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REVIEW

The Effect of Aerobic and Resistance Training and Combined Exercise Modalities on Subcutaneous Abdominal Fat: A Systematic Review and

Meta-analysis of Randomized Clinical Trials

Habib Yarizadeh,1,2Reza Eftekhar,2Javad Anjom-Shoae,2John R Speakman,3,4and Kurosh Djafarian5

1Students’ Scientific Center, Tehran University of Medical Sciences, Tehran, Iran;2Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran;3School of Biological Sciences, University of Aberdeen, Aberdeen, United Kingdom;4State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China; and5Clinical Nutrition Department, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran

ABSTRACT

Subcutaneous abdominal adipose tissue (SAT), is the largest fat depot and major provider of free fatty acids to the liver. Abdominal fat is indirectly (via increased levels of low-grade inflammation) correlated with many of the adverse health effects of obesity. Although exercise is one of the most prominent components of obesity management, its effects on SAT are still unclear. The aim of this study was to investigate the independent effects of aerobic training (AT) and resistance training (RT) modalities and combined exercise modalities on SAT in adults. PubMed, SCOPUS, and Google Scholar were searched to find relevant publications up to November 2018. The effect sizes were represented as weighted mean difference (WMD) and 95% CIs. Between-study heterogeneity was examined using theI2test. Overall, 43 identified trials that enrolled 3552 subjects (2684 women) were included. After removal of outliers, combining effect sizes indicated a significant effect of AT (WMD:13.05 cm2; 95% CI:18.52,7.57;P<

0.001), RT (WMD:5.39 cm2; 95% CI:9.66,1.12;P=0.01), and combined exercise training (CExT; WMD:28.82 cm2; 95% CI:30.83,26.81;P<

0.001) on SAT relative to control groups. Pooled effect sizes demonstrated a significant effect of AT on SAT compared with a CExT group (WMD: 11.07 cm2; 95% CI: 1.81, 20.33;P=0.01). However, when comparing the AT and RT groups, no significant difference was seen in SAT (WMD:0.73 cm2; 95% CI:4.50, 3.04;P=0.70). Meta-analysis of relevant trials indicated that AT, RT, and CExT lead to SAT reduction. Aerobic exercise was shown to produce greater efficacy in decreasing SAT. Adv Nutr2021;12:179–196.

Keywords: aerobic exercise, resistance training, combined exercise, subcutaneous abdominal fat, and meta-analysis

Introduction

The prevalence of obesity and chronic disease has been increasing at an alarming rate (1). It is now widely recognized that increased deposition of abdominal fat has been impli- cated as a key etiology in the development and progression of various chronic conditions such as obesity, diabetes, cardiovascular diseases, and some cancers (2). Abdominal fat has been suggested to be associated with these chronic diseases through the release of cytokines and bioactive

The authors reported no funding received for this study.

Author disclosures: The authors report no conflicts of interest.

Address correspondence to KD (e-mail:[email protected]).

Abbreviations used: AT, aerobic training; CExT, combined exercise training; HR, heart rate; HRR, heart rate reserve; MeSH, medical subject heading; RT, resistance training; SAT, subcutaneous abdominal adipose tissue; WMD, weighted mean difference; VAT, visceral adipose tissue;

VO2max, maximum oxygen consumption; 1-RM, 1-repetition maximum.

mediators (3). Although persons with abdominal obesity appear to develop metabolic syndrome more frequently than individuals with peripheral body fat distribution, the site of abdominal fat accumulation (subcutaneous compared with visceral) is potentially important and still a matter of debate (4–6). Over recent years, most attention has focused on visceral adipose tissue (VAT) (7); however, it should be kept in mind that subcutaneous abdominal adipose tissue (SAT) accounts for ∼80% of abdominal fat and is the major provider of free fatty acids to the liver (8, 9).

In a meta-analysis that included 89 studies, the effect of different exercise on visceral and subcutaneous fat loss was investigated. Based on the included studies, it indicated a greater decrease in SAT compared with VAT (7) across all of the strategies (10). Currently, in addition to exercising,

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other approaches for the removal of these tissues, including bariatric or liposuction surgeries, have attracted more and more people. In addition, nowadays, more individuals are using the aggressive method for the removal of these tissues, the cost-benefit consequences of which are really prominent in terms of economic aspects, although their effect on human life is still unclear (11, 12). Also, reduction in body fat through aggressive procedures (liposuction) had no effect on improving metabolic parameters (13).

Many other methods to prevent obesity such as dietary interventions have been investigated over the past decades as well (14). It is now well known that a minimal loss of 5–10% of the initial body weight (especially abdominal fat) is effective in improving risk profiles of diseases related to obesity (15,16). However, a 20% reduction in body fat (or 40% of subcutaneous fat) through an aggressive pro- cedure (liposuction) had no effect on improving metabolic parameters. This can be due to specific differences between visceral and subcutaneous fat or a fundamental problem of energy imbalance (13,17). Along with dietary modifications, exercise seems to be another important and central compo- nent of weight-loss programs. Exercise-induced weight-loss interventions can affect the amount of abdominal fat and thereby prevent the onset of chronic diseases. Also, despite effects on body fat, regular exercise has many health benefits, including reduced blood pressure and blood lipids, improved diabetes, and other metabolic health outcomes independent of body fat loss (18–21). In the past years, a great deal of attention has been focused on the impact of aerobic exercise with or without caloric restriction in subjects with obesity (16, 19, 20, 22, 23). On the other hand, there has been considerable recent interest regarding the effects of resistance exercise on metabolic profile and weight loss in individuals with obesity (23–26). Although many studies compared the effect of resistance exercise and aerobic exercise on abdominal fat (24,27,28), it is still not clear which of these exercise modalities is better for the reduction of SAT (27,29).

Thus, our main objective in this study was to systematically review the present evidence on the effects of aerobic exercise (aerobic training; AT), resistance training (RT), and a combination of these modalities (combined exercise training;

CExT) on SAT reduction, and to summarize the available findings in a meta-analysis.

Methods

This study was carried out based on the guidelines of the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analysis) statement.

Search strategy

We performed a literature search using the online databases of Medline (PubMed) and Scopus for relevant publications up to November 2018. To find relevant publications, the following medical subject headings (MeSH) and non-MeSH keywords were searched by 2 independent investigators (HY and KD) as follows: (Subcutaneous Fat, Subcutaneous

Adipose Tissue, Abdominal Subcutaneous Fats, Adipose Tis- sue, Abdominal Subcutaneous, Abdominal Fat, Abdominal Adipose Tissue) and (Exercise, Physical Activity, Physical Ex- ercise, Acute Exercise, Aerobic Exercise, endurance training, cardio training or Exercise Tolerance, Resistance Training, Strength Training, Weight-Lifting Strengthening Program, progressive training, weight training). We also searched systematic reviews from the above-mentioned databases and hand checked reference lists to identify studies that might have been missed. Unpublished studies were excluded, as well as duplicate citations.

Selection of studies

After removal of duplications, the search results were evaluated by 1 investigator (HY). Then, retained studies were retrieved and reviewed by 2 investigators. Any disagreement between the 2 researchers was resolved by discussion or by a third person (30).

Inclusion and exclusion criteria for studies

In our meta-analysis, eligible publications were included based on the following criteria:1) all studies assessing the effects of exercise on abdominal fat area;2) studies that used a randomized controlled clinical trial design;3) those studies that only investigated the effect of intervention on abdominal fat area (cm2) but not other indicators of fat tissue, such as its volume (cm3), thickness (31), and weight (kg);4) computed tomography (CT) or MRI was used for quantification of SAT;

5) human studies with a minimum follow-up period of 4 wk;

and6) manuscripts published in the English language.

Studies that met the following criteria were excluded:1) participants<18 y,2) non–original research (letters, review articles, and meta-analysis),3) not enough information was available, 4) studies on specific diseases (e.g., spinal cord injury and AIDS), and 5) the other methods used for quantification of SAT (such as ultrasound or DXA).

Data extraction

The following data of interest from each individual study were extracted: first author, year of publication, study population, sample size, age, sex, weight, and BMI (Table 1);

exercise details (nutritional intervention, exercise frequency, intensity, session duration and intervention duration) and subcutaneous fat quantification (type of measurement tech- nique and region) (Table 2). For 3 studies that presented data graphically, means and SDs were extracted using the GetData Graph Digitizer 2.24 (Fedorov 2008).

Assessment of study quality

Study quality was assessed by a modified Jadad scale, in which the total score ranges from 0 to 5 points based on the following criteria:1) randomization present,2) method of randomization,3) double blinding performed,4) method of double blinding, and5) reports of dropouts and withdrawals.

In the current study, trials scored 1 point for each area addressed in the study design with a possible score of 0 to 3 (highest level of quality). In exercise studies, it is impossible

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TABLE1SummarydemographiccharacteristicsofthestudiesexaminingtheeffectsofAT,RT,andCExTmodalitiesonsubcutaneousabdominalfat1 Firstauthor(reference);yearStudypopulation%Male%FemaleSamplesize, nMeanage, yMeanBMI, kg/m2Meanweight, kg Bacchietal.(27);2013Sedentarysubjectswithtype2diabetesAT:71 RT:70AT:29 RT:30AT:14 RT:17AT:55.6 RT:56AT:30.5 RT:28.8NR Binderetal.(32);2005Oldersedentarywithphysicalfrailty0100C:38 RT:53C:83 RT:83C:26 RT:27C:71 RT:77 Boudouetal.(33);2003Middle-agedmenwithtype2diabetes1000C:8 AT:8C:47.9 AT:42.9C:30.85 AT:28.3C:86.9 AT:90.4 Brochuetal.(34);2009Postmenopausalwomen0100C:71 RT:36C:58 RT:57.2C:32.2 RT:32.6C:83.6 RT:84.1 Brownetal.(35);2016Womenwithhighriskforbreastcancer3961C:13 AT:14NRC:29.2 AT:29.5C:83.7 AT:86.2 Brownetal.(35);2016Womenwithhighriskforbreastcancer3961C:13 AT:12NRC:29.2 AT:32.5C:83.7 AT:92.2 Carretal.(36);2005SubjectswithimpairedglucosetoleranceC:17 AT:12C:83 AT:88C:32 AT:30C:57.2 AT:55.7C:26.6 AT:25.7C:69.7 AT:66.5 Choietal.(37);2012Koreanwomen0100C:15 AT:15C:45.4 AT:45.4C:26.1 AT:25.6C:63 AT:64.4 Choietal.(37);2012Koreanwomen0100C:15 AT:15C:45.4 AT:45.4C:26.1 AT:25.1C:63 AT:63.2 Choietal.(37);2012Patientswithtype2diabetes0100C:37 AT:38C:55 AT:53.8C:26.8 AT:26.8C:64.9 AT:64.6 Christiansenetal.(38);2009Obesemenandwomen5050C:19 AT:21C:35.6 AT:37.5C:35.3 AT:34.2C:107.8 AT:105.8 Cuetal.(23);2003Obesepostmenopausalwomenwithtype2 diabetes0100C:9 CExT:10 AT:9 C:60 CExT:63.4 AT:59.4 C:36.7 CExT:33.3 AT:32.5

C:95.6 CExT:89.5 AT:81.2 DiPietroetal.(39);1998HealthyoldermenandwomenNRNRC:7 AT:9C:73 AT:72C:26.8 AT:27.5C:69 AT:65 Donnellyetal.(40);2003Sedentaryoverweightandmoderately obese0100C:18 AT:25C:21 AT:24C:29.3 AT:28.7C:79.9 AT:77 Donnellyetal.(40);2003Sedentaryoverweightandmoderately obese1000C:15 AT:16C:24 AT:22C:29 AT:29.7C:94.1 AT:94 Drapeauetal.(41);2011Overweightandobesepostmenopausal women0100C:22 RT:24C:58.5 RT:58C:32.1 RT:32.9C:82.5 RT:84.4 Fisheretal.(29);2011Healthypremenopausalwomen0100C:29 AT:43 RT:54

NRC:28 AT:28 RT:28

C:78 AT:77 RT:78 (Continued)

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TABLE1(Continued) Firstauthor(reference);yearStudypopulation%Male%FemaleSamplesize, nMeanage, yMeanBMI, kg/m2Meanweight, kg Fisheretal.(29);2011Healthypremenopausalwomen0100C:24 AT:32 RT:41

NRC:28 AT:28 RT:28

C:79 AT:75 RT:78 Friedenreichetal.(42);2011Normal-weighttoobesepostmenopausal women0100C:160 AT:160C:60.6 AT:61.2C:29.2 AT:29.1C:76.3 AT:75.6 García-Uncitietal.(43);2012Obesewomen0100C:9 RT:13C:50.2 RT:48.6C:35 RT:35C:88.9 RT:90.2 Haysetal.(44);2006Oldermenandwomen4060C:11 AT:11C:67.5 AT:64.8C:31 AT:30.8C:89.6 AT:82.9 Henríquezetal.(45);2017Sedentarywomen0100AT:18 RT:16AT:58 RT:55AT:30.6 RT:30.8AT:75 RT:77.1 Houghtonetal.(46);2017PatientswithsedentarylifestylesandNASH (nonalcoholicsteatohepatitis)NRNRC:12 CExT:12C:51 CExT:54C:33 CExT:33C:94 CExT:90 Houghtonetal.(46);2017Patientswhowereoverweightorobese andconsumingalcoholNRNRC:14 CExT:13C:56 CExT:51C:31 CExT:33NR Hunteretal.(47);2010Healthypremenopausalwomen0100C:30 AT:18 RT:21

C:34.8 AT:34.7 RT:34.1 C:23.9 AT:23.5 RT:23.9

C:65 AT:62.8 RT:66 Ibáñezetal.(48);2010Obesewomen0100C:12 RT:13C:51.4 RT:48.6C:34.6 RT:35C:88 RT:90.2 Irvingetal.(72);2008Obesewomen0100C:7 AT:11C:51 AT:51C:32.7 AT:34.7C:89.6 AT:97.2 Irvingetal.(72);2008Obesewomen0100C:7 AT:9C:51 AT:51C:32.7 AT:34.7C:89.6 AT:93.5 Irvingetal.(49);2009ObeseadultswiththemetabolicsyndromeC:40 AT:24C:60 AT:76C:10 AT:13C:49.2 AT:49.2C:32 AT:35.5C:95.9 AT:101.7 Irvingetal.(49);2009ObeseadultswiththemetabolicsyndromeC:40 AT:28C:60 AT:72C:10 AT:11C:49.2 AT:49C:32 AT:34.2C:95.9 AT:97.7 Irwinetal.(50);2003Overweightpostmenopausalwomen0100C:86 CExT:87C:60.6 CExT:61C:30.6 CExT:30.5C:81.7 CExT:81.6 Janssenetal.(51);2002Obesepremenopausalwomen0100C:13 AT:11 RT:14

C:40.1 AT:37.5 RT:34.8 C:33.7 AT:36 RT:31.6 C:90.8 AT:99.9 RT:86.1 JanssenandRoss(52);1999Upper-body-obesemen1000C:10 AT:10 RT:10

C:45.6 AT:47.4 RT:37.9 C:31.6 AT:33 RT:33.6 C:98.1 AT:101.9 RT:109.1 JanssenandRoss(52);1999Upper-body-obesewomen0100C:10 AT:10 RT:10

C:39.6 AT:39 RT:37.3 C:34.5 AT:35.5 RT:32.5

C:92.9 AT:98.3 RT:87.2 Johnsonetal.(53);2009ObesesedentaryNRNRC:7 AT:12C:47.3 AT:49.1C:31.1 AT:32.2C:98.8 AT:94.4 (Continued)

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TABLE1(Continued) Firstauthor(reference);yearStudypopulation%Male%FemaleSamplesize, nMeanage, yMeanBMI, kg/m2Meanweight, kg Kimetal.(73);2008Womenwithmetabolicsyndrome0100C:10 CExT:10NRC:25.7 CExT:26.1C:58.33 CExT:58.13 Kooetal.(54);2010Womenwithtype2diabetes0100C:18 AT:13C:57 AT:59C:28.5 AT:25.5C:66 AT:64 Kooetal.(54);2010Womenwithtype2diabetes0100C:19 AT:14C:57 AT:53C:27.1 AT:29.4C:67.4 AT:69.4 Leeetal.(55);2012Overweightorobesepremenopausal women0100C:7 AT:8C:38.3 AT:41.6C:27.3 AT:27.4C:70.3 AT:67.3 Leeetal.(55);2012Overweightorobesepremenopausal women0100C:7 AT:7C:38.3 AT:41.7C:27.3 AT:25.4C:70.3 AT:65.2 McTiernanetal.(56);2007Sedentary0100C:51 AT:49C:53.7 AT:54.4C:28.5 AT:28.9C:77.9 AT:78 McTiernanetal.(56);2007Sedentary1000C:51 AT:51C:56.6 AT:56.2C:30.1 AT:29.7C:97.4 AT:94.8 Moghadasietal.(57);2012Sedentaryoverweightandobesemen1000C:8 AT:8C:41.18 AT:41.18C:32.03 AT:32.08C:90.47 AT:87.86 Mourieretal.(58);1997Non–insulin-dependentdiabetes(NIDDM)NRNRC:11 AT:10C:46 AT:45C:30.1 AT:30.4C:84.4 AT:85.3 Poehlmanetal.(28);2000Premenopausalwomen0100C:20 AT:14 RT:17

C:28 AT:29 RT:28

C:22 AT:22 RT:22

C:60 AT:59 RT:58 Ryanetal.(59);2011Patientswithimpairedglucosetolerance andobesepostmenopausalwomen0100C:17 AT:16C:65 AT:62C:32.7 AT:34.8C:84.4 AT:91.4 Ryanetal.(59);2011Obesepostmenopausalwomen0100C:29 AT:33C:60 AT:59C:32.8 AT:30.6C:88.3 AT:81.4 Schmitzetal.(60);2007Overweightandobesewomen0100C:67 RT:71C:36 RT:36C:29.4 RT:29.4C:80.7 RT:81.6 Schmitzetal.(60);2007Overweightandobesewomen0100C:63 RT:70C:36 RT:36C:29.4 RT:29.4C:80.7 RT:81.6 Shojaee-Moradieetal.(61);2007Sedentaryhealthymen1000C:7 AT:10C:55 AT:47C:27.6 AT:27.6C:84.1 AT:87.4 Sigaletal.(31);2007Adultswithtype2diabetesC:65 CExT:62 AT:65 RT:62

C:35 CExT:38 AT:35 RT:38

C:63 CExT:64 AT:60 RT:63

C:54.8 CExT:53.5 AT:53.9 RT:54.7

C:35 CExT:35 AT:35.6 RT:34.1

C:101.3 CExT:101.9 AT:103.5 RT:99.1 Slentzetal.(62);2011SedentarymenandwomenCExT:43 AT:45 RT:42

CExT:57 AT:55 RT:58

CExT:44 AT:48 RT:52

CExT:46.9 AT:49.5 RT:49.7 CExT:30.7 AT:30.4 RT:30.5

CExT:90.4 AT:88.5 RT:88.6 (Continued)

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TABLE1(Continued) Firstauthor(reference);yearStudypopulation%Male%FemaleSamplesize, nMeanage, yMeanBMI, kg/m2Meanweight, kg Slentzetal.(63);2005Overweightormildlyobesewithmoderate lipidabnormalitiesC:49 AT:55C:51 AT:45C:47 AT:40C:52.3 AT:54C:29.8 AT:29.8NR Slentzetal.(63);2005Overweightormildlyobesewithmoderate lipidabnormalitiesC:49 AT:50C:51 AT:50C:47 AT:46C:52.3 AT:53C:29.8 AT:29.7NR Slentzetal.(63);2005Overweightormildlyobesewithmoderate lipidabnormalitiesC:49 AT:54C:51 AT:46C:47 AT:42C:52.3 AT:51.5C:29.8 AT:29.1NR Sunetal.(64);2018Healthyelderlymen1000C:10 AT:10C:69 AT:72C:22.6 AT:22.7C:61.6 AT:62.8 Zhangetal.(65);2017Obeseyoungwomen0100C:13 AT:15C:20.8 AT:20.9NRC:67.5 AT:68.5 Zhangetal.(65);2017Obeseyoungwomen0100C:13 AT:15C:20.8 AT:21.5NRC:67.5 AT:67.3 1Alldataarereportedasmeans.AT,aerobictraining;C,controls;CExT,combinedexercisetraining;NR,notreported;RT,resistancetraining.

to blind the people to the intervention. As a result, scores of 5 are impossible to achieve, hence we defined high- quality publications as those that had a Jadad score of ≥3 (Table 2).

Data synthesis and statistical analysis

This analysis was conducted using Stata software version 14 (StataCorp LP). Random- and fixed-effects models were utilized to obtain pooled estimates of training impacts on SAT, using weighted mean difference (WMD). Studies that reported ≥2 interventions of different exercise intensity were entered as separate studies. Also, studies that reported separate results for male and female subjects were also entered separately. We performed 5 analyses to compare the effect of1) AT compared with control,2) RT compared with control, 3) CExT compared with control,4) AT compared with RT, and5) CExT compared with AT on SAT change. The mean change (66) in SAT from baseline was used to calculate the mean difference (with 95% CI) between the intervention and control groups. Some studies provided an SEM from which we calculated the SD (66) according to the formula (SD =SEM× square root of N). Then we calculated the SD of the mean difference as follows: SD change=square root [(SDbaseline2 +SDfinal2)−(2×R×SD baseline× SD final)]. The SD of mean differences was calculated using a correlation coefficient “R” of 0.9 (67). When the publications revealed medians and ranges or 95% CIs, the mean (66) was calculated by the method of Hozo et al. (68). The between- trial WMD and 95% CI were calculated. Between-study heterogeneity was examined using the I2test. To assess the influence of each study on the overall mean difference, we used a sensitivity analysis by the jack-knife approach, which involves systematically removing and replacing each study.

Publication bias was assessed by visual evaluation of the funnel plot and Egger’s test.Pvalues<0.05 were considered significant.

Results

Included studies

A total of 7250 studies were identified through the PubMed and Scopus databases, and after removal of duplicates a total of 6997 studies remained. Furthermore, we found 4 more studies from the reference lists of the manuscripts retrieved.

After elimination of articles based on the eligibility criteria, 43 articles remained (Figure 1).

Study characteristics

A total of 3552 individuals (with a mean age range of 20.8–

83 y) had been enrolled in the trials, which included 761 men and 2684 women and gender was not reported for 107 subjects. Of the 59 studies (43 articles) in the meta- analysis, 33 studies were exclusively conducted in women, 7 studies were exclusively conducted in men, and 14 studies were conducted in both men and women, whereas sex was not reported in 5 studies. The mean BMI (kg/m2)

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TABLE2SummaryexercisedetailsofthestudiesexaminingtheeffectsofAT,RT,andCExTmodalitiesonsubcutaneousabdominalfat1 Firstauthor(reference); yearNutritionalintervention2(%)Weight change,kgIntensityFrequency, d/wkSession durationIntervention durationMeasureRegionJadad score Bacchietal.(27);2013Accordingtostandard recommendationsforpeoplewith type2diabetes

NRAT:60–65%HRR RT:70–80%1-RM360min17wkCTL4-L55 Binderetal.(32);2005SupplementalcalciumandvitaminDC:0.0 RT:0.0RT:65–100%1-RM2–360–90min26wkMRIL4-L55 Boudouetal.(33);2003Notchangetheirdiet (50%CHO,30%fat,20%PRO)C:-1.65 AT:-1.9AT:50–85%VO2peak1–2C:20min AT:45min8wkMRIL4-L52 Brochuetal.(34);2009Reducetheircaloricintakeby500–800 kthcal/d (55%CHO;30%fat;15%PRO)

C:-5.1 RT:-5.8RT:65–80%1RM3NR26wkCTL4-L53 Brownetal.(35);2016NotchangetheirdietC:1.04 AT:-0.49AT:50–70%maxHRNR150min/wk26wkCTWholebody5 Brownetal.(35);2016NotchangetheirdietC:10.4 AT:-0.31AT:50–70%maxHRNR300min/wk26wkCTWholebody5 Carretal.(36);2005AHAisocaloricdiet (30%fat,7%SFA,200mg cholesterol,55%CHO,15%PRO) C:-0.9 AT:-3AT:70%HRR360min104wkCTUmbilical3 Carretal.(36);2005AHAisocaloricdiet (30%fat,7%SFA,200mg cholesterol,55%CHO,15%PRO)

C:0.6 AT:-1.8AT:maximal

˙ VO

2max360min26wkCTUmbilical3 Choietal.(37);2012Notchangetheirdiet (70%CHO,12%fat,18%PRO)C:1.5 AT:-2.1AT:40–50%of VO2max3Expended 300–400 kcal/session

12wkCTL4-L55 Choietal.(37);2012Notchangetheirdiet (70%CHO,12%fat,18%PRO)C:1.5 AT:-2.8AT:70–75%VO2max3400kcal/d12wkCTL4-L55 Choietal.(37);2012NotchangetheirdietC:-1 AT:-1NR560min12wkCTNR5 Christiansenetal.(38);2009Reducetheircaloricintakeby600and 800kcal/d(55%CHO,30%fat,15% PRO)

C:-12.3 AT:-12.3AT:70%HRR360–75min12wkMRIL5-L43 Cuetal.(23);2003NotchangetheirdietC:2 CExT:-2.9 AT:-1.2

AT:60–75%HRR RT:121-RM375min16wkCTL4-L52 DiPietroetal.(39);1998NRC:0 AT:-1AT:55–75%HRmax460min13wkCTL4-L52 Donnellyetal.(40);2003NotchangetheirdietC:-0.5 AT:-5.2AT:60–75%HRRNR20–45min26wkCTL4-L54 Donnellyetal.(40);2003NotchangetheirdietC:2.9 AT:0.6AT:60–75%HRRNR20–45min26wkCTL4-L53 (Continued)

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