the effects of exercise training on fat-mass loss in obese patients during energy intake restriction

16
Sports Med 2007; 37 (1): 31-46 REVIEW ARTICLE 0112-1642/07/0001-0031/$44.95/0 © 2007 Adis Data Information BV. All rights reserved. The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction Dominique Hansen, 1,2 Paul Dendale, 2 Jan Berger, 2 Luc J.C. van Loon 3 and Romain Meeusen 1 1 Human Physiology and Sports Medicine, Vrije Universiteit Brussel (VUB), Faculty LK, Brussels, Belgium 2 Rehabilitation and Health Centre, Virga Jesse Hospital, Hasselt, Belgium 3 Human Biology and Movement Sciences, Nutrition Research Institute Maastricht (NUTRIM), Maastricht University, Maastricht, The Netherlands Contents Abstract ..................................................................................... 31 1. Effects of Exercise Training on Fat Mass ...................................................... 33 1.1 Effects of Endurance Training on Fat-Mass Loss During Caloric Restriction ................... 33 1.2 Site Specific Fat-Mass Loss ............................................................. 35 1.3 Predictive Factors for Fat-Mass Loss ..................................................... 35 2. Endurance Training and Energy Balance .................................................... 36 2.1 Energy Balance ....................................................................... 36 2.2 Energy Expenditure and Physical Exercise ............................................... 36 2.3 Basal Metabolic Rate ................................................................. 37 2.4 Fat Oxidation ......................................................................... 37 3. Influences of Training Modalities on Fat-Mass Loss ............................................ 39 3.1 Exercise Intensity ...................................................................... 39 3.2 Amount of Exercise ................................................................... 39 3.3 Type of Endurance Exercise ............................................................ 41 3.4 Resistance Exercise ................................................................... 41 4. Future Directions .......................................................................... 42 5. Conclusions .............................................................................. 43 Dietary restriction combined with endurance exercise training represents an Abstract effective strategy to promote weight loss and reduce fat mass in obese patients. Exercise programmes without dietary restriction are less efficient. However, addition of exercise to a dietary restriction programme does not induce a greater fat-mass loss than dietary restriction alone. The latter is likely attributed to a compensatory reduction in daily physical activity following the implementation of exercise training. Nonetheless, inclusion of an exercise training programme is important to prevent a decrease in fat-free mass, increase relative visceral fat-mass loss, improve dietary compliance and eventually maintain long-term weight control. Obese male patients with the highest fat mass are most likely to lose the largest amount of fat mass in such lifestyle intervention programmes. Influences

Upload: luc-j-c-van-loon

Post on 13-Dec-2016

217 views

Category:

Documents


0 download

TRANSCRIPT

Page 1: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

Sports Med 2007; 37 (1): 31-46REVIEW ARTICLE 0112-1642/07/0001-0031/$44.95/0

© 2007 Adis Data Information BV. All rights reserved.

The Effects of Exercise Training onFat-Mass Loss in Obese PatientsDuring Energy Intake RestrictionDominique Hansen,1,2 Paul Dendale,2 Jan Berger,2 Luc J.C. van Loon3 andRomain Meeusen1

1 Human Physiology and Sports Medicine, Vrije Universiteit Brussel (VUB), Faculty LK,Brussels, Belgium

2 Rehabilitation and Health Centre, Virga Jesse Hospital, Hasselt, Belgium3 Human Biology and Movement Sciences, Nutrition Research Institute Maastricht (NUTRIM),

Maastricht University, Maastricht, The Netherlands

ContentsAbstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 311. Effects of Exercise Training on Fat Mass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33

1.1 Effects of Endurance Training on Fat-Mass Loss During Caloric Restriction . . . . . . . . . . . . . . . . . . . 331.2 Site Specific Fat-Mass Loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 351.3 Predictive Factors for Fat-Mass Loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35

2. Endurance Training and Energy Balance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 362.1 Energy Balance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 362.2 Energy Expenditure and Physical Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 362.3 Basal Metabolic Rate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 372.4 Fat Oxidation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37

3. Influences of Training Modalities on Fat-Mass Loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393.1 Exercise Intensity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393.2 Amount of Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393.3 Type of Endurance Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 413.4 Resistance Exercise . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41

4. Future Directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43

Dietary restriction combined with endurance exercise training represents anAbstracteffective strategy to promote weight loss and reduce fat mass in obese patients.Exercise programmes without dietary restriction are less efficient. However,addition of exercise to a dietary restriction programme does not induce a greaterfat-mass loss than dietary restriction alone. The latter is likely attributed to acompensatory reduction in daily physical activity following the implementation ofexercise training. Nonetheless, inclusion of an exercise training programme isimportant to prevent a decrease in fat-free mass, increase relative visceral fat-massloss, improve dietary compliance and eventually maintain long-term weightcontrol. Obese male patients with the highest fat mass are most likely to lose thelargest amount of fat mass in such lifestyle intervention programmes. Influences

Page 2: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

32 Hansen et al.

of training modalities during energy intake restriction on fat-mass loss arereviewed. The relationship between total energy expenditure during exercisetraining and overall fat-mass loss has been firmly established. The amount oftraining forms a more important predictor of fat-mass loss than training intensity.The sort of exercise (e.g. walking, cycling, swimming) plays another importantpredictor of fat-mass loss in intervention programmes. The implementation ofresistance training in such programmes does not augment fat-mass loss butimproves body composition by increasing fat-free mass. Further studies areneeded to define the optimal interventional programme for obese patients.

In the past two decades, the world has exper- diet and food intake modification, exercise trainingienced an increased prevalence of obesity, resulting interventions, surgical modification of the gastro-in-in a global obesity epidemic.[1,2] A key reason be- testinal tract, liposuction and medication, have be-hind this epidemic is the lack of daily physical come available to the obese patient.[7,8] In the firstactivity and food abundance. Our genome was prob- line of medical intervention, most patients will beably selected in the late Palaeolithic period offered an exercise and/or dietary intervention pro-(50 000–10 000BC) from criteria that favoured sur- gramme. In such a lifestyle intervention programme,vival in a physically demanding environment, such two main goals are formulated: (i) weight loss; andas our ancestor’s hunter and gatherer society. Fluc- (ii) enhanced physical workload capacity. At pre-tuations between feast and famine was not unusual, sent, an energy deficit of 500–1000 kcal/day isresulting in oscillations in endogenous fuel storage, recommended to induce proper weight loss.[9] Thisplasma insulin and metabolic regulatory proteins, energy deficit should be realised by a combinationwhich in turn may have driven a selection of a of dietary restriction and physical exercise. Signifi-metabolic genotype optimal for such conditions. cant health benefits can be obtained when perform-The ‘thrifty genes’ theory states that these ing a minimum of 150 minutes of moderate intensityfeast-famine cycles are required for optimal meta- exercise per week (at 55–70% of maximal heart ratebolic function.[3,4] Those individuals in the late capacity), with a progressive increase to 200–300Palaeolithic period who were capable of converting minutes per week.[9]

calories into adipose tissue and easily stored fat The results from combined dietary and exerciseduring feasting, were likely to have had a higher intervention programmes on fat-mass loss and exer-survival rate during famine and were capable of cise capacity suggest a dissociated progress of bothpassing their genes on to the next generation.[5] It outcome measures.[10,11] In other words, fat-massmight be the case that many individuals of our loss is not always associated with an enhanced exer-modern society are carriers of this thrifty genotype. cise capacity and vice versa.[10-21] In this review, weTherefore, overfeeding in combination with a seden- focus on the effects of dietary restriction and exer-tary lifestyle, as seen in the modern era, could be cise training intervention on fat-mass loss and bodyresponsible for the increased prevalence of devastat- composition. We also review the influence of differ-ing consequences such as obesity and type 2 diabe- ent training modalities on the changes in fat mass.tes mellitus. It is important to note that when we refer to ‘fat

In addition to increasing overall mortality, obesi- mass’, we mean ‘adipose tissue mass’. In this re-ty is closely linked to the development of hyperten- view, when mentioning a change in fat mass, we aresion, type 2 diabetes, dyslipidaemia, gallbladder dis- referring to the content of the fat cell and not theease, osteoarthritis, coronary heart disease, stroke, actual number of fat cells. Therefore, with a declinesleep apnoea and other respiratory problems.[6] At in fat mass, it is the content of the fat cell thatpresent, various therapeutic interventions, such as declines (referred as ‘adipose tissue mass’), without

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 3: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

Training and Fat-Mass Loss in Obese Subjects 33

a change in the number of adipocytes. This is in tional effects of exercise training on fat-mass lossclear contrast to the effects of liposuction proce- have the lowest sample sizes, which might questiondures, where a large number of adipocytes are re- their statistical power.moved without affecting adipocyte size. Here, we In table I, it is shown that the duration of theuse ‘fat-mass loss’ as a reference to a reduction in implemented training programme varies considera-adipose tissue mass. bly between studies. However, both in the short and

In this review, we selected studies where the long-term intervention programmes, additional ex-subjects were obese (BMI >30 kg/m2), >19 years of ercise training did not seem to augment fat-massage and who were subjected to an intervention pro- loss during caloric restriction. Therefore, both ingramme. short- and long-term interventions, it seems unlikely

that exercise training promotes fat-mass loss during1. Effects of Exercise Training on caloric restriction. As such, other factors might beFat Mass more important in determining the impact of addi-

tional exercise training on fat-mass loss.In obese patients, fat-mass loss can be effectivelyWhatley et al.[21] reported an enhanced fat-massachieved by combining dietary restriction with en-

loss following dietary restriction in combinationdurance exercise training. Miller et al.[22] state thatwith a training programme with high levels of exer-the average weight loss as a result of 16 weeks ofcise, as opposed to a training regimen with lowcombined endurance exercise and caloric restrictionlevels of exercise, where no enhanced fat-mass lossaverages ≈11kg. Even without dietary restriction,was detected. This study clearly showed the impor-endurance exercise training effectively lowerstance of the amount of endurance training to max-bodyweight,[20,23,24] although to a lesser extent (onimise fat-mass loss. This adds to the apparent con-average ≈3kg of bodyweight loss).[22] As such, mosttradictory findings in the literature. Given that thedata suggest that dietary restriction combined withamount of caloric expenditure as result of enduranceaerobic exercise training is the most effective strate-training is of great importance to predict additionalgy to maximise bodyweight loss. But, how much dofat-mass loss during caloric restriction, it is unfortu-we know about the real effects of endurance trainingnate that most studies (see table I) do not mentionon fat-mass loss during programmes that combinethe caloric expenditure per training session.exercise intervention with caloric restriction?

Although there seems to be no substantial addi-1.1 Effects of Endurance Training on tional effect of endurance exercise interventions onFat-Mass Loss During Caloric Restriction fat-mass loss in obese subjects under dietary restric-

tion, exercise interventions are associated with otherIt has been debated to what extent endurancemajor health benefits. The latter is supported bytraining augments fat-mass loss in obese subjectsnumerous studies showing improved maintenanceunder dietary restriction. As shown in table I, manyof the initial bodyweight loss following combinedstudies report that the inclusion of aerobic exercise,exercise and dietary intervention, as opposed toin addition to an energy intake restriction pro-dietary restriction alone.[22] However, in this meta-gramme, does not appear to facilitate fat-massanalysis, the therapy compliance was not analysed.loss.[10,12,14,16,18,19,23,25-34] This is confirmed in aThis is unfortunate as it has been speculated thatmeta-analysis by Miller et al.[22] and only a fewcompliance to a dietary restriction can be improvedstudies show otherwise.[35-38] It remains to be estab-by the implementation of exercise training in thelished which factors are responsible for the apparentinterventional programme.[38]

contradictory findings, as the body fat assessmentprocedure, subject age, intervention duration and The meta-analysis conducted by Ballor andapplied methodology were similar in these studies. Poehlman[39] revealed another important effect ofNonetheless, those studies with evidence for addi- exercise training on the changes in fat-free mass as

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 4: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

34H

ansen et al.

© 2007 A

dis D

ata

Info

rma

tion

BV. A

ll righ

ts rese

rved

.Sp

orts M

ed

2007; 37 (1)

Table I. Studies comparing caloric restriction with combined caloric restriction/endurance training: effects of additional endurance training on fat-mass loss

Author (reference) Subject characteristics (two groups compared in each study) Daily caloric Programme Effect of extra

mean age mean BMI mean % fat sex no. of expenditure during duration (weeks) training on fat-(years) (kg/m2) participants exercise mass loss during

(kilocalories) caloric restriction

Ashutosh et al.[14] 46 vs 40 NA NA f 6 vs 8 NA 52 –

Dengel et al.[10] 61 vs 57 30.1 vs 30.3 30.2 vs 30.1 m 28 vs 23 NA 40 –

Dengel et al.[34] 60 vs 58 NA 29.3 vs 29.5 m 14 vs 14 NA 40 –

Donnelly et al.[16] NA 38.2 vs 37.5 47.0 vs 46.6 f 26 vs 16 NA 12 –

Donnelly et al.[33] NA NA 46.9 vs 46.7 f 28 vs 18 NA 12 –

Fox et al.[29] 66 vs 65 29.8 vs 30.6 43.3 vs 42.8 f 13 vs 16 200 24 –

Geliebter et al.[18] 36 vs 36 NA 39.8 vs 41.3 m and f 23 vs 22 64 8 –

Hays et al.[35] 67 vs 65 31.0 vs 30.8 42.1 vs 41.2 m and f 11 vs 11 NA 14 +

Hill et al.[36] 37 vs 35 35 vs 36 44.3 vs 44.5 f 3 vs 5 288 5 +

Kempen et al.[37] 37 vs 39 31.7 vs 32.4 41.8 vs 41.6 f 10 vs 10 201 10 +

Lennon et al.[27] 34 vs 31 NA 31.1 vs 29.7 m and f 22 vs 20 120 (f) and 211 (m) 12 –

Marks et al.[30] 38 vs 39 30.1 vs 28.7 41.5 vs 38.3 f 10 vs 8 76 20 –

Nieman et al.[26] 45 34.2 vs 32.6 44.3 vs 43.3 f 22 vs 26 NA 12 –

Pronk et al.[19] 43 vs 44 NA 47.5 vs 46.7 f 40 vs 23 NA 12 –

Utter et al.[23] 45 vs 49 34.2 vs 32.6 44.3 vs 43.4 f 26 vs 22 182 12 –

Racette et al.[38] 41 vs 36 NA 44.2 vs 45.0 f 6 vs 5 105 12 +

Sweeney et al.[25] 32 vs 40 34.4 vs 34.6 45.1 vs 44.3 f 5 vs 5 NA 24 –

van Aggel-Leijssen et al.[12] 39 vs 39 32.0 vs 32.6 34.6 vs 33.5 m 17 vs 20 164 10 –

Wadden et al.[31] 41 vs 43 36.4 vs 35.3 46.7 vs 46.8 f 29 vs 29 NA 48 –

Weinstock et al.[32] 43 35.2 vs 36.4 NA f 15 vs 14 NA 48 –

Wirth et al.[28] 43 vs 44 36 vs 34 29.1 vs 26.8 m and f 20 vs 20 NA 4 –

BMI = body mass index; f = female; m = male; NA = data not available; – indicates no effect of adding exercise training to caloric restriction; + indicates greater fat-mass loss byadding exercise training to caloric restriction.

Page 5: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

Training and Fat-Mass Loss in Obese Subjects 35

observed during dietary restriction. Although the caused as a result of an increased β1- and β2-adre-authors reported comparable bodyweight losses fol- noreceptor density and sensitivity, and reducedlowing dietary restriction or combined dietary re- α2-adrenoreceptor affinity and number in the ab-striction and exercise training, the programme in- dominal and visceral adipose tissue.[47]

cluding the endurance training regimen resulted in aless significant decline in fat-free mass. As such, 1.3 Predictive Factors for Fat-Mass Lossexercise intervention seems to be effective as a

Dengel et al.[10] and Wadden et al.[31] observed ameans to reduce or even prevent the decline in fat-correlation between total baseline bodyweight/fatfree mass that is generally observed during energymass with the subsequent reduction in bodyweight/intake restriction.fat mass following intervention programmes aimedAlthough Bond Brill et al.[40] also reported noto reduce bodyweight. Subjects with the highestdifferences in fat-mass loss between dietary restric-baseline fat mass experienced the greatest absolutetion or a combined dietary restriction/endurancefat mass reduction. Furthermore, gender was showntraining programme, a greater decline in sagittal andto be a major factor in determining the extent of fat-waist diameter was observed in the combined dieta-mass loss. Ballor and Keesey[48] observed in theirry restriction/endurance training programme. Thesemeta-analysis that men show a larger bodyweightfindings imply a preferential loss of central adiposi-loss as a result of dietary restriction and exercisety following a combined energy intake restrictiontraining, when compared with women. In contrast,and exercise training programme. This would re-Andersson et al.[49] showed that the bodyweight andpresent a major health benefit as there is a strongfat-mass loss was comparable between obese menrelationship between visceral obesity and insulinand women as a result of a 3-month combinedresistance, and cardiovascular risk.[41,42]

intervention programme. However, when looking atthe data in more detail, it seems that in the Ander-1.2 Site Specific Fat-Mass Losssson et al.[49] study, baseline fat mass was greater inthe female participants. After correction for differ-Fat-mass loss as a result of dietary intake restric-ences in baseline fat mass, the men had actually losttion and endurance exercise training seems to occura higher amount of fat. The authors explained thein certain regions of the body. Ross et al.[43] applieddiscrepancy in fat-mass loss by an increased energymagnetic resonance imaging to show a greater rela-intake in the female subjects, while the men showedtive reduction in the visceral fat depots, when com-no compensation in energy intake for the greaterpared with the gluteal/femoral fat depots, followingenergy expenditure.[49]a combined diet-exercise intervention in males. The

It seems that obesity is an emerging problem withinclusion of aerobic exercise training, in addition toincreasing age and that this could be partially causeddietary restriction, seems to facilitate this region-by factors such as a lower basal metabolic rate,dependent effect.[44,45] This indicates that mainlyreduced daily physical activity, endocrine changesvisceral fat depots are under the influence of exer-and/or the progressive development of insulin resis-cise training and dietary restriction, while the effecttance.[50,51] Although a combination of caloric intakeis less obvious for the gluteal/femoral fat depots.[12]

restriction and exercise intervention can effectivelyThis region-dependent effect might be caused byreduce fat mass in the elderly,[10] a direct compari-differences in catecholamine-induced lipolysis andson of fat-mass loss following lifestyle interventionthe sensitivity to the anti-lipolytic properties of cir-programmes in young and elderly obese subjects isculating insulin levels.[46] In line with these results,presently unavailable.it was shown that abdominal visceral adipocytes are

more sensitive to adrenergic stimulation and less Although the prevalence of obesity is higher insensitive to the anti-lipolytic effect of insulin, when African American women compared with Caucasiancompared with femoral adipocytes.[47] This could be women in the US,[52] the response to dietary restric-

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 6: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

36 Hansen et al.

tion and exercise intervention on fat-mass loss, as ty. However, Hill and Melanson[53] suggested thatassessed by air displacement plethysmography, has there are only minor differences in total energy and/been shown to be similar between the two popula- or fat intake between lean and obese subjects. Intions.[52] These results suggest that ethnic differ- addition, by measuring total energy expenditureences do not form a major factor in determining with the doubly labelled water method, Schoeller[54]

programme outcome. reported that obese individuals maintain their obesestate with an energy intake lower than those of lean

2. Endurance Training and individuals. According to these data, the obesityEnergy Balance epidemic is more likely to be a result of lifestyle

changes than merely changes in dietary intake. InThe only way to prevent obesity is to restore the

accordance, others have reported that the substantialbalance between caloric intake and energy expendi-

progressive decline in the level of physical activityture. Theoretically, the implementation of additional

over the last few decades is largely responsible forexercise training during caloric restriction should

the increased prevalence in obesity in our Westerninduce an increased negative energy balance and

society.[55,56] These results were obtained throughfurther augment fat-mass loss.

high-quality daily physical activity assessment pro-However, most studies indicate that the imple-

cedures, such as a respiratory chamber combinedmentation of endurance training during dietary re-

with the use of body accelerometers and the doublystriction does not further reduce weight loss or fat-

labelled water method.mass loss in obese subjects.[22] This seems to be

During dietary restriction interventions, energyatypical from an energy balance point of view. How-

intake is profoundly reduced. People have been re-ever, this can be explained by the observation that

luctant to superimpose exercise training in additionafter the implementation of exercise training in to

to the caloric restriction regimen as this would likelythe daily routine, people tend to compensate for the

affect hunger/satiety and could consequently reduceincreased energy expenditure by increasing energy

compliance to the dietary restriction. However, dataintake and/or by reducing energy expenditure

indicate that long-term exercise training does notthroughout their daily routine, as assessed by the

increase hunger or daily food intake.[57] Blundell etdoubly labelled water method.[37] In this section, we

al.[58] showed that, after correction for the increasefocus on these compensatory mechanisms to explain

in energy expenditure, food consumption followingthe rather marginal benefits of endurance training on

combined exercise and dietary restriction was simi-fat-mass loss during dietary restriction in obese sub-

lar or even reduced when compared with energyjects.

restriction only. Only ≈30% of the consumed energyduring exercise training was compensated through2.1 Energy Balanceelevated food intake.[58] So, exercise training actual-

Bodyweight reduction as result of exercise train- ly seems to stimulate the maintenance of a moreing and energy intake restriction is attributed to the negative energy balance.change in energy balance, in which energy expendi-ture is increased through physical exercise and ener- 2.2 Energy Expenditure and Physical Exercisegy intake is either maintained or reduced.[6] Thethree most important factors in this energy balance Physical activity levels have declined dramatical-are: (i) food intake; (ii) energy expenditure through ly over the last few decades. The reduction in dailyphysical activity; and (iii) energy expenditure physical activity in our modern civilisation is associ-through basal metabolic rate. ated with a progressive, long-term increase in

It has often been suggested that a high dietary fat bodyweight.[55,56] Following the implementation ofintake is the main cause for an increase in dietary intake restriction, energy expenditure is fur-bodyweight over the years, resulting in overt obesi- ther decreased by a compensatory decline in daily

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 7: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

Training and Fat-Mass Loss in Obese Subjects 37

physical activity.[59] The implementation of an en- 2.3 Basal Metabolic Ratedurance exercise programme seems to be effective

Basal metabolic rate accounts for approximatelyin preventing this decline in daily energy expendi- two-thirds of the total resting energy expenditure.ture during dietary restriction. Moreover, Racette et Ravussin et al.[60] showed that basal metabolic rateal.[38] observed that 12 weeks of dietary restriction represents a good predictor for long-term weightresulted in decreased daily physical activity in obese gain. During a 2-year follow-up, the risk of gainingwomen. Interestingly, when these subjects partici- >7.5kg of bodyweight increased 4-fold for thosepated in an endurance training regimen (3 sessions patients with a low adjusted 24 hour resting energy

expenditure. Following dietary restriction, basalper week, 45 minutes per session), their averagemetabolic rate tends to decrease bydaily physical activity outside the training centre10–20%.[18,21,36,37,61,62] The implementation of en-also significantly increased. Discrepant findingsdurance exercise training does not seem to preventwere reported by Kempen et al.[37] Following energythis decline in basal metabolic rate, according tointake restriction, they also reported a reduction instudies using open circuit spirometry.[18,21,36,37,61,62]

daily energy expenditure. However, the implemen-Whatley et al.[21] reported no significant effects on

tation of an endurance training programmes did notthe decline in basal metabolic rate following the

increase total daily energy expenditure, as subjects addition of both moderate (200 minutes per week) orcompensated for their reduced energy intake by longer (400 minutes per week) periods of endurancereducing daily physical activity outside the training exercise to a dietary restriction intervention. Thiscentre. There is no apparent explanation for the seems to be in accordance with the observation thatcontradictory findings, as the subject populations endurance exercise training does not augment fat-and intervention types between studies were nearly mass loss during energy intake restriction.identical. Nonetheless, an important difference in

2.4 Fat Oxidationdaily physical assessment methodology was foundbetween these studies. Kempen et al.[37] assessed Generally, obesity is secondary to the long-termdaily physical activity level by dividing average presence of a mismatch between energy intake anddaily metabolic rate by sleeping metabolic rate, and energy expenditure. However, there is also evidenceby subtracting sleeping metabolic from average dai- to suggest that metabolic disturbances are responsi-

ble for weight gain in obese patients. A disturbed fatly metabolic rate. Racette et al.[38] measured dailyoxidative capacity could be an important factor inphysical activity level with identical calculations,the aetiology of obesity. Zurlo et al.[63] reported thatalthough they added results from 7-day physicalresting respiratory quotient (RQ) forms a good pre-activity questionnaires and continuous heart-ratedictor of bodyweight gain. In this study, subjectsmonitoring. As both studies assessed physical activ-with a high baseline 24-hour RQ (90th percentile)ity levels with excellent methodology, it remainshad a 2.5-fold higher risk of gaining >5kgspeculative whether exercise training affects dailybodyweight during follow-up than subjects with a

physical activity. Therefore, it seems to be impossi-low resting RQ (10th percentile). Hainer et al.[64]

ble to predict the effect of additional exercise train- found similar effects on resting RQ on long-terming on daily physical activity and, as such, on overall bodyweight control in obese patients after complet-energy balance. As a result of these discrepant find- ing a very low energy intake diet. These studiesings in the literature, more research is warranted to suggest that basal fat oxidation rate represents anelucidate how endurance training affects daily phys- important factor in bodyweight management.ical activity and how to design exercise interven- Unfortunately, dietary restriction often leads totions that are most effective in modulating daily an additional decline of the basal fat oxidationenergy balance. rate.[12] This is an important negative effect as the

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 8: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

38 Hansen et al.

maintenance or reduction of bodyweight gets more ance training on the fat oxidation capacity duringdifficult as the dietary intervention progresses. The exercise in obese women during caloric restriction.addition of exercise training to dietary restriction However, important influences of training intensitybecomes interesting since one might assume that and body fat distribution were reported in otherincreased physical activity prevents the decline of studies and might explain this negative result.[13,44]

basal fat oxidation. Whether exercise training has a Van Aggel-Leijssen et al.[13] reported an increase instimulating effect on basal fat oxidation rate and fat fat oxidation rates during exercise following a low-oxidation capacity during exercise conditions in intensity endurance exercise training programmes,obese patients remains a matter of debate. whereas no effects were reported following a high-

intensity endurance training. A different study[44]Some authors have reported no effect of endur-also indicated that besides training intensity, bodyance exercise training on basal fat oxidationfat distribution tends to modulate the training re-rate,[13,48,65,66] whereas others have reported asponse on fat oxidation capacity during exercise.stabilisation[12,67] or even an increased basal fat oxi-

dation rate.[37,68,69] Since the applied assessment pro- Van Aggel-Leijssen et al.[44] clearly showed thatcedure for fat oxidation analysis (indirect calorime- only female patients with abdominal adipositytry, some in combination with stable isotope tracer showed an increase in fat oxidation capacity duringmethodology) is not substantially different between moderate-intensity exercise, following the low-in-studies, this is not likely to be responsible for the tensity endurance training. Female patients withapparent contradictory findings. Nonetheless, analy- predominantly gluteal-femoral adiposity showed nosis of the baseline lipid oxidation capacity-affecting changes in fat oxidation capacity during exercise.[44]

factors (e.g. intramyocellular triacylglycerol con- These results suggest that visceral fat depots aretent, mitochondrial density, fatty acid binding prote- more susceptible to exercise training when com-in and β-oxidation enzyme activity) should be incor- pared with the gluteal-femoral fat depots. This couldporated in these studies. It may be the case that these be attributed to the differences in adrenergic recep-baseline factors vary considerably between obese tor number and binding affinity between abdominalindividuals, consequently affecting changes in lipid and gluteal fat depots.[70] Therefore, future studiesoxidation capacity by exercise training. Besides

on this topic should take in to account body-fatthese suggestions, the discrepant findings in the

distribution and training intensity in order to explainliterature may be related to differences in training

the effects of additional endurance training duringmodalities in the various exercise interventioncaloric restriction on fat oxidation capacity duringprogrammes. In accordance, Goodpaster et al.[67]

exercise in obese subjects.reported a significant correlation between thestabilisation of basal fat oxidation rate and energy Circulating plasma-free fatty acids could play anexpenditure of the exercise training sessions. The important role in the presence or absence of possiblehigher the energy expenditure during training, the effects of exercise and/or dietary intervention on fatgreater the chance of stabilisation of the resting fat oxidation rates. However, a stable isotope study[13]

oxidation rate during caloric restriction. In conclu- indicated that the reported increase in fat oxidationsion, it still remains to be established whether there rate during exercise, as a result of endurance train-are any positive effects of additional endurance ing, is entirely attributed to an increase in the use oftraining during caloric restriction on basal resting fat fat sources other than plasma-free fatty acids. Theseoxidation rate in obese subjects. other fat sources include lipoprotein and/or intra-

muscular-derived triacylglycerol.[12,13] The increaseThe effects of exercise training, as an addition toin the use of the intramuscular triacylglycerol poolcaloric restriction, on the fat oxidation capacity dur-following endurance training is likely to be associat-ing exercise are also controversial. Kanaley et al.[69]

found no influence of 16 weeks of additional endur- ed with alterations in cellular metabolism,[71,72] skel-

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 9: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

Training and Fat-Mass Loss in Obese Subjects 39

etal muscle insulin sensitivity[66,67,73] and β-adrener- method with questionable precision.[79] Van Aggel-gic sensitivity.[12,74,75] Leijssen et al.[13] also showed no influence of train-

ing intensity (40% vs 70% maximal oxygen uptake3. Influences of Training Modalities on [VO2max]) on fat-mass loss or body compositionFat-Mass Loss following 12 weeks of endurance training in obese

men (as assessed by hydrostatic weighing). TheThe addition of an exercise regimen within a

absence of marked differences in bodyweight and/ordietary restriction programme does not seem to in-

fat mass between high- and low-intensity trainingduce a substantially greater fat-mass loss than dieta-

might simply be attributed to the fact that the studiedry restriction alone. This neutral effect can be attrib-

obese subjects are generally sedentary with a veryuted to a decreased physical activity level outside

low exercise capacity. As a result, absolute differ-the training centre and the lack of a stimulating or

ences in energy expenditure between a workload setstabilising effect on the basal metabolic rate and

at their individual 40–50% VO2max and a 70–80%resting fat oxidation capacity. However, the efficacy

VO2max might simply be negligible on the whole-of an exercise intervention programme to stimulate

body fat-mass balance.fat-mass reduction might be determined by many of

The available data suggest that training intensityits components. In this section, the role of differentdoes not represent a major factor in determining fat-training modalities on stimulating fat-mass reduc-mass loss during dietary intake restriction in obesetion are reviewed, including training intensity,subjects. However, compliance to an exercise regi-amount of exercise, type of exercise and inclusion ofmen has been reported to be associated with theresistance exercise (see table II). From table II, itimpact of the training workload.[80] Because compli-should be noted that only a few studies investigatedance to a high-intensity training programme is likelymale obese subjects.to be lower than to a low-intensity training pro-gramme, this could explain the absence of a greater3.1 Exercise Intensityreduction in fat-mass loss in high-intensity training

In clinical practice, obese patients are generally programmes. Wadden et al.[31] reported treatmentadvised to participate in a low-intensity exercise attendance at the training centre to correlate with theprogramme. Ballor et al.[15] compared the following resultant weight loss during a combined dietary re-two subgroups of obese women during energy in- striction and exercise training programme in obesetake restriction: (i) a high intensity training group subjects. As compliance to an exercise programme(exercising for 25 minutes at 80–90% peak oxygen is a main factor determining the efficacy and long-uptake [VO2peak] per session); and (ii) a low intensi- term weight maintenance, low-intensity exercisety training group (exercising for 50 minutes at programmes seem to be preferred when designing40–50% VO2peak per session). After 8 weeks (three combined dietary and exercise interventionsessions per week) of exercise training, no differ- programmes to reduce bodyweight/fat mass in obeseences in fat mass or body composition were ob- patients.served between the two groups (as assessed by hy-drostatic weighing). Leutholtz et al.[76] investigated 3.2 Amount of Exercisethe influence of endurance training at 40% and 60%of heart rate reserve (three sessions per week, over a In a study of Bond Brill et al.,[40] the dose-3-month period), in combination with a dietary re- dependent effect of walking on body compositionstriction intervention. No differences in fat mass or was analysed during a dietary restriction pro-bodyweight loss were observed between the groups. gramme. One group of obese women were instruct-However, it should be noted that bio-electrical im- ed to walk for 30 minutes, 5 days a week, whereaspedance analysis was applied to assess fat mass in the other group walked for 60 minutes, 5 days athis study, which has been shown to represent a week. After 12 weeks of training, no differences in

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 10: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

40H

ansen et al.

© 2007 A

dis D

ata

Info

rma

tion

BV. A

ll righ

ts rese

rved

.Sp

orts M

ed

2007; 37 (1)

Table II. Influences of training modalities on fat-mass loss during caloric restriction in obese subjects

Author (reference) Subject characteristics (two groups compared in each study) Analysed training modality Effects of training modality on

mean age mean BMI mean % fat sex no. of fat-mass loss(years) (kg/m2) participants

Ballor et al.[15] NA NA 36.1 vs 37.5 f 14 vs 13 Intensity No effect found

Leutholtz et al.[76] 43 vs 40 NA 44.4 m and f 20 vs 20 Intensity No effect found

van Aggel-Leijssen et al.[13] 43 vs 40 31.6 vs 32.2 31.9 vs 31.3 m 12 vs 12 Intensity No effect found

Bond Brill et al.[40] 39 vs 40 35.3 vs 33.8 41.6 vs 41.2 f 21 vs 19 Session volume/expenditure No effect found

Jeffery et al.[77] 42 31.7 NA m and f 101 vs 101 Session volume/expenditure Greater weight loss withhigher levels of training

Whatley et al.[21] 39 vs 36 36.0 vs 35.4 45.8 vs 43.5 f 8 vs 8 Session volume/expenditure Greater fat-mass loss withhigher levels of training

Gwinup[78] 31 vs 28 vs NA 30–40 f 11 vs 10 vs 8 Mode Walking or cycling: effect32 swimming: no effect

Donnelly et al.[16] NA 38.2 vs 38.2 47.0 vs 45.5 f 26 vs 18 Resistance ex in diet No effect found

Marks et al.[30] 38 vs 39 30.1 vs 30.4 41.5 vs 40.9 f 10 vs 11 Resistance ex in diet No effect found

Pronk et al.[19] 42 vs 36 NA 47.4 vs 45.3 f 40 vs 23 Resistance ex in diet No effect found

Ross et al.[43] 47 vs 39 31.6 vs 33.5 NA m 11 vs 11 Resistance ex in diet No effect found

Wadden et al.[31] 41 vs 40 36.4 vs 36.5 46.7 vs 45.0 f 29 vs 31 Resistance ex in diet No effect found

Weinstock et al.[32] 43 35.2 vs 36.2 NA f 15 vs 16 Resistance ex in diet No effect found

Ashutosh et al.[14] 41 vs 45 NA NA f 8 vs 9 Resistance ex in diet/ No effect foundendurance ex

Donnelly et al.[16] NA 37.5 vs 38.3 46.6 vs 46.5 f 16 vs 9 Resistance ex in diet/ No effect foundendurance ex

Donnelly et al.[33] NA NA 46.7 vs 46.2 f 18 vs 21 Resistance ex in diet/ No effect foundendurance ex

Marks et al.[30] 39 vs 40 28.7 vs 31.3 38.3 vs 43.3 f 10 vs 10 Resistance ex in diet/ No effect foundendurance ex

Sweeney et al.[25] 32 vs 29 34.3 vs 36.7 45.1 vs 44.9 f 5 vs 6 Resistance ex in diet/ Effect at 3 months, no effectendurance ex at 6 months

Wadden et al.[31] 41 vs 43 37.3 vs 35.3 47.3 vs 44.2 f 31 vs 29 Resistance ex in diet/ No effect foundendurance ex

BMI = body mass index; ex = exercises; f = female; m = male; NA = data not available.

Page 11: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

Training and Fat-Mass Loss in Obese Subjects 41

fat-mass loss were observed between the groups, as between groups might have disappeared and no dif-ferences in fat-mass loss between the groups coulddetermined by the hydrodensitometry method.[40]

be found, Therefore, Whatley et al.[21] and Jeffery etWhatley et al.[21] compared the effects of two exer-al.[77] provided more reliable results for interpretingcise intervention programmes in obese females. Onethe effects of the amount of exercise training on fat-group exercised for 400 minutes per week (fivemass loss.sessions per week), whereas the other group exer-

In conclusion, increasing the amount of trainingcised for just 210 minutes per week (three sessionsseems to represent an effective means to augmentper week) for a period of 12 weeks, during whichthe net decline in fat mass/bodyweight during aenergy intake was restricted. In this study, the train-combined dietary and exercise intervention pro-ing group with high levels of exercise lost consider-gramme.ably more fat mass through underwater weighing

than the low-level training group (16 ± 4kg vs 13 ±3.3 Type of Endurance Exercise4kg, respectively). Furthermore, a significant corre-

lation between fat-mass loss and total work duration The type of exercise that is most effective inwas reported. In accordance, Jeffery et al.[77] report- reducing body fat in obese subjects remains unclear.ed an important contribution of energy expenditure Gwinup[78] investigated the effects of a walking,during exercise to weight loss in obese patients. In cycling or swimming regimen on bodyweight in 29their study, one group of obese patients was includ- obese women, in the absence of any dietary restric-ed into a standard behaviour intervention pro- tion. All women progressively increased physicalgramme with an energy expenditure goal of 1000 activity up to 60 minutes per day. After 6 months ofkcal/week, whereas a second group received the exercise training, only the cycling and walkingsame behaviour intervention programme, together groups showed a significant decline in bodyweight,with a high physical activity treatment (energy ex- whereas no changes were observed in the swimmingpenditure at 2500 kcal/week). After 12 and 18 group. However, it should be noted that trainingmonths, the reported cumulative weight loss was intensity and/or energy expenditure were notsignificantly higher in the highly active versus the standardised in this study. Furthermore, as changesstandard intervention group. Again, the reported in body composition were not assessed in this study,weight loss correlated well with the estimated ener- no information was provided on the changes in fat-gy expenditure. free mass and fat mass in each of the intervention

groups. More research is warranted to confirm theseThe results of Whatley et al.[21] and Jeffery etresults. When performed at the same relative wor-al.[77] were in clear contradiction with those of Bondkload, energy expenditure is considerably higherBrill et al.[40] However, in the study by Bond Brill etduring walking than with arm cycling or cycling.[81]

al.,[40] the training intensity was self-selected and notIn addition, during walking the relative contributionrecorded, while this was standardised in the studiesof fat oxidation to total energy expenditure is higherby Whatley et al.[21] and Jeffery et al.[77] Analysis ofwhen compared with cycling at an identical relativeVO2peak in the study by Bond-Brill et al.[40] revealedworkload.[82] Considering the relationship betweenthat the subjects improved their peak exercise capac-caloric expenditure during training and fat-massity to a greater extent as a result of short trainingloss, walking (and/or running) exercise seems to besessions (11.7% increase in VO2peak), comparedthe preferred type of exercise in obese patients.with long training sessions (6.6% increase in

VO2peak). Therefore, it might be suggested that dur-3.4 Resistance Exercise

ing the short exercise bouts the subjects trained at ahigher self-chosen intensity compared with the long The implementation of resistance exercise train-exercise bouts. Consequently, the differences in ca- ing within a dietary intake restriction pro-loric expenditure as a result of exercise training gramme[16,19,30-32,43] or a combined dietary restriction

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 12: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

42 Hansen et al.

and endurance training programme[14,16,25,30,31,33] has In conclusion, the addition of resistance trainingto endurance training and dietary restrictionbeen intensively studied. Even though energy ex-programmes does not modulate fat-mass loss, butpenditure was increased as a consequence of resis-prevents the decline in fat-free mass and restingtance training, it was not sufficient to augment fat-metabolic rate. As such, resistance training can re-mass loss. The change in bodyweight, as a result ofpresent an effective means to improve body compo-endurance exercise training and/or dietary restric-sition and maintain the reduced fat mass.tion, could not be modulated through resistance

training.4. Future Directions

Despite the absence of any effects of resistanceexercise on fat-mass loss, positive effects have been The most striking finding in this review is thereported regarding muscle/fat-free mass. The addi- neutral effect of additional exercise training on fat-tion of resistance training to dietary restriction and/ mass loss during caloric restriction. There might beor endurance training prevents the loss of fat-free an indication that alterations in daily physical activi-mass, secondary to dietary restriction.[83] Sweeney et ty and food intake patterns, as a result of this exer-al.[25] reported, by applying hydrostatic weighing, a cise training programme, suppresses the effects onsmaller decline in fat-free mass following a com- fat-mass loss, although no conclusive evidencebined endurance and resistance training programme could be provided. Therefore, it remains to be ex-in obese patients under dietary restriction after amined how exercise training affects food intake3 months of intervention, when compared with en- and daily physical activity outside the training cen-

tre in obese subjects during caloric restriction. Aredurance training alone. In addition, the same meth-there compensatory behavioural actions in these pa-odology was applied by Geliebter et al.[18] showingtients and how can we deal with them?that the inclusion of resistance exercise training in a

dietary intervention programme (without endurance In addition, most studies focus on fat-masschange, while many of the obesity-related healthtraining) prevented the loss of fat-free mass in obesecomplications, such as insulin resistance and cardio-subjects.vascular disease, are affected by exercise training,As such, it seems that resistance training shouldeven in the absence of measurable changes in body-form an integrative part of any exercise interventionfat mass. For example, the fat mass/fat-free massto improve muscle mass and function.[84] This de-ratio, daily physical functioning, quality of life andcreased functional capacity is especially relevant forfeelings of well-being have been reported to im-the older obese patient in which age-related loss ofprove with exercise training in obese subjects in the

muscle mass (sarcopenia) causes a progressive de-absence of significant changes in fat mass. There-

cline in functional capacity. This can lead to afore, exercise interventions studies should not limit

further reduction in daily physical activity, acceler-their focus on changes in fat mass, but should pro-

ating fat-mass gain and the development of chronic vide an insight in to the many other health benefitsmetabolic diseases. of lifestyle intervention in the prevention and treat-

Since endurance exercise performance can be ment of chronic metabolic diseases.improved with the implementation of resistance Furthermore, it remains to be elucidated howtraining,[85] this could assist in the overall process of exercise training affects resting and fat oxidationweight reduction through exercise training and in capacity during exercise. As this capacity is a strongthe prevention of other important negative effects of predictor for long-term bodyweight control and itcaloric restriction. Similar to the observations re- could potentially be affected by exercise training,garding fat-free mass, resistance training prevents efforts in this area might provide great insights forthe decline in resting metabolic rate, which is gener- reversing obesity through exercise training. For ex-ally observed during dietary restriction.[86] ample, it might be of interest to assess the effects of

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 13: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

Training and Fat-Mass Loss in Obese Subjects 43

exercise training modalities (e.g. intensity, bout du- marily established at visceral fat depots and to aration, frequency, inclusion of strength exercises) on lesser extent at the gluteal/femoral fat depots, and isfat oxidation capacity at rest and during exercise in associated with an improved insulin sensitivity andobese individuals. lipid profile. Obese male patients with the highest

fat mass are most susceptible to losing the largestThere is considerable evidence to support theamount of fat mass.inclusion of resistance exercise and caloric restric-

Various training modalities of the exercise inter-tion to exercise training as a means to further im-vention programme, when combined with energyprove body-fat mass loss and body composition.intake restriction, seem to effect fat-mass loss. ThereHowever, only a few studies have investigated theseems to be no direct influence of training intensityeffects of the type, intensity, duration, frequencyon fat-mass loss. So, a low-intensity training regi-and mode of training in subjects at risk of develop-men is preferred, because of greater compliance. Asing chronic metabolic disease (e.g. cardiovasculara greater amount of exercise training induces adisease, type 2 diabetes). Therefore, it is necessarygreater fat-mass loss, the relationship between ener-to elucidate the effects of these training modalitiesgy expenditure during exercise training and fat-massboth on fat-mass loss during caloric restriction, asloss has been established. There might be an influ-well as on the prevention of cardiovascular/metabol-ence of the type of exercise on fat-mass loss; walk-ic disease in obese individuals.ing and cycling have been shown to reduceFinally, as most investigations have includedbodyweight, whereas swimming does not. The in-obese women, further studies should be performedclusion of resistance training in addition to a dietaryto assess potential gender differences in the responserestriction intervention does not influence fat-massto exercise training. This could result in exerciseloss, but could augment fat-free mass and, as such,intervention programmes being designed specifical-prevent a decrease in basal metabolic rate duringly for each gender in order to optimise health bene-energy intake restriction.fits.

For obese patients, the following interventionprogramme can be proposed: combined caloric re-5. Conclusionsstriction and endurance training at three to five

Dietary restriction combined with endurance ex- training sessions per week. The training intensityercise training represents an effective strategy to should be moderate (55–65% VO2max), while thepromote weight loss and reduce fat mass in obese training session duration should be long (>1 hour).patients. Exercise interventions without dietary re- Walking or cycling exercises are preferred, in com-striction are less efficient. Generally, addition of bination with strength training exercises.exercise interventions within a dietary restrictionprogramme does not induce a greater fat-mass loss Acknowledgementsthan dietary restriction alone. This is attributed to acompensatory reduction in daily physical activity We would like to thank Dr Massa Guy for his kindfollowing the implementation of exercise training. assistance in reviewing this article and offering textual sug-As obese patients are often focused on reducing gestions.

No sources of funding were used to assist in the prepara-bodyweight, it is of great importance to point to-tion of this review. The authors have no conflicts of interestwards the other health benefits of additional exercisethat are directly relevant to the content of this review.training, which include the following: prevention of

a decrease in fat-free mass; a higher dietary compli-ance and better maintenance of bodyweight at a References

1. Galobardes B, Costanza MC, Bernstein MS, et al. Trends in risklong-term; and a relative greater loss of visceral fatfactors for the major ‘life-style related diseases’ in Geneva,mass. The reduction in fat mass in a combined Switzerland, 1993-2000. Ann Epidemiol 2003 Aug; 13 (7):

dietary and exercise intervention programme is pri- 537-40

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 14: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

44 Hansen et al.

2. Chopra M, Galbraith S, Darnton-Hill I. A global response to a exercise-induced weight loss in men. Ann Intern Med 2000 Julglobal problem: the epidemic of overnutrition. Bull World 18; 133 (2): 92-103Health Organ 2002; 80 (12): 952-8 21. Whatley JE, Gillespie WJ, Honig J, et al. Does the amount of

3. Chakravarthy MV, Booth FW. Eating, exercise, and ‘thrifty’ endurance exercise in combination with weight training and agenotypes: connecting the dots towards an evolutionary under- very-low-energy diet affect resting metabolic rate and bodystanding of modern diseases. J Appl Physiol 2004 Jan; 96 (1): composition? Am J Clin Nutr 1994 May; 59 (5): 1088-923-10 22. Miller WC, Koceja DM, Hamilton EJ. A meta-analysis of the

4. Booth FW, Chakravarthy MV, Gordon SE, et al. E. Waging war past 25 years of weight loss research using diet, exercise or dieton physical inactivity: using modern molecular ammunition plus exercise intervention. In J Obes 1997 Oct; 21 (10): 941-7against an ancient enemy. J Appl Physiol 2002 Jul; 93 (1): 3-30 23. Utter AC, Nieman DC, Shannonhouse EM, et al. Influence of

5. Neel JV. Diabetes mellitus: a ‘thrifty’ genotype rendered detri- diet and/or exercise on body composition and cardiorespirato-mental by ‘progress’. Am J Hum Genet 1962 Dec; 14: 353-62 ry fitness in obese women. Int J Sport Nutr 1998 Sep; 8 (3):

6. Pronk NP. Economic aspects of obesity: a managed-care per- 213-22spective. In: Andersen RE, editor. Obesity; etiology, assess- 24. Mayo MJ, Grantham JR, Balasekaran G. Exercise-inducedment, treatment, and prevention. Champaign (IL): Human weight loss preferentially reduces abdominal fat. Med SciKinetics, 2003: 33-44 Sports Exerc 2003 Feb; 35 (2): 207-13

7. American Gastroenterological Association. American Gas-25. Sweeney ME, Hill JO, Heller PA, et al. Severe vs moderatetroenterological Association medical position statement on

energy restriction with and without exercise in the treatment ofobesity. Gastroenterology 2002 Sep; 123 (3): 879-81obesity: efficiency of weight loss. Am J Clin Nutr 1993 Feb;

8. Cummings S, Parham ES, Strain GW. Position of the American57 (2): 127-34

Dietetic Association: weight management. J Am Diet Assoc26. Nieman DC, Brock DW, Butterworth D, et al. Reducing diet2002 Aug; 102 (8): 1145-55

and/or exercise training decreases the lipid and lipoprotein risk9. Jakicic JM, Clark K, Coleman E, et al. Appropriate interventionfactors of moderately obese women. Int J Obes 2002 Aug; 21strategies for weight loss and prevention of weight regain for(4): 344-50adults: position stand of The American College of Sports

27. Lennon D, Nagle F, Stratman F, et al. Diet and exercise trainingMedicine. Med Sci Sports Exerc 2001 Dec; 33 (12): 2145-56effects on resting metabolic rate. Int J Obes 1985; 9 (1): 39-4710. Dengel DR, Hagberg JM, Coon PJ, et al. Effects of weight loss

by diet alone or combined with aerobic exercise on body 28. Wirth A, Vogel I, Schomig A, et al. Metabolic effects and bodycomposition in older obese men. Metabolism 1994 Jul; 43 (7): fat mass changes in obese subjects on a very-low-calorie diet867-71 with and without intensive physical training. Ann Nutr Metab

1987; 31 (6): 378-8611. Lamarche B, Despres JP, Pouliot MC, et al. Is body fat loss adeterminant factor in the improvement of carbohydrate and 29. Fox AA, Thompson JL, Butterfield GE, et al. Effects of diet andlipid metabolism following aerobic exercise training in obese exercise on common cardiovascular disease risk factors inwomen? Metabolism 1992 Nov; 41 (11): 1249-56 moderately obese older women. Am J Clin Nutr 1996 Feb; 63

12. van Aggel-Leijssen D, Saris WHM, Hul GB, et al. Short-term (2): 225-33effects of weight loss with or without low-intensity exercise 30. Marks BL, Ward A, Morris DH, et al. Fat-free mass is main-training on fat metabolism in obese men. Am J Clin Nutr 2001 tained in women following a moderate diet and exercise pro-Mar; 73 (3): 523-31 gram. Med Sci Sports Exerc 1995 Sep; 27 (9): 1243-51

13. van Aggel-Leijssen D, Saris WHM, Wagenmakers AJM, et al. 31. Wadden TA, Vogt RA, Andersen RE, et al. Exercise in theEffect of exercise training at different intensities on fat metab- treatment of obesity: effects of four interventions on bodyolism of obese men. J Appl Physiol 2002 Mar; 92 (3): 1300-9 composition, resting energy expenditure, appetite, and mood. J

14. Ashutosh K, Methrotra K, Fragale-Jackson J. Effects of sus- Consult Clin Psychol 1997 Apr; 65 (2): 269-77tained weight loss and exercise on aerobic fitness in obese

32. Weinstock RS, Dai H, Wadden TA. Diet and exercise in thewomen. J Sports Med Phys Fitness 1997 Dec; 37 (4): 252-7treatment of obesity. Arch Intern Med 1998 Dec; 158 (22):

15. Ballor DL, McCarthy JP, Wilterdink EJ. Exercise intensity does 2477-83not affect the composition of diet- and exercise-induced body

33. Donnelly JE, Jacobsen DJ, Jakicic JM, et al. Very low caloriemass loss. Am J Clin Nutr 1990 Feb; 51 (2): 142-6diet with concurrent versus delayed and sequential exercise.16. Donnelly JE, Pronk NP, Jacobsen DJ, et al. Effects of a very-Int J Obes 1994 Jul; 18 (7): 469-75low-calorie diet and physical-training regimens on body com-

34. Dengel DR, Pratley RE, Hagberg JM, et al. Distinct effects ofposition and resting metabolic rate in obese females. Am J Clinaerobic exercise training and weight loss on glucose homeosta-Nutr 1991 Jul; 54 (1): 56-61sis in obese sedentary men. J Appl Physiol 1996 Jul; 81 (1):17. Frey-Hewitt B, Vranizan KM, Dreon DM, et al. The effect of318-25weight loss by dieting or exercise on resting metabolic rate in

35. Hays NP, Starling RD, Kiu X, et al. Effects of an ad libitum low-overweight men. Int J Obes 1990 Apr; 14 (4): 327-34fat, high-carbohydrate diet on body weight, body composition,18. Geliebter A, Maher MM, Gerace L, et al. Effects of strength orand fat distribution in older men and women. Arch Intern Medaerobic training on body composition, resting metabolic rate,2004 Jan 26; 164 (2): 210-7and peak oxygen consumption in obese dieting subjects. Am J

36. Hill JO, Sparling PB, Shields TW, et al. Effects of exercise andClin Nutr 1997 Sep; 66 (3): 557-63food restriction on body composition and metabolic rate in19. Pronk NP, Donnelly JE, Pronk SJ. Strength changes induced byobese women. Am J Clin Nutr 1987 Oct; 46 (4): 622-30extreme dieting and exercise in severely obese women. J Am

Coll Clin Nutr 1992 Apr; 11 (2): 152-8 37. Kempen KPG, Saris WHM, Westerterp KR. Energy balance20. Ross R, Dagnone D, Jones PJH, et al. Reduction in obesity and during an 8-wk energy-restricted diet with and without exer-

related comorbid conditions after diet-induced weight loss or cise in obese women. Am J Clin Nutr 1995 Oct; 62 (4): 722-9

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 15: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

Training and Fat-Mass Loss in Obese Subjects 45

38. Racette SB, Schoeller DA, Kushner RF, et al. Exercise enhances 58. Blundell JE, Stubbs RJ, Hughes DA, et al. Cross talk betweendietary compliance during moderate energy restriction in activity and appetite control: does physical activity stimulateobese women. Am J Clin Nutr 1995 Mar; 62 (3): 345-9 appetite? Proc Nutr Soc 2003 Aug; 62 (3): 651-61

39. Ballor DL, Poehlman ET. Exercise-training enhances fat-free 59. Westerterp KH. Obesity and physical activity. Int J Obes 1999mass preservation during diet-induced weight loss: a meta- Feb; 23 Suppl. 1: S59-64analytical finding. Int J Obes 1994 Jan; 18 (1): 35-40 60. Ravussin E, Lillioja S, Knowler WC, et al. Reduced rate of

40. Bond Brill J, Perry AC, Parker L, et al. Dose-response effect of energy expenditure as a risk factor for body-weight gain. Nwalking exercise on weight loss: how much is enough? Int J Engl J Med 1988 Feb; 318 (8): 467-72Obes 2002 Nov; 26 (11): 1484-93 61. Byrne HK, Wilmore JH. The effects of a 20-week exercise

41. Ohlsen LO, Larsson B, Svardsudd K, et al. The influence of training program on resting metabolic rate in previously seden-body fat distribution on the incidence of diabetes mellitus: 13.5 tary, moderately obese women. Int J Sport Nutr Exerc Metabyears of follow-up of the participants in the study of men born 2001 Mar; 11 (1): 15-31in 1913. Diabetes 1985 Oct; 34 (10): 1055-8 62. Racette SB, Schoeller DA, Kushner RF, et al. Effects of aerobic

42. Peiris AN, Sothmann MS, Hoffmann RG, et al. Adiposity, fat exercise and dietary carbohydrate on energy expenditure anddistribution, and cardiovascular risk. Ann Intern Med 1989; body composition during weight reduction in obese women.110: 867-72 Am J Clin Nutr 1995 Mar; 61 (3): 486-94

43. Ross R, Rissanen J, Pedwell H, et al. Influence of diet and 63. Zurlo F, Lillioja S, Esposito-Del Puente A, et al. Low ratio of fatexercise on skeletal muscle and visceral adipose tissue in men. to carbohydrate oxidation as predictor of weight gain: study ofJ Appl Physiol 1996 Dec; 81 (6): 2445-55 24-h RQ. Am J Physiol 1990 Nov; 259 (5 Pt 1): E650-7

44. van Aggel-Leijssen D, Saris WHM, Wagenmakers AJM, et al. 64. Hainer V, Kunesova M, Parizkova J, et al. Respiratory quotientThe effect of low-intensity exercise training on fat metabolism in obesity: its association with an ability to retain weight lossof obese women. Obes Res 2001 Feb; 9 (2): 86-96 and with parental obesity. Sb Lek 2000; 101 (1): 99-104

45. You T, Murphy KM, Lyles MF, et al. Addition of aerobic65. Nicklas BJ, Rogus EM, Goldberg AP. Exercise blunts declinesexercise to dietary weight loss preferentially reduces abdomi-

in lipolysis and fat oxidation after dietary-induced weight lossnal adipocyte size. Int J Obes 2006 Aug; 30 (8): 1211-6in obese older women. Am J Physiol 1997 Jul; 273 (1 Pt 1):

46. Wajchenberg BL. Subcutaneous and visceral adipose tissue: E149-55their relation to the metabolic syndrome. Endocr Rev 2000

66. Gan SK, Kriketos AD, Ellis BA, et al. Changes in aerobicDec; 21 (6): 697-738capacity and visceral fat but not myocyte levels predict in-

47. Bouchard C, Despres JP, Mauriege PO. Genetic and nongenetic creased insulin action after exercise in overweight and obesedeterminants of regional fat distribution. Endocr Rev 1993 men. Diabetes Care 2003 Jun; 26 (6): 1706-13Feb; 14 (1): 72-93

67. Goodpaster BH, Katsiaras A, Kelley DE. Enhanced fat oxida-48. Ballor DL, Keesey RE. A meta-analysis of the factors affectingtion through physical activity is associated with improvementschanges in body mass, fat mass and fat-free mass in males andin insulin sensitivity in obesity. Diabetes 2003 Sep; 52 (9):females. Int J Obes 1991 Nov; 15 (11): 717-262191-7

49. Andersson B, Xu XF, Rebuffe-Scrive M, et al. The effects of68. Pasman WJ, Westerterp MS, Saris WH. The effect of bodyexercise, training on body composition and metabolism in men

weight changes and endurance training on 24h substrate oxida-and women. Int J Obes 1991 Jan; 15 (1): 75-81tion. Int J Obes 1999 Dec; 23 (12): 1223-32

50. Kennedy RL, Chokkalingham K, Srinivasan R. Obesity in the69. Kanaley JA, Weatherup-Dentes MM, Alvarado CR, et al. Sub-elderly: who should we be treating, and why, and how? Curr

strate oxidation during acute exercise and with exercise train-Opin Clin Nutr Metab Care 2004 Jan; 7 (1): 3-9ing in lean and obese women. Eur J Appl Physiol 2001 Jul; 8551. Elia M. Obesity in the elderly. Obes Res 2001 Nov; 9 Suppl. 4:(1-2): 68-73S244-8

70. Wahrenberg H, Lonnqvist F, Arner P. Mechanisms underlying52. Glass JN, Miller WC, Szymanski LM, et al. Physiologicalregional differences in lipolysis in human adipose tissue. J Clinresponses to weight-loss intervention in inactive obese Afri-Invest 1989 Aug; 84 (2): 458-67can-American and Caucasian women. J Sports Med Phys

71. Mandroukas K, Krotkiewski M, Hedberg M, et al. PhysicalFitness 2002 Mar; 42 (1): 56-64training in obese women: effects of muscle morphology, bio-53. Hill JO, Melanson EL. Overview of the determinants of over-chemistry and function. Eur J Appl Physiol Occup Physiolweight and obesity: current evidence and research issues. Med1984; 52 (4): 355-61Sci Sports Exerc 1999 Nov; 31 Suppl. 11: S515-21

72. Krotkiewski M, Bylund-Fallenius AC, Holm J, et al. Relation-54. Schoeller DA. The importance of clinical research: the role ofship between muscle morphology and metabolism in obesethermogenesis in human obesity. Am J Clin Nutr 2000 Mar; 73women: the effects of long-term physical training. Eur J Clin(3): 511-6Invest 1983 Feb; 13 (1): 5-1255. Zurlo F, Ferraro RT, Fontvielle AM, et al. Spontaneous physical

73. Segal KR, Edano A, Abalos A, et al. Effect of exercise trainingactivity and obesity: cross-sectional and longitudinal studies inon insulin sensitivity and glucose metabolism in lean, obese,Pima Indians. Am J Physiol 1992 Aug; 263 (2 Pt 1): E296-300and diabetic men. J Appl Physiol 1991 Dec; 71 (6): 2402-1156. Weinsier RL, Hunter GR, Desmond RA, et al. Free-living

74. Mauriege P, Despres JP, Prud’Homme D, et al. Regional varia-activity energy expenditure in women successful and unsuc-tion in adipose tissue lipolysis in lean and obese men. J Lip Rescessful at maintaining a normal body weight. Am J Clin Nutr1991 Oct; 32 (10): 1625-332002 Mar; 75 (3): 499-504

57. Blundell JE, King NA. Effects of exercise on appetite control: 75. De Glisezinski I, Crampes F, Harant I, et al. Endurance trainingloose coupling between energy expenditure and energy intake. changes in lipolytic responsiveness of obese adipose tissue.Int J Obes 1998 Aug; 22 Suppl. 2: S22-9 Am J Physiol 1998 Dec; 275 (6 Pt 1): E951-6

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)

Page 16: The Effects of Exercise Training on Fat-Mass Loss in Obese Patients During Energy Intake Restriction

46 Hansen et al.

76. Leutholtz BC, Keyser RE, Heusner WW, et al. Exercise training 83. Stiegler P, Cunliffe A. The role of diet and exercise for theand severe caloric restriction: effect on lean body mass in the maintenance of fat-free mass and resting metabolic rate duringobese. Arch Phys Med Rehabil 1995 Jan; 76 (1): 65-70 weight loss. Sports Med 2006; 36 (3): 239-6

77. Jeffery RW, Wing RR, Sherwood NE, et al. Physical activity84. van Etten MLA, Westerterp KR, Verstappen FTJ, et al. Effect ofand weight loss: does prescribing higher physical activity goals

an 18-wk weight training program on energy expenditure andimprove outcome? Am J Clin Nutr 2003 Oct; 78 (4): 684-978. Gwinup G. Weight loss without dietary restriction: efficacy of physical activity. J Appl Physiol 1997 Jan; 82 (1): 298-304

different forms of aerobic exercise. Am J Sports Med 1987; 15 85. Skinner J, McLellan T. The transition from aerobic to anaerobic(3): 275-9

metabolism. Res Q Exerc Sport 1980 Mar; 51 (1): 234-4879. Lazzer S, Boirie Y, Meyer M, et al. Evalution of two foot-to-86. Bryner RW, Ullrich IH, Sauers J, et al. Effects of resistance vs.foot bioelectrical impedance analysers to assess body compo-

sition in overweight and obese adolescents. Br J Nutr 2003; 90: aerobic training combined with an 800 calorie liquid diet on987-92 lean body mass and resting metabolic rate. J Am Coll Clin Nutr

80. Perri MG, Anton SD, Durning PE, et al. Adherence to exercise 1999 Apr; 18 (2): 115-21prescriptions: effects of prescribing moderate versus higherlevels of intensity and frequency. Health Psychol 2002 Sep; 21(5): 452-8

Correspondence and offprints: Professor Romain Meeusen,81. Davis JA, Vodak P, Wilmore JH, et al. Anaerobic threshold andmaximal aerobic power for three modes of exercise. J Appl Department of Human Physiology and Sports Medicine,Physiol 1976 Oct; 41 (4): 544-50 Vrije Universiteit Brussel (VUB), Faculty LK, Pleinlaan 2,

82. Achten J, Venables MC, Jeukendrup AE. Fat oxidation rates areBrussels, 1050, Belgium.higher during running compared with cycling over a wideE-mail: [email protected] of intensities. Metabolism 2003 Jun; 52 (6): 747-52

© 2007 Adis Data Information BV. All rights reserved. Sports Med 2007; 37 (1)