Physical activity,sedentary behaviors,physical fitness,and their relation to health outcomes in youth with type 1 and type 2 diabetes: A review of the epidemiologic literature

Angla D.Lis,Xiaoguang Ma,David M.Maahs,Jnnifr L.Trilk

aCenter for Research in Nutrition and Health Disparities,Department of Epidemiology and Biostatistics,Arnold School of Public Health,University of South Carolina,Columbia,SC 29208,USA

bDepartment of Epidemiology and Biostatistics,Arnold School of Public Health,University of South Carolina,Columbia,SC 29208,USA

cBarbara Davis Center for Childhood Diabetes,Department of Pediatrics and School of Public Health,University of Colorado Denver,Aurora,CO 80045,USA

dDepartment of Epidemiology,University of Colorado Denver,Aurora,CO 80045,USA

eDepartment of Biomedical Sciences,University of South Carolina School of Medicine Greenville,Greenville,SC 29605,USA

Physical activity,sedentary behaviors,physical fitness,and their relation to health outcomes in youth with type 1 and type 2 diabetes: A review of the epidemiologic literature

Angela D.Liesea,*,Xiaoguang Mab,David M.Maahsc,d,Jennifer L.Trilke

aCenter for Research in Nutrition and Health Disparities,Department of Epidemiology and Biostatistics,Arnold School of Public Health,University of South Carolina,Columbia,SC 29208,USA

bDepartment of Epidemiology and Biostatistics,Arnold School of Public Health,University of South Carolina,Columbia,SC 29208,USA

cBarbara Davis Center for Childhood Diabetes,Department of Pediatrics and School of Public Health,University of Colorado Denver,Aurora,CO 80045,USA

dDepartment of Epidemiology,University of Colorado Denver,Aurora,CO 80045,USA

eDepartment of Biomedical Sciences,University of South Carolina School of Medicine Greenville,Greenville,SC 29605,USA

Diabetes is a leading chronic disease of childhood and adolescence.In addition to the well-known auto-immune,insulin-dependent diabetes mellitus(type 1 diabetes(T1D)),the past two decades have witnessed the emergence of type 2 diabetes(T2D)in children and adolescents,which previously was only seen in middle-aged or older adults.One of the key components of diabetes management is physical activity(PA).The beneficial effects of increased PA and decreased sedentary behavior are extremely important in youth with diabetes because of the markedly increased long-term risk of cardiovascular disease in this population compared to persons without diabetes.This review aims to comprehensively summarize the epidemiologic,observational research published and listed in PubMed between 1970 and 2012 on PA and sedentary behaviors,as well as physical fitness in children and adolescents with T1D and T2D.Additionally,we describe briefly the state of knowledge on perceived barriers of PA in persons with diabetes,with a focus on hypoglycemia.Finally,we provide an overview of the epidemiological literature pertaining to health benefits of increased PA in youth with T1D and T2D and briefly discuss the topic of exercise-related hypoglycemia.

Copyright?2012,Shanghai University of Sport.Production and hosting by Elsevier B.V.All rights reserved.

Cardiovascular risk;Children;Exercise;Glycemic control;Hypoglycemia;Physical activity;Physical fitness;Sedentary behavior;Type 1 diabetes mellitus;Type 2 diabetes mellitus;Youth

1.Introduction

One of the leading chronic diseases of childhood and adolescence is auto-immune,insulin-dependent diabetes mellitus,which now is commonly referred to as type 1 diabetes (T1D).In T1D,the destruction of pancreatic beta cells leads to insulin deficiency and lifelong dependency on insulin therapy. Unfortunately,the risk of T1D is increasing worldwide at about 2%—3%per year,which has recently been confirmed for non-Hispanic white youth in the United States(USA).1—3In 2001,more than 140,000 youth under the age of 20 years inthe USA were affected by this incurable disease4and likely about 3 million persons of all age groups in total.5,6Recent estimates from the SEARCH for diabetes in youth study7suggest that the burden has substantially increased from 2001 to 2009.8,9Despite improvements in treatment of T1D, the trends for cardiovascular complications have not improved.10Persons with T1D still exhibit a greater than three-fold higher risk of acute cardiovascular disease(CVD) compared to persons without diabetes,resulting in approximately 7 years of lower life expectancy.11—15Among youth with T1D,14%have two or more CVD risk factors,166%have hypertension,17and 19%present with lipid abnormalities.18While adiposity historically has not been considered a characteristic of T1D,the prevalence of overweight(22%)in youth with T1D is higher than their peers without diabetes(16%), while the prevalence of obesity is lower in T1D(13%)than in youth without diabetes(17%).19The increases in adiposity in T1D may offset some of the improvements made in T1D care in the past.20

Furthermore,the past two decades have witnessed the emergence of type 2 diabetes(T2D)in youth,formerly known as non-insulin dependent diabetes mellitus,and previously only seen in middle-aged or older adults.21—24In 2006—2007, the SEARCH for Diabetes in Youth study published some of the first population-based data on the prevalence and incidence of youth T2D in the USA and found that T2D was present in all racial and ethnic groups.4,25More recent estimates from SEARCH suggest that the prevalence has increased by more than 20%from 2001 to 2009.26Overweight and obesity are extremely common in T2D,affecting about 90%of youth19and 92%have two or more CVD risk factors.16Hypertension affects approximately 23%of youth with diabetes and lipid abnormalities about 33%.18Youth with T1D have been designated Tier 1(high)risk for CVD by the American Heart Association(AHA),as they constitute a population for which there is“pathological and/or clinical evidence for manifest coronary heart disease before 30 years of age”.27Youth with T2D have been designated as Tier 2(moderate)risk for CVD, which is defined as“pathophysiological evidence for arterial dysfunction indicative of accelerated atherosclerosis before 30 years of age”.27

In this context,the importance of physical activity(PA)is evident,as it is one of the few behavioral factors that have been shown to decrease the risk of CVD and many other chronic conditions.28,29PA is defined as any bodily movement produced by skeletal muscles that requires energy expenditure.29It is therefore not surprising that PA is recognized as one of the four cornerstones of care for persons with diabetes, along with medical nutritional therapy(MNT),glucose monitoring,and medication-based(insulin-based for T1D) management for the achievement of good glycemic control.30Patient care is highly advanced for insulin treatment,glucose monitoring and MNT.31However,clinical guidelines for exercise and PA,although largely based on evidence on the relation of PA and T2D,are still evolving for T1D youth.In addition,physical fitness,a broad concept encompassing several specific types of fitness including aerobic power, strength,flexibility,and balance32is important for persons with diabetes33and also is closely related to all-cause mortality.34,35Therefore,it is included in our review.

According to the 2008 Physical Activity Guidelines for Americans,“being physically active is one of the most important steps that Americans of all ages can take to improve their health”.28Children and adolescents should engage in 60 min daily of moderate-to-vigorous PA(MVPA).The recommendations by the American Academy for Pediatric36and the World Health Organization37are essentially identical.A joint statement issued by the American Diabetes Association and the American College of Sports Medicine recommends 150 min/week of moderate-to-vigorous activity for adults with T2D,“spread out during at least 3 days during the week,with no more than 2 consecutive days between bouts of aerobic activity”.38Additionally,“…persons with type 2 diabetes should undertake moderate-to-vigorous resistance training at least 2—3 days/week”.38Current data suggest that only 8%of U.S.youth meet the 60-min/day MVPA recommendation,based on accelerometer data,and that many youth exhibit sedentary behavior and are subsequently largely physically inactive.39Summarizing what is known about current PA in youth with T1D and T2D in the USA and worldwide is one of the key aims of this review.Additionally, we also aim to summarize information on sedentary behaviors, defined as“… any waking behavior characterized by an energy expenditure≤1.5 METs while in a sitting or reclining posture”according to the Sedentary Behaviour Research Network(SBRN).40We focus on the health risks of sedentary behavior because physical inactivity has been identified as the fourth leading risk factor for global mortality causing an estimated 3.2 million deaths globally.29Therefore,it is essential that more information be obtained regarding PA and sedentary behaviors in T1D and T2D youth.

Recently,Chimen et al.41published a comprehensive review on the health benefits of PA in T1D focusing on intervention studies.While intervention studies are the gold standard to determining causality,they typically reflect very specific,controlled conditions.Observational research,on the other hand,offers insights into the actual behavior of individuals in free-living situations.Thus,this review will focus on epidemiologic research on PA,and sedentary behaviors and physical fitness in children and adolescents(henceforth referred to as“youth”)with T1D and T2D,with youth broadly considered as persons in the first two decades of life.Specifically,this review will address the following:

1.What is known about PA,sedentary behaviors,and physical fitness in youth with T1D and T2D,including the most frequent types,intensities,and settings of PA behaviors in real-life settings?

2.What is known about perceived barriers to PA,including fear of hypoglycemia,in youth with T1D?

3.What can be learned from observational research to date about the health benefits of PA,sedentary behaviors,and physical fitness in youth with T1D and T2D?

2.Methods

Epidemiological studies on PA and diabetes mellitus in youth were identi fied through Medline/PubMed(MeSH)and key word search terms were“type 1 diabetes mellitus”,“type 2 diabetes mellitus”,“insulin dependent diabetes mellitus”,“IDDM”,and“NIDDM”for diabetes mellitus,“physical activity”,“exercise”,“physical fitness”for PA and fitness,“sedentary lifestyle”, “sedentary behavior”, “sedentary behaviour”,“television”,“video game”,“internet”,“homework”,“reading”,“physical inactivity”,“media use”,“sitting”for sedentary behavior,and“children”,“youth”,“adolescent”,“children,preschool”for youth.

Initially,837 articles were identi fied in PubMed with the combination of above MeSH and key word search terms.We limited our search to include entries from January 1,1970 to August 31,2012,written in English and performed on human subjects,which reduced the number of articles to 760.We then used the filters from PubMed to remove clinical trials(124), meta-analysis studies and reviews(137),clinical guidelines (4),and editorials(15).In the end,480 articles were included in the manual review process.

One member of the research team(XM)reviewed these articles(titles and abstracts)identi fied from PubMed in order to identify those that clearly focused on PA(or physical fitness)and diabetes mellitus in youth and had been conducted with an observational study design(e.g.,cross-sectional studies,case-control studies,cohort studies,follow-up studies, case studies,and reports).For articles without abstracts or without study design information in the abstract,we requested the full-length version of the article.Further review of eligible observationalstudieswasconducted by research team members(ADL,XM)with the inclusion criteria in mind.To meet out inclusion criteria,studies had to present original data and results on PA,sedentary behaviors or physical fitness in youth with T1D or T2D and had to be observational in nature. In the 480 studies,most studies were performed among adults, did not focus on PA or fitness,or were conducted with intervention designs(as the systematic identification of clinical trials as a publication type in PubMed was only introduced in 2008 and applied retrospectively through 1991).In the end, there were 38 studies meeting our inclusion criteria.Among these,one letter was included because the authors reported original results.

The reference list of each eligible publication was carefully reviewed to identify additional studies(3 studies)which were not identified in the PubMed search.If multiple publications originated from the same study,all were included as long as the results were not duplicative.We also included one study focusing on energy expenditure measured using Armbands and two studies that were in press.In the end,n=44 observational studies on PA,sedentary behaviors,or physical fitness and diabetes in youth were included.

Furthermore,since hypoglycemia can be a serious consequence of PA in persons with T1D and T2D,we also examined these 44 publications for studies examining barriers to physical activities,specifically fear of hypoglycemia,and provided a brief overview of the issue.While a comprehensive review of hypoglycemia is a topic onto itself,42—45our interest here was in how hypoglycemic fear affects PA and therefore we focused our paper accordingly.Lastly,we discussed the epidemiologic studies focusing on health benefits of PA or fitness in youth with T1D or T2D in the interest of supplementing the intervention literature,which has been summarized previously.41

3.Results

3.1.PA,sedentary behaviors,and physical fitness in youth with T1D and T2D

The literature on PA and sedentary behaviors in youth with diabetes is still quite finite.PA research for persons with T1D has been increasing rapidly in the past decade,whereas for persons with T2D it is still extremely limited.In the following section,we summarize the literature with respect to(1)the type of instruments used to assess PA and sedentary behavior, (2)the amount and type of activity and the amount of sedentary behaviors observed in youth with diabetes,(3)how the amounts in youth with T1D and T2D compare to each other and to youth without diabetes,and(4)what is known about fitness levels in youth with diabetes.Table 1 provides a brief summary of all epidemiologic studies on PA,sedentary behaviors,and physical fitness in youth with diabetes that were included in this review.Papers are listed alphabetically by the first author’s last name and the citation number is included as superscripts.

3.1.1.Assessment methods for PA and sedentary behaviors

Table1providesanoverviewofthetypesofinstrumentsused to assess PA and sedentary behavior.46—89About half of the studies published to date have utilized questionnaires (either self-reported by the participants or their parents) with the other half relying on objective measurement of PA.Questionnaire-types ranged from short screener instruments,46,50,54,56,57,60,62,64,67,69to longer structured instruments such as the previous day PA recall(PDPAR),593-day PA recall (3DPAR),58,617-day PA recall,51,52,68the PA questionnaire (PAQ-A),49,53otherstructuredinstruments,48,50,63andtheuseof diaries.65The vast majority of these instruments have been validated,and there were only four studies for which we could notconfirmwhethervalidationhadoccurred.48,63,65,66Objective assessment of PA or physical fitness included using heart rate monitoring,73,74,80,84exercise/fitness testing,70,71,78,88pedometers(also known as step counters),82and accelerometers (activity monitors that measure position and motion).59,85,87One study used Armband technology.53Before considering what is known to date about the amount and type of activity observed in youth with diabetes,it is important to point out that alargeproportionofpublisheddescriptive papershavereliedon sample sizes of less than 100 youth,including(with a few exceptions)46,50,51,54,56—58,60,62—64,67,69,78,80—82the majority of studies that used objective measurements.

In reviewing the literature,one needs to keep in mind that in general,self-report of PA is likely to be overestimated.90,91With this caveat in mind,the following picture emerges on PA (Table 2)and sedentary behavior patterns(Table 3)in youth with diabetes,each of which will be discussed sequentially by type of diabetes.

Table 1 Summary of observational studies on PA,sedentary behavior,or physical fitness in youth with diabetes by instrument type.

Table 1(continued)

Table 1(continued)

Table 1(continued)

3.1.2.PA levels in youth with T1D

Studies using shorter questionnaires or screener items with more global assessments of PA suggest that T1D youth are not entirely inactive,as results range from 22 to 76 min/day of self-reported PA,recognizing that these studies span a variety of settings and age groups.47,48,50,54,56,57,63,66According to the largest study of self-reported PA to date published by Herbst et al.,56,57youth in Germany and Austria reported an average of 1.3 units of 30 min/week of regular PA that was conducted outside of school.About 45%were not physically active at all, 37%engaged in 1—2 units of regular PA per week,and 18%in 3 or more units.

More detailed information can be obtained from studies distinguishing different levels of intensity of activity based on self-report,i.e.,vigorous PA(VPA),moderate PA(MPA),the aggregated category of MVPA(which is particularly important as it links to current guidelines),sedentary behavior(SB),and light PA(LPA).Note that for the sake of comparability across studies,as before,we converted study-specific measurement units to minutes per day.According to studies relying on selfreport,timespentinVPAbyadolescentswithT1D(10yearsand older)ranged from 3 to 57 min/day.58,62Time spent in MVPA rangedfrom65to156min/dayinadolescentboyswithT1Dand from 50 to 156 min/day in adolescent girls with T1D.58,62Monitor-based studies suggest that the lower end of these ranges may be more realistic,with studies ranging from 6 to 25minofVPA74,80,84and46—70min/dayofMVPA.74,80,84,85,87These rather wide ranges are likely due to the wide age range examined in the study populations.For the sake of comparison to a general population of youth,accelerometer data from the 2003—2004 NHANES indicate that during ages 12—15, adolescent boys and girls obtain about 45 and 25 min/day of MVPA,respectively,whereas 16—19 years old boys and girls spend 33and20min/dayofMVPA,respectively.39Most studies suggest that boys with diabetes tend to be more active than girls withdiabetes.46,48,58,62,66,69,74,84OnestudyreportedPAinterms of metabolic equivalents of a task(METs).51,52

In terms of meeting recommendations,we focused on youth reaching at least 60 min of MVPA per day,in line with current recommendations issued in the USA and by the World Health Organization.28,37Data based on 3DPAR suggest that about 81%—82%of youth with T1D achieve 60 min of MVPA per day,58which is likely a substantial overestimate given that the average of pedometer-based steps per day(Girls:6773±2986; Boys:8071±3702)was substantially lower than the recommended levels(e.g.,school-age boys:13,000—15,000,schoolage girls:11,000—12,000,and adolescent boys and girls: 10,000—11,700).82,92Trigona et al.87reported that 35%of youth with T1D spent a minimum of 60 min per day engaged in MVPA.Schweiger et al.67reported an average of 3.1 days for meeting the recommendations,with only 4.7%of youth meeting the recommendation of 60 min of PA each day,and 35%on 5 or more days,but 30%reported only one or no days per week of 60 min of PA.Aman et al.46reported 4.2 days of meeting the 60-min recommendation for boys and 3.6 days for girls with T1D in a typical week.In comparison,accelerometer data from the U.S.national NHANES study suggest that only 11%of boys and 4%of girls aged 12—19 participate in the recommended amount of PA.Accelerometry is currently the gold standard for measurement of PA of all ages.93,94

New measurement tools of PA and energy expenditure are continuously being developed.SenseWear armbands are versatile monitors that allow for convenient collection and analysis regarding PA in the free-living environment.The instrument has shown reasonable concordance with doubly labeled water for measuring daily energy expenditure in freeliving.95A recently published study reported that the amountof PA measured by SenseWear armbands(1.8±0.8 h/day) was higher than that assessed by self-reported questionnaire (0.6±0.3 h/day)among children with T1D.53The SenseWear armband has been validated in children.94

Table 2 Amount and type of PA observed in youth with diabetes.

Table 2(continued)

Table 3 Amount and type of sedentary behavior observed in youth with diabetes.

Comparison of PA levels in youth with and without T1D yielded inconsistent results.In a few studies,including our own,both groups exhibited similar levels of self-reported VPA,MVPA,electronic media and TV use49,50,53,58,61and there were no statistically significant differences in terms of steps per day.82However,other studies have found PA levels of T1D youth to be lower than in controls without diabetes69,87including in two small accelerometer-based studies85,87and one using SenseWear armbands.53One study reported higher activity levels in youth with T1D than in controls.63

3.1.3.PA in youth with T2D

With respect to youth with T2D,very little epidemiologic research has been published.51,52,55,58,61,64,68,82Our own work suggests a very low number of steps per day among girls and boys(4565±3633;6175±2708,respectively).82Self-reported amounts of MVPA observed in youth with T2D range from 7 to 153 min/day in boys and 6—141 min per day in girls.55,58,68Faulkner et al.51,52reported an average of 34 METs per day, while Nadeau et al.61reported a markedly higher average of 64 METs per day in youth with T2D.The proportion of youth withT2Dwhomeetthe60-minMVPAstandardisabout65%for boysand71%forgirlsbasedonself-reportedinformation,58yet theaverageofpedometer-based stepsperdayislessthanhalfof the recommended levels.82,92

Compared to youth without diabetes,T2D youth seem to engage in markedly less PA.58,82In terms of steps per day, O’Neill et al.82suggest a 1500—2000 step difference, depending on gender.The few studies that have compared activity levels between youth with T1D and T2D seem to indicate that activity levels are lower in T2D than in T1D.51,52,58,82This difference may be as large as 2000 steps per day82and more than one metabolic equivalent.51

3.1.4.Sedentary behavior levels in youth with T1D and T2D

Table 3 summarizes data on sedentary behaviors in youth with T1D and T2D.With respect to sedentary behaviors inT1D youth,all studies to date consistently report a large amount of TV watching,ranging approximately between 110 and 140 min/day for adolescent boys and girls alike.46,47,50,58,60,62Time spent on computer use by youth with T1D ranges from 40 min to 255 min/day.47,62Total time spent on electronic media use and computer use,however,seems greater for boys than for girls,similar to that reported in youth without diabetes39(90vs.72 min daily of weekday computer use46;105vs.59 min daily average computer use62;207vs.147 min daily average electronic media).58Total media use was estimated by Galler et al.54at 174 min/day.Weekend use of TV and electronic media was greater than weekday use.46With respect to recommendations pertaining to TV watching,recent data by Overby et al.62from Norway,Benevento et al.47and Galler et al.54from Germany,Rothman et al.64and Lobelo et al.58from the USA58suggest that T1D youth markedly exceed the recommendation of≤2 h of TV per day, whereas an international study by Aman et al.46reported TV on weekday markedly below the recommendation.

Electronic media use in T2D youth seems to be very high with on average 3.6 h for boys and 2.9 h/day for girls,of which the majority is spent watching TV.58Rothman et al.64reported that only 32%of their population watched one hour of TV or less per day,while the remained watched 2 or more hours. Compared to youth without diabetes,96,97youth with T2D seem to engage in markedly more sedentary behaviors.58,82

3.1.5.Physical fitness in youth with T1D and T2D

A noteworthy number of studies also shed light on physical fitness levels in youth with T1D and T2D(Table 4).Physical fitness can be categorized as cardiorespiratory fitness, muscular strength,flexibility,or balance.For this review, physical fitness is defined as cardiorespiratory fitness(as determined by maximal oxygen consumption(VO2max)or peak oxygen consumption(VO2peak)depending on the study criteria),or power output during a standardized heart rate (PWC170).98Four studies to date report very consistent fitness levels of VO2peakof about 34—41 mL/kg/min in youth with T1D,which is considered in the low cardiorespiratory fitness range for youth51,52,70,71,99Fitness levels in youth with T2D arelowerthan in T1D youth (atabout25 mL/kg/ min).61,68,75,89This study also compared VO2peakand peak work rate for T2D youth compared to control youth and found markedly lower levels of fitness in T2D youth.61In comparison,for cardiorespiratory fitness levels in youth,data from NHANES 1999—2002 indicate that 12—19 years old boys have an estimated VO2maxrange of 44.6—47.6 mL/kg/min, while 12—19 years old girls have an estimated VO2maxrange of 39.7—39.5 mL/kg/min,and that approximately 65%of 12—19 years old boys and girls meet criterion-referenced standards(FITNESSGRAM?)that are linked to health outcomes.100

Another measure of cardiorespiratory fitness,the physical working capacity(PWC170)test,is a cycle ergometer test that predicts the power output(watts)at a projected heart rate of 170 beats per minute(bpm).This test is standardized to determine physical fitness98and has been used to some success to track physical fitness from youth to adulthood.101Heyman et al.76,77found that 13—18 years old girls with diabetes had a PWC170ranging from 1.66 to 2.28 w/kg.

3.2.Fear of hypoglycemia as a specific barrier to PA in youth with diabetes

While there are many barriers to PA behaviors in general, fear of hypoglycemia is an important additional and highly prevalent concern for persons with diabetes,as evidenced by several extensive reviews.42—44The Hypoglycemia Fear Survey is one of the most common instruments used to assess this issue.42,102As reviewed by Barnard et al.,42hypoglycemia avoidance behaviors by parents of youth with T1D typically include having fast-acting sugars on hand and frequent feedings.103

Two recent studies have also shown that fear of hypoglycemia is a concrete barrier to PA in adults and children.104,105The Barriers to PA in Diabetes Questionnaire(BAPAD-1)was developed and validated by Dube et al.105in youth and young adults with T1D,ages 11—20,with frequency of hypoglycemia ranging from 0 to 12%and HbA1clevels ranging from 7.2%to10%.Constructs include perceived fears related to diabetes,physical abilities,time constraints,and environment. Participants indicate the degree of likelihood that an issue will keep them from participating in regular PA.The BAPAD-1 has been shown to have very good psychometric properties and test—retest reliability.105Furthermore,a recent study has shown that the BAPAD-1 has good predictive validity when evaluated against accelerometer in persons with T1D.106

None of the 44 studies meeting the criteria of this review reported any data on fear of hypoglycemia.Thus,to date,there seems to be a lack of large,representative studies of T1D youth that have addressed the relation between fear of hypoglycemia and specific types of PA,including using self-reported information on the types of activity and objective information on the amount and intensity of activity,at least within the studies abstracted in PubMed.

3.3.Health benefits of PA in youth with diabetes

A comprehensive review of published intervention research focusing on the health benefits of PA in youth with T1D was recentlypublishedbyChimenetal.41Theauthorsconcludedthat PA(1)“…improves insulin requirements in type 1 diabetes but shows a limited effect on glycemic control”,(2)“…improves lipid levels,endothelial function and insulin resistance but not bloodpressure,”and(3)“…isassociatedwithreducedCVDand mortality in patients with type 1 diabetes”.In this section of the review,we provide a brief overview of the current epidemiological studies which addressed these three groups of research questions(Table 5)in free-living populations.

With respect to insulin requirements and glycemic control in T1D youth,there is clearly a continuing need to identify ways to improve glycemic control in youth as various studies, including clinical trials,have shown that intensive glycemic control prevents or delays the progression of microvascularcomplications of diabetes and the risk of macrovascular disease.107—109The SEARCH study has shown that 17%of T1D youth and 27%of T2D youth110had poor glycemic control (HbA1c≥ 9.5%),consistent with several others.111,112As summarized by Chimen et al.41PA does seem to impact on glycemic control in intervention studies.Additionally,there are a number of observational studies that are consistent with this conclusion.46,48,65,69,80For example,Schweiger et al.67demonstrated that self-reported MVPA of at least 60 min on 3 days/week in T1D youth was significantly associated with good glycemic control.Galler et al.54reported that among youth with T1D,those who spent 3.9 or more hours per day utilizing media(i.e.,TVor computer)had higher HbA1clevels. The Hvidoere Study Group reported an association of computer time with increased HbA1clevels but no association with PA.46Lastly,in a large,multi-center practice-based study, Herbst et al.57found that self-reported PA of 30 min once a week was associated with good glycemic control in T1D youth.However,there are also a number of observational studies that did not find a significant impact of PA onHbA1clevels or glycemic control.50,51,73,74,85

Table 4 Physical fitness in youth with diabetes.

With respect to CVD risk factors such as lipid levels, insulin resistance,and blood pressure,there are several epidemiologic studies which are consistent with the positive findings in the review.41Concretely,Herbst et al.56observed associations with dyslipidemias,triglycerides,total,LDL and HDL cholesterol and blood pressure.Valerio et al.69reported associations with triglycerides and metabolic control,but a study by Faulkner51did not support associations with a variety lipid levels.

Non-invasive techniques now exist to evaluate cardiovascular function well before diabetes-related vascular disease becomes irreversible.113—118Pulse wave velocity(PWV)and augmentation index(AIx),both measures of arterial stiffness, are associated with CVD risk factors including in T1D.119—123In fact,PWV has been shown to predict mortality in T1D independently of traditional CVD risk factors and glycemic control.120Cardiac autonomic neuropathy is another common chronic complication of diabetes,commonly assessed by heart rate variability(HRV).Low HRV is associated with hyperglycemia,recurrent hypoglycemia,increased arterial stiffness and a significantly increased mortality,independent of other risk factors.124—127Moreover,cardiac autonomic neuropathy has been shown to be prevalent in newly-diagnosed T1D patients,including youth.128—131Thus,evidence suggests that youth with diabetes are at a critical juncture of theircardiovascular health,at which irreversible changes can likely be prevented.

Table 5 Effect of PA and sedentary behaviors on health outcomes among youth with diabetes.

The association of PA and CVD risk in T1D youth may resemble the association in youth without T1D,132but to the best of our knowledge very few studies have examined this relationship.The literature on PA and measures of arterial stiffness is entirely limited to T2D and suggests a strong health-promoting effectofPA on arterialstiffnessin adults133—135and youth.136,137With respect to cardiac autonomic function,habitual PA increases HRV.138Two studies have shown positive associations of PA with HRV in youth with T1D49,51and T2D.51There is also evidence for youth without diabetes.139—142Gutin et al.140,141demonstrated that 4 months of aerobic exercise training and games designed to maintain a heart rate＞150 beats/min improved HRV in obese youth.Buchheit et al.139observed that preadolescent youth have enhanced HRV indexes with VPA(measured by accelerometery),but not with MPA,suggesting that more intense activities may be necessary to observe more favorable HRV in young people.In summary,only very limited data exist on the relationship of PA to cardiovascular function in youth with T1D and T2D.

With respect to studies of physical fitness on health outcomes in youth with diabetes(Table 6),the literature suggests inverse associations between fitness levels and glycemic control and lipid levels in youth with T1D,although results are not entirely consistent.61,70,71,81,89In youth with T2D,only two studies were found with conflicting results with respect to glycemic control51,61and two with somewhat confliction results with respect to lipid levels.51,89

Finally,it isimportant toconsider hypoglycemia,notonlyas a barrier to PA as reviewed above,but also as a potentially dangerous consequence of PA in persons with T1D.The literature on the relation of PA to hypoglycemia is inconsistent.The DirecNetStudyGroupreportedresultsofaprolongedmoderate aerobic exercise intervention in 50 T1D youth which suggested that hypoglycemia is common(86%)if pre-exercise glucose levels are below 120 mg/dL.143Furthermore,nighttime hypoglycemia alsowas more common following afternoon exercise. In contrast,the two large epidemiologic studies did not find anassociation of PAwith risk of hypoglycemia,46,57but both were based on self-reported data.Thus,more research is needed assessingthe real-life PApatterns objectively,paired withstateof-the art measure of glucose levels,to better understand the relationship between PA and hypoglycemia and how to avoid hypoglycemia so that youth with T1D can benefit from the positive effects of PA on health.Another related issue is that of consumption of food and specifically carbohydrates prior to, during,or after PA to prevent hypoglycemia which may be potentially offsetting some of the benefits of PA on healthy weight maintenance.

Table 6 Effect of physical fitness on health outcomes among youth with diabetes.

4.Conclusion

In summary,the epidemiologic evidence on the health benefits of PA and physical fitness,as well as the detrimental influence of sedentary behavior is generally quite consistent with that of intervention studies recently reviewed by Chimen et al.41With respect to the influence of PA on hypoglycemia, there is clearly more need for research,especially in real-life settings,as the current literature is quite inconsistent.Fear of hypoglycemia is likely an important barrier to PA in youth with T1D,and more research is needed on how to address this barrier.Furthermore,epidemiologic data to date suggest that a large proportion of youth with diabetes do not engage in sufficient amounts and intensities of PA to meet current recommendations of 60 min of MVPA per day and that a large proportion of youth with diabetes watch excessive amounts of TV.Fitness levels of youth with diabetes seem to be in the low range,with youth with T2 having poorer fitness levels than youth with T1D.Furthermore,there is an absence of large, representative studies using state-of-the-art objective assessment instruments such as accelerometers or other technologies in populations of youth with T1D or T2D.Very few studies have had sufficient sample sizes to describe activity levels by race or ethnic characteristics and these suggest that activity levels may be markedly lower in minority populations.67,82There are virtually no data on what types of activities youth with diabetes engage in,and if those differ from youth without diabetes.48,50,69What is also not known is if youth with diabetes experience an age-related decline in activity levels that exceeds that observed in youth without diabetes.39,66Given that diabetes is one of the most common chronic conditions in youth,there is clearly a need for research addressing the aforementioned gaps in knowledge.A detailed description of prevailing PA and sedentary behavior amounts and patterns, using state-of-the-art objective and self-reported assessment instruments can provide the basis for much needed public health and clinical intervention efforts targeted at improving the health of this vulnerable population.

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Received 27 June 2012;revised 15 September 2012;accepted 16 October 2012

*Corresponding author.

E-mail address:liese@sc.edu(A.D.Liese)

Peer review under responsibility of Shanghai University of Sport

2095-2546/$-see front matter Copyright?2012,Shanghai University of Sport.Production and hosting by Elsevier B.V.All rights reserved. http://dx.doi.org/10.1016/j.jshs.2012.10.005