidizedduring exercise,adequate intake is essential to allow for mus-cle regeneration and hypertrophy during training.It is gener-ally recommended that 0.8 to 1 g protein/kg body weight issufficient for recreational athletes,while those involved inompetition and heavy training may need up to 1.7 g protein/kg body weight/day (26).Precompetition nutritionDuring the hours prior to competition,it is critical to main-tain BG levels in the near-normal range (4 to 7 mmol/L) tolimit the risks of dehydration,extreme lethargy,hypo-glycemia and associated autonomic counterregulatory fail-ure.This may be accomplished by frequent BG monitoringand refinements in either insulin and/or carbohydrateintake.Individuals may need small increases in insulin priorto competition to counter the stress-associated increases inglucose counterregulatory hormones.Ideally,a meal 3 to 4 h prior to competition is desirable since it will maximizeenergy stores and should not cause gastric upset.If possible,a carbohydrate beverage containing 1 to 2 g carbo-ydrate/kg body weight should be consumed 1 h prior tocompetition to maximize pre-exercise glycogen stores,provid-ing energy for oxidation and fluid for maintenance of adequateydration.Generally,6% carbohydrate-electrolyte beveragescomposed of simple sugars (i.e.sucrose,fructose) are best,since they have optimal fluid and carbohydrate absorption ratescompared with other more concentrated beverages such asjuice or carbonated drinks that may delay gastric absorption andcause stomach upset.Water may also be suitable if pre-exerciseBG concentrations are elevated (i.e.�10 mmol/L).many endurance athletes train or compete after an overnightast,perhaps to limit any gastric upset that may occur witheating during periods of stress,this practice in a patient withtype 1 diabetes will reduce hepatic glycogen storage and maypredispose the individual to exercise-associated hypo-glycemia and premature fatigue.During competitionDuring prolonged competitions,particularly if the pre-exercisensulin dose is not reduced significantly,carbohydrate ingestion is essential for maintaining BG concentrations.Carbohydrate intake delays fatigue and provides fuel for oxi-dation by the working muscles.The amount of carbohydratediabetes and vigorous exercise CANADIAN JOURNAL OF DIABETES.2006;30(1):63-71. 70 consumed depends on a number of variables including theexercise intensity,gender,age,and the timing and dose of thelast insulin injection.As a general rule,1 to 1.5 g carbohydrate/kg body weight/h should be consumed during exercise per-formed during peak insulin action (2).This amount may beconsiderably lower if exercise is performed when circulatinginsulin levels are low.For example,60 min of moderate-intensity aerobic exercise performed 1 h after insulin admin-istration was shown to require ~1 g/kg body weight ofcarbohydrate to prevent hypoglycemia,while these sameindividuals needed only ~0.5 g/kg and only 0.25 g/kg whenthe same exercise was performed 2.5 and 4 h after insulinadministration,respectively (27).It is important to note thatthese guidelines for carbohydrate intake are in addition toany carbohydrates ingested in the meal prior to exercise.Foractive children with type 1 diabetes,carbohydrate intakematched to total carbohydrate utilization (~1.5 g carbo-ydrate/kg body weight/h of exercise) limits hypoglycemiaduring moderate-intensity exercise (8).Consuming bohydrate,rather than adjusting insulin,is advantageoussince a childÕs activities are often spontaneous and of unpre-dictable duration and intensity.In these instances,tables ofÒexercise exchangesÓcan be used to prescribe carbohydrateintake for a variety of activities and sports performed duringpeak insulin times (15,24).As discussed in the companionpaper by Perkins (23),insulin pump therapy provides theoption of spontaneous insulin dose changes for exercise.Inaddition,estimates of insulin adjustments based on energyexpenditures can be calculated and tested.Nonetheless,thesume extra carbohydrate for training and competition,sincehigh ingestion rates have been associated with improved per-formance by both maintaining high rates of glucose oxidationand by sparing hepatic glycogen stores (2).During exercise,it is imperative to prevent dehydration,which is associated with impaired performance,musclecramps,hyperglycemia and heat stroke,the latter of whichmay even result in death.Ideally,fluid intake should closelymatch sweating rate during exercise.Sweating rates rangefrom 0.75 to 1 L/h depending on the exercise intensity,ambient temperature and relative humidity.On average,fluid intake should be approximately 250 mL every 20 min of exercise and the first drink should precede exercise by 20 min (26).Again,carbohydrate-electrolyte beverages may�be best for activities lasting 60 min,since they contain bothequirements of carbohydrate and fluid.Nutrient intake following exerciseost-exercise,carbohydrate intake is necessary to help replen-ish liver and muscle glycogen stores.During this period,whichmay last up to 12 to 24 h,insulin sensitivity remains elevatedand there is a high risk of hypoglycemia in patients with diabetes (10).To quickly replenish muscle glycogen stores,perhaps for subsequent competition,carbohydrate intake should be started within the first few hours after the end ofexercise.For patients who tend to experience post-exerciselate-onset hypoglycemia during the night,a complex carbohy-drate (e.g.uncooked corn starch) or a mixed snack containingt and protein may be particularly beneficial at bedtime (28).BG LEVELS AND ATHLETIC PERFORMANCESurprisingly,there are few published studies on BG concen-trations and athletic performance in individuals with type 1diabetes.Clearly,in athletes without diabetes,hypoglycemiadramatically lowers exercise performance,increases the rat-ing of perceived exertion (RPE) and causes prematurefatigue during prolonged exercise.Likely,the same is truefor athletes with type 1 diabetes who become hypoglycemicmore frequently.Hypoglycemia and the deterioration ofexercise performance can be dramatically reversed with car-bohydrate ingestion during exercise.For example,in activeadolescents with type 1 diabetes,hypoglycemia reducesexercise endurance and the consumption of carbohydratethat attenuates the drop in BG improves their capacity (8).Hyperglycemia likely impairs performance in individualswith type 1 diabetes for 2 reasons.First,if hyperglycemiaexists prior to exercise,the individual may already be dehy-drated.Evidence suggests that even a 1% decrease in bodymass because of dehydration noticeably impairs performance(26).Second,hyperglycemia has been associated with theeduced ability to secrete beta-endorphins during exercise (29)and is associated with increases in RPE for leg effort (29) andwhole-body effort (30).Interestingly,poor metabolic control,as measured byA1C levels,is associated with poor maximal aerobic capacityin both patients with type 1 (31) and type 2 (32) diabetes.Assuch,it may be particularly important to maintain goodmetabolic control during training and competition to maxi-mize aerobic performance.Special considerations are needed for the physically activeindividual with diabetes.Although regular exercise is benefi-cial for all patients,exercise training and competition cancause major disturbances in BG control.Both insulin andnutritional adjustments are often required because of thestress associated with activity and the profound changes ininsulin sensitivity that accompany exercise.Reductions ininsulin and increases in carbohydrate and fluid intake allowindividuals to compete and excel during vigorous exercise.CKNOWLEDGEMENTSDr.Riddell is grateful to K.Iscoe for her assistance in prepar-ing this manuscript.No duality of interest declared. 71 1.Riddell MC,Ruderman NB,Berger M,et al.Exercise physiol-ogy and diabetes:From antiquity to the age of exercise sci-ences.In:Ruderman NB,Devlin JT,Schneider S,et al,eds.Handbook of Exercise in Diabeteslexandria,VA:AmericanDiabetes Association;2002:3-16.2.Wasserman DH,Davis SN,Zinman B.Fuel metabolism duringexercise in health and diabetes.In:Ruderman NB,Devlin JT,Schneider S,et al,eds.Handbook of Exercise in DiabetesAlexandria,VA:American Diabetes Association;2002:63-100.3.Raguso CA,Coggan AR,Gastaldelli A,et al.Lipid and carbo-ydrate metabolism in IDDM during moderate and intenseexercise.4.Riddell MC,Bar-Or O,Hollidge-Horvat M,et al.Glucoseingestion and substrate utilization during exercise in boys withJ Appl PhysiolThe Diabetes Control and Complications Trial ResearchGroup.The effect of intensive treatment of diabetes on thedevelopment and progression of long-term complications ininsulin-dependent diabetes mellitus.6.Zinman B,Murray FT,Vranic M,et al.Glucoregulation duringmoderate exercise in insulin treated diabetics.J Clin Endocrinol7.Peter R,Luzio SD,Dunseath G,et al.Effects of exercise on theabsorption of insulin glargine in patients with type 1 diabetes.Diabetes Care8.Riddell MC,Bar-Or O,Ayub BV,et al.Glucose ingestionmatched with total carbohydrate utilization attenuates hypo-glycemia during exercise in adolescents with IDDM.Int J Sport9.Schiffrin A,Parikh S.Accommodating planned exercise in type I diabetic patients on intensive treatment.Diabetes Care10.McDonald MJ.Postexercise late-onset hypoglycemia in insulin-dependent diabetic patients.Diabetes Care11.Dagogo-Jack SE,Craft S,Cryer PE.Hypoglycemia-associatedautonomic failure in insulin-dependent diabetes mellitus.Recent antecedent hypoglycemia reduces autonomic respons-es to,symptoms of,and defence against subsequent hypo-glycemia.J Clin Invest12.Marliss EB,Vranic M.Intense exercise has unique effects onboth insulin release and its roles in glucoregulation:implica-tions for diabetes.13.Mitchell TH,Abraham G,Schiffrin A,et al.Hyperglycemiaafter intense exercise in IDDM subjects during continuousDiabetes Care14.Hargreaves M,Angus D,Howlett K,et al.Effect of heat stresson glucose kinetics during exercise.J Appl PhysiolRiddell MC,Bar-Or O.Children and adolescents.In:Ruderman NB,Devlin JT,Schneider S,et al,eds.Exercise in DiabetesAlexandria,VA:American DiabetesAssociation;2002:547-566.16.McNiven-Temple MY,Bar-Or O,Riddell MC.The reliability and repeatability of the blood glucose response to 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exercise:usingthe insulin pump to maximum advantage.24.Grimm JJ,Ybarra J,Berne C,et al.A new table for preventionof hypoglycaemia during physical activity in type 1 diabeticpatients.Franz MJ.Nutrition,physical activity,and diabetes.In:Ruderman NB,Devlin JT,Schneider S,et al,eds.Exercise in DiabetesAlexandria,VA:American DiabetesAssociation;2002:321-338.etrie HJ,Stover EA,Horswill CA.Nutritional concerns for thehild and adolescent competitor.Nutrition27.Francescato MP,Geat M,Fusi S,et al.Carbohydrate require-ment and insulin concentration during moderate exercise intype 1 diabetic patients.28.Kalergis M,Schiffrin A,Gougeon R,et al.Impact of bedtimesnack composition on prevention of nocturnal hypoglycemia inadults with type 1 diabetes undergoing intensive insulin man-agement using lispro insulin before meals:A randomized,placebo-controlled,crossover trial.Diabetes Care29.Wanke T,Auinger M,Formanek D,et al.Defective endogenousopioid response to exercise in type I diabetic 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