Efecto de Las Modificaciones de La Dieta

7232019 Efecto de Las Modificaciones de La Dieta

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OBESITY | VOLUME 18 NUMBER 9 | SEPTEMBER 2010 1725

nature publishing group ARTICLES

INTERVENTION AND PREVENTION

INTRODUCTION

Overweight and obesity continues to be a major medical andpublic health concern affecting the lives of over 144 million(66) US adults (1) Based on prevalence trends from theNational Health and Nutrition Examination Studies it is esti-mated that within 30 years nearly all American adults will beoverweight or obese if successful long-term prevention andor treatment strategies to combat this epidemic are not imple-mented (2) Tis public health concern has prompted numerousdiets proposing ldquooptimal weight lossrdquo mediated by decreasedappetite and food intake wo of the more popular dietaryapproaches promoting better weight management includehigher protein intake and greater eating frequency (3)

Accumulating evidence suggests that diets containing higherdietary protein (ranging from 11 to 16 g proteinkgday) leadto greater reductions in total energy intake body weight and fatmass while preserving lean body mass compared to diets con-taining 08 gkgday (the recommended dietary allowance RDA)(4ndash8) One key factor in the efficacy of these diets involves the

improvement in appetite control Single higher protein mealsgenerally reduce postprandial hunger (9) and increase postpran-dial satiety (9ndash12) Tey do so by reportedly altering hormonesassociated with appetite regulation such as ghrelin (9) andpeptide YY (PYY) (13) Limited data exist as to whether thesealterations continue when individuals consume higher proteinmeals throughout the course of an entire day Accordingly theprimary aim of this study was to explore the effects of higherprotein intake on perceived appetite and hormonal responsesthroughout the day in overweight and obese men

Although there is strong scientific support for the incor-poration of additional dietary protein for improved appetitecontrol and weight management the influence of eating fre-quency on these outcomes is highly conflicting Te majorityof studies have focused on whether greater eating frequencyleads to increased daily energy expenditure (see Review byBellisle et al (14)) yet most have found little if any impacton these outcomes (14ndash16) Researchers are now beginning tofocus their attention on the other side of the energy balance

The Influence of Higher Protein Intake

and Greater Eating Frequency on AppetiteControl in Overweight and Obese MenHeather J Leidy 12 Cheryl LH Armstrong2 Minghua Tang2 Richard D Mattes2

and Wayne W Campbell2

The purpose of this study was to determine the effects of dietary protein intake and eating frequency on perceived

appetite satiety and hormonal responses in overweightobese men Thirteen men (age 51 plusmn 4 years BMI

313 plusmn 08 kgm2 ) consumed eucaloric diets containing normal protein (79 plusmn 2 g proteinday 14 of energy intake as

protein) or higher protein (138 plusmn 3 g proteinday 25 of energy intake as protein) equally divided among three eating

occasions (3-EO every 4 h) or six eating occasions (6-EO every 2 h) on four separate days in randomized order

Hunger fullness plasma glucose and hormonal responses were assessed throughout 11 h No protein times eating

frequency interactions were observed for any of the outcomes Independent of eating frequency higher protein led

to greater daily fullness ( P lt 005) and peptide YY (PYY) concentrations ( P lt 005) In contrast higher protein led to

greater daily ghrelin concentrations ( P lt 005) vs normal protein Protein quantity did not influence daily hunger

glucose or insulin concentrations Independent of dietary protein 6-EO led to lower daily fullness ( P lt 005) and PYY

concentrations ( P lt 005) The 6-EO also led to lower glucose ( P lt 005) and insulin concentrations ( P lt 005) vs 3-EO

Although the hunger-related perceived sensations and hormonal responses were conflicting the fullness-related

responses were consistently greater with higher protein intake but lower with increased eating frequency Collectively

these data suggest that higher protein intake promotes satiety and challenge the concept that increasing the number

of eating occasions enhances satiety in overweight and obese men

Obesity (2010) 18 1725ndash1732 doi101038oby201045

1Department of Dietetics amp Nutrition University of Kansas Medical Center Kansas City Kansas USA 2Department of Foods amp Nutrition Ingestive Behavior ResearchCenter Purdue University West Lafayette Indiana USA Correspondence Heather J Leidy (hleidykumcedu )

Received 21 September 2009 accepted 10 February 2010 published online 25 March 2010 doi101038oby201045



1726 VOLUME 18 NUMBER 9 | SEPTEMBER 2010 | wwwobesityjournalorg

ARTICLES


equation by examining the impact of eating frequency onappetite control and food intake In some (1517) but not all(161819) studies greater eating frequency has led to reducedhunger increased satiety and decreased food intake (15ndash19)Te discrepant findings may stem from the wide range of eat-ing frequencies that have been arbitrarily defined as frequent

eating when consisting of 4ndash17 eating occasionsday and infre-quent eating when consisting of one to three mealsdayAlthough the overall message in the mainstream media

proposes an ldquoeat six times a dayrdquo strategy for better appetitecontrol and food intake regulation very little if any scientificevidence exists to evaluate the efficacy of this approach Tusa second aim of this study was to compare the effects of eatingthree timesday which has been the standard dietary pattern inthe past vs six timesday on these outcomes Tis study designalso permitted investigation of a possible synergistic effect ofhigher protein intake and greater eating frequency on per-ceived appetite and hormonal responses throughout the day

METHODS AND PROCEDURES

SubjectsPotential participants were recruited through newspaper advertise-ments Eligibility was based on the following criteria (i) men agege21 years (ii) BMI 250ndash349 kgm2 (iii) percent body fat gt25assessed through skinfold measurements (iv) not dieting and noweight loss or gain (ge45 kg) within the past 6 months (v) nonsmok-ing (vi) nondiabetic (vii) clinically normal blood profiles (normal liver

and kidney function fasting blood glucose lt110 mgdl) (viii) consist-ent habitual activity patterns over the past 3 months and (ix) habitualdietary pattern of consuming three mealsday for the past 3 monthswenty-five men were screened 21 gave informed consent 16 beganand 13 completed all study procedures Reasons for the three dropoutswere military duty relocation and nonstudy compliance Participantssigned an informed consent form approved by the Purdue UniversityBiomedical Institutional Review Board and received monetary com-

pensation for completing all study procedures Clinical testing occurredbetween January 2008 and July 2008 Subject characteristics for thecompleted participants are displayed in Table 1

Experimental designTis study incorporated a randomized crossover design consisting offour 11-h trials On separate days the participants consumed eucaloricdiets containing either normal protein (79 plusmn 2 g proteinday 08 g kgday) or higher protein (138 plusmn 3 g proteinday 14 gkgday) equallydivided among three eating occasions (3-EO provided every 4 h) orsix eating occasions (6-EO provided every 2 h) in a randomized orderPre- and postprandial hunger satiety plasma glucose and hormonalresponses (plasma insulin ghrelin and PYY) were assessed throughouteach 11-h trial

Specific testing day proceduresOn the evening prior to each trial participants were provided with astandardized normal protein dinner to be consumed at home between5 and 7 983152983149 Te participants then fasted until their arrival at the labo-ratory between 7 and 8 983137983149 the following morning Upon arrival theparticipants were placed in a supine position on a bed and a catheterwas inserted in an antecubetal vein of the nondominant arm and keptpatent for the remainder of the testing period by saline drip For the next30 min the participants acclimated to the room and were familiarizedwith the testing day procedures At time 0 a baseline (fasting) bloodsample was taken questionnaires were completed and the first eatingoccasion was provided to the participants Over the remaining 11 hblood sampling and questionnaires were repeated every 20 min Teremaining eating occasions were provided to the participants at set timesand in specific quantities according to the treatment randomization

For each eating occasion the participants were required to consume allfoods and water provided to them within 15 min No additional foodor drink was provided to the participants During the testing periodparticipants remained in a semi-supine position and were permittedto watch television read or use computers At the end of the 11 h thecatheter was removed and the participants were permitted to leave thelaboratory Tere were 1ndash2 weeks between each of the four trials

Eating occasionsTe characteristics of the diets are shown in Table 2 Te participantswere fed according to their daily energy needs Due to the reducedactivity of the volunteers during the 11-h testing days daily energy need

Table 1 Subject characteristics of 13 overweight and obese

men

Subject characteristics Mean plusmn sem

Age (year) 51 plusmn 4

Height (cm) 178 plusmn 2

Weight (kg) 996 plusmn 24

BMI (kgm2 ) 313 plusmn 08

Body fat () 31 plusmn 3

Fasting glucose (mgdl) 97 plusmn 1

Fasting insulin (pmoll) 75 plusmn 16

Habitual meal pattern ( mealsday) 29 plusmn 03

Data expressed as mean plusmn sem

Table 2 Dietary characteristics of the test day diets

Dietary

characteristics

Normal protein testing day Higher protein testing day

3 Eating occasions (3-EO) 6 Eating occasions (6-EO) 3 Eating occasions (3-EO) 6 Eating occasions (6-EO)

Average

eating

occasion Total (sum)

Average

eating


Average

eating


Average

eating


Energycontent (kcal)

710 plusmn 30a 2130 plusmn 80b 352 plusmn 15c 2110 plusmn 90b 728 plusmn 28a 2180 plusmn 80b 360 plusmn 15b 2160 plusmn 90b

PRO (g) 26 plusmn 1a 79 plusmn 2b 13 plusmn 0c 78 plusmn 2b 46 plusmn 1d 139 plusmn 4e 23 plusmn 1a 137 plusmn 4e

CHO (g) 109 plusmn 6a 331 plusmn 15b 55 plusmn 3c 327 plusmn 15b 91 plusmn 4d 272 plusmn 13e 45 plusmn 2f 270 plusmn 13e

Fat (g) 21 plusmn 1a 63 plusmn 2b 10 plusmn 0c 62 plusmn 3b 21 plusmn 1a 64 plusmn 3b 11 plusmn 1c 63 plusmn 3b

Data presented as mean plusmn sem Different letters denote significance across rows significance P lt 005 repeated measures ANOVA within and between treatmentsEating occasion columns include the average for each of the eating occasions consumed during the testing day Total (sum) columns include the sum of all of the eatingoccasions consumed during the testing dayCHO carbohydrate PRO protein




ARTICLES


was estimated as resting energy expenditure times 10 activity factor usingthe Harris Benedict equation for men (20) For the 3-EO pattern energyintake was equally divided among all 3-EO provided every 4 h with280 ml of water provided with each eating occasion Tus each meal inthe 3-EO pattern contained one-third of the participantrsquos daily energyneeds During the 6-EO pattern energy intake was equally dividedamong all 6-EO provided every 2 h with 140 ml of water provided witheach eating occasion Tus each meal in the 6-EO pattern containedone-sixth of the participantrsquos daily energy needs Regardless of eatingfrequency the normal protein diet contained 14 protein (~08 g pro-teinkgday) 60 carbohydrate and 26 fat the higher protein dietcontained 25 protein (~14 g proteinkgday) 49 carbohydrate and

26 fat Te additional dietary protein in the higher protein diet wasprimarily from lean pork and egg products (25 and 15 of total pro-tein intake respectively) whereas the normal protein diet was void ofall striated tissue and eggs

Appetite questionnairesQuestionnaires assessing perceived hunger and satiety (fullness) werecompleted every 20 min throughout each trial using a 100-mm visualanalog scale presented in paper form Te visual analog scale had endanchors ranging from ldquonot at allrdquo to ldquoextremelyrdquo and included vali-dated appetite questions such as ldquoHow strong is your feeling of helliprightnowrdquo(21)

Perceived appetitea

b Perceived satiety

0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)

H u n g e r ( m m )

H u n g e r A U C

( times 1 0

3 ( m m middot

2 4 0 m i n ) )

Period II

H u n g e r A U C

( x 1 0

3 ( m m middot

2 4 0 m i n ) )

Period III

Period I Period II Period III

H u n g e r A U C (

x 1 0

3 ( m m middot

1 4 0 m i n ) )

NP HP 3-EO 6-EO NP HP 3-EO 6-EO NP HP 3-EO 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

0

10

20

30

40

50

60

70

80

90

100

0 60 120 180 240 300 360 420 480 540 600

Time (min)

F u l l n e s s ( m m )

0

10

20

30

40

50

60

70

80

90

100

0

2

4

6

8

10

12

F u l l n e s s A U C

( times 1 0

3 ( m m middot

2 4 0 m i n ) )


( times 1 0

3 ( m m middot

2 4 0 m i n ) )

3-EO vs 6-EO


3-EO vs 6-EO

NP vs HP

0

2

4

6

8

10

12

14

16

18

20

0

2

4

6

8

10

12

14

16

18

20


( times 1 0

3 ( m m middot

1 4 0 m i n ) )

0

2

4

6

8

10

12

14

16

18

20

0

2

4

6

8

10

12

0

2

4

6

8

10

12

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

Figure 1 Perceived appetite and satiety throughout the 11-h testing days following the dietary protein and eating frequency treatments Main effects

P lt 005 Period I time 0ndash240 min period II time 240ndash480 min period III time 480ndash620 min




ARTICLES


Hormonal responsesBlood samples were drawn into tubes containing EDA (ethylenedi-aminetetraacetic acid) every 20 min throughout each of the 11-h trialsSamples were centrifuged at minus4 degC for 15 min the plasma was sepa-rated and stored in microcentrifuge tubes at minus80 degC for future analysesProtease inhibitors (Pefabloc SC Roche Applied Science IndianapolisIN) were added to reduce protein degradation Plasma active ghrelinand total PYY were measured with 2-plex Milliplex assay kits andLuminex technologies (MilliporeLINCO Research St Charles MO)

Data and statistical analysiso assess perceived appetite (hunger) satiety (fullness) glucoseand hormonal responses total 11-h area under the curve (AUC) wascalculated from the fasting (baseline) time point and the 31 postprandial

time points for each outcome We further divided the testing day intothree segments period I time 0ndash240 min period II time 240ndash480 minand period III time 480ndash620 min and calculated individual AUCs foreach outcome with these periods With all AUC measurements the trap-ezoidal rule was utilized (22) Additionally pre- and postmeal appetitiveand hormonal peak responses were also identified for each eating occa-sion A two-factor repeated measures analysis of variance was utilizedto identify main effects of dietary protein eating frequency and interac-tions on all study outcomes Data are expressed as mean plusmn sem P lt 005was considered statistically significant Te sample size (n = 13) providedgt80 observed power to detect main effect differences among dietaryprotein and eating frequency treatments perceived hunger satiety andPYY concentrations Analyses were conducted using the StatisticalPackage for the Social Sciences (SPSS version 160 SPSS Chicago IL)

0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)

G l u c o s e ( m g d l )

G l u c o s e A U C ( times 1 0

3 ( m g d l middot 2 4 0 m i n ) )

Period II Period III


NP HP 3-EO 6-EO

80

100

120

140

160

180

200

a

0 60 120 180 240 300 360 420 480 540 600

Time (min)

I n s u

l i n ( p m o l l )

0

400

200

600

800

1200

1000

1400

b

Plasma glucose

Plasma insulin

0

5

10

15

20

25

30

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 1 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175


3 ( m g d l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

20

25

30


3 ( m g d l middot 1 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

20

25

303-EO vs 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

3-EO vs 6-EO

3-EO vs 6-EO

3-EO vs 6-EO

Figure 2 Plasma glucose and insulin responses throughout the 11-h testing days following the dietary protein and meal frequency treatments Main

effects P lt 005 Period I time 0ndash240 min period II time 240ndash480 min period III time 480ndash620 min




ARTICLES


RESULTS

As shown in Figures 1ndash3 the line graphs illustrate the appetitiveand hormonal responses completed every 20 min throughoutthe 11-h testing day whereas the bar graphs depict the AUCanalyses for periods I II and III of each testing day

Perceived appetite

Perceived hunger gradually declined throughout each of the 11-htesting days and exhibited eating-occasion oscillations with largerfluctuations observed following the 3-EO vs 6-EO (Figure 1a)

No protein times eating frequency interactions or main effects of die-tary protein and eating frequency were observed for total (11 h)perceived hunger AUC (Table 3) When examining the dataaccording to specific time periods across the day (ie periods III III) no main effects or interactions for perceived appetite weredetected (Figure 1a) Although the overall hunger responses werenot different between protein and eating frequency treatmentsthe average premeal hunger peak prior to each eating occasionwas greater in 3-EO (54 plusmn 6 mm) vs 6-EO (47 plusmn 6 mm P lt 001)with no difference with respect to dietary protein

0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)

G h r e l i n - c h a n g e f r o m b a s e l i n e ( p g m

l )



NP HP 3-EO 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

ndash10

ndash5

0

5

10

15

20

25

30

35

40

a

0 60 120 180 240 300 360 420 480 540 600

Time (min)

P Y Y - c h a n g e f r o m b

a s e l i n e ( p g m l )

0

15

10

5

20

25

35

30

40

45

50

b

Active ghrelin

Total PYY

0

5

10

15

NP HP 3-EO 6-EO0

5

10

15

P Y Y A U C

( times 1 0 3 ( p g m l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO NP HP 3-EO 6-EO0

5

10

15

20

25

P Y Y A U C


0

5

10

15

20

25

NP HP 3-EO 6-EO P Y Y A U C


0

5

10

15

20

25

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 1 4 0 m i n ) )

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP vs HP

NP vs HP

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

NP vs HPNP vs HP

NP vs HP

3-EO vs 6-EO3-EO vs 6-EO

3-EO vs 6-EO

Figure 3 Plasma active ghrelin and total PYY responses throughout the 11-h testing days following the dietary protein and meal frequency

treatments Main effects P lt 005 Period I time 0ndash240 min period II time 240ndash480 min period III time 480ndash620 min




ARTICLES


Perceived satiety

Perceived fullness gradually increased throughout each of the11-h testing days and exhibited eating-occasion oscillations

with larger fluctuations observed following the 3-EO vs 6-EO(Figure 1b) No protein times eating frequency interactions wereobserved for total (11 h) fullness AUC Subsequently main effectsof dietary protein (P lt 005) and eating frequency (P lt 005) wereobserved for total (11 h) fullness AUC (Table 3) With both eat-ing frequency patterns combined the higher protein diet led to a6 increase in 11-h fullness AUC vs normal protein (P lt 005)(Table 3) Alternately when combining the higher protein andnormal protein diets the 6-EO pattern led to a 10 reduction in11-h fullness AUC vs 3-EO pattern (P lt 005) (Table 3) Similarmain effects and post hoc comparison were also observed whenexamining the data according to specific time periods across the

day (ie periods I II III) (Figure 1b) Additionally the aver-age postmeal fullness peak was greater in higher protein (87 plusmn35 mm) vs normal protein (83 plusmn 4 mm P lt 001) but smaller in6-EO (79 plusmn 5 mm) vs 3-EO (90 plusmn 3 mm P lt 001)

Glucose

Eating-relating oscillations in plasma glucose concentrationswere observed following each eating occasion with larger fluc-tuations observed following the 3-EO vs 6-EO (Figure 2a) Noprotein times eating frequency interactions were observed for total(11 h) glucose AUC With respect to main effects although nodifference in total (11 h) glucose AUC was observed betweennormal protein vs higher protein a main effect of eating fre-quency (P lt 005) was identified (Table 3) Independent of die-tary protein 6-EO led to a 4 reduction in 11-h glucose AUC vs 3-EO (Table 3) When separating the 11-h testing day intoperiods the main effect of eating frequency was only observedduring the middle segment (period II) (Figure 2a)

Insulin

Eating-relating oscillations in plasma insulin concentrationswere observed following each eating occasion with larger fluc-tuations observed following the 3-EO vs 6-EO (Figure 2b)No protein times eating frequency interactions were observed fortotal (11 h) insulin AUC Although no difference in total (11 h)

insulin AUC was observed between normal protein vs higherprotein a main effect of eating frequency (P lt 005) was identi-fied (Table 3) Independent of dietary protein 6-EO led to 20

reduction in 11-h insulin vs 3-EO (Table 3) Main effect ofeating frequency was observed during periods I II and III (allP lt 005) (Figure 2b) Tere was no effect of dietary proteinwithin any of the time periods (Figure 2b)

Active ghrelin

Eating-relating oscillations in plasma ghrelin concentrationswere observed within 3-EO but not 6-EO (Figure 3a) No pro-tein times eating frequency interactions were observed for total11-h ghrelin AUC Although no difference in total (11 h) ghre-lin AUC was observed between 3-EO vs 6-EO a main effect ofdietary protein (P lt 005) was identified (Table 3) With both

eating frequencies combined higher protein diet led to 44increase in 11-h ghrelin AUC vs normal protein diet (P lt 005)(Table 3) When separating the 11-h testing day into periodsthe main effect of dietary protein was observed during periodsIIndashIII (P lt 005) (Figure 3a) Te average premeal ghrelin peakwas greater in higher protein (352 plusmn 44 pgml) vs normalprotein (254 plusmn 40 pgml P lt 005) treatments with no differ-ences occurring between eating frequency patterns

Total PYY

Gradual eating-relating oscillations in plasma PYY concentra-tions were observed following each eating occasion with largerfluctuations observed following the 3-EO vs 6-EO (Figure 3b)No protein times eating frequency interactions were observed fortotal (11 h) PYY AUC Main effects of dietary protein (P lt 005)and eating frequency (P lt 005) were observed for total (11 h)PYY AUC (Table 3) With both eating frequency patterns com-bined higher protein diet led to a 20 increase in 11-h PYYAUC vs normal protein (P lt 005) (Table 3) Alternately whencombining the higher protein and normal protein diets 6-EOled to a 9 reduction in 11-h PYY AUC vs 3-EO (P lt 005)(Table 3) Similar main effects in PYY were observed whenexamined according to specific time periods across the day(ie periods I II III) (Figure 3b) Te average postmeal PYYpeak was greater in higher protein (608 plusmn 61 pgml) vs normal

Table 3 Total area under the curve (AUC) assessments for the appetitive and hormonal responses following each study treatment

in 13 overweight and obese men

Outcomes NP 3-EO NP 6-EO HP 3-EO HP 6-EO

Perceived sensations

Hunger (times103 (mmmiddot620 min)) 153 plusmn 36 178 plusmn 71 135 plusmn 27 162 plusmn 39

Fullness (times103 (mmmiddot620 min))ab 429 plusmn 37 386 plusmn 36 450 plusmn 30 410 plusmn 35

Plasma glucose (times103 (mgdlmiddot620 min))b 684 plusmn 279 676 plusmn 343 691 plusmn 264 648 plusmn 232

Hormonal responses

Insulin (times103 (pmollmiddot620 min))b 248 plusmn 47 205 plusmn 38 250 plusmn 56c 191 plusmn 36

Ghrelin (times103 (pgmlmiddot620 min))a 133 plusmn 25 146 plusmn 32 199 plusmn 30 203 plusmn 31

PYY (times103 (pgmlmiddot620 min))ab 351 plusmn 33 325 plusmn 38 426 plusmn 36 385 plusmn 35

Data expressed as mean plusmn semNP normal protein PYY peptide YY 3-EO 3 eating occasions 6-EO 6 eating occasionsaMain effect of protein P lt 005 bMain effect of eating occasion P lt 005




ARTICLES


protein (508 plusmn 6 pgml P lt 0001) but not different betweeneating frequency treatments

DISCUSSION

We sought to provide scientific evidence regarding the effectsof higher protein intake and greater eating frequency on per-

ceived appetite and hormonal responses in overweight andobese men Dietary protein and eating frequency were shownto have no effect on perceived hunger and led to inconsist-ent andor conflicting glucose insulin and ghrelin responsesHowever both of these dietary factors significantly altered sati-ety Whereas higher protein intake increased daily perceivedfullness frequent eating led to reductions in daily perceivedfullness Tese findings were further supported by the elevatedPYY concentrations observed with higher vs normal proteinintake and by the reduced PYY concentrations observed withfrequent vs infrequent eating Tese data strengthen the cur-rent literature indicating that increased dietary protein leadsto increased satiety refute the long-standing assumption that

increased eating frequency has beneficial effects and suggestthat overweight and obese men might achieve better appetitecontrol by consuming three higher protein meals per day

Tere is convincing evidence that higher protein consump-tion at single meals and during longer-term dietary interven-tions leads to increased perceived satiety (6) Many of thestudies confirming these findings focused on single mealswith large amounts and proportions of dietary protein (ie80ndash100 of the meal) (56) Several recent tightly-controlledrespiratory chamber studies have tracked appetitive sensationswhile administering higher protein diets (~30 of intake asdietary protein) over an entire day of eating In two specific

studies participants consumed breakfast lunch and dinnermeals containing either 10 or 30 of total energy intake asdietary protein Te 30 protein diets led to reduced overallhunger and greater overall satiety compared to the 10 proteindiets (P lt 005) (2324) Our current study further supports thesatiating properties of dietary protein when consumed at thisquantity but shows very little if any influence on hunger

One potential mechanism contributing to the reported sati-ety-enhancing and hunger-suppressing properties of dietaryprotein may involve hormonal responses to specific macronu-trients (9) Several researchers report that meals andor dietscontaining increased dietary protein lead to initial and sus-tained increases in postprandial PYY concentrations along withreductions in postprandial ghrelin concentrations (91325) Inour current study overall PYY concentrations were greaterfollowing the higher vs normal protein diet a finding thatis consistent with the current literature However the higherghrelin concentrations following the higher vs normal proteindiet are not consistent with the perceived hunger responses inthis study nor the ghrelin responses observed in our previousstudy (9) Te disparate findings between our two studies maybe attributable to the gender andor energy state differences ofthe participants In our previous study overweight and obesewomen consumed an energy restriction weight loss dietwhereas the current study was performed in overweight and

obese men who consumed a eucaloric diet Further research isneeded to identify whether gender and energy state differencesin appetite control exist with respect to how dietary protein isperceived and which mechanisms are altered

Although many of the protein studies incorporate similarquantities of protein the eating frequency studies have a myr-

iad of experimental design approaches making it challengingto develop an overall conclusion regarding the influence of eat-ing frequency on appetite control and food intake For exampleof the studies that compare frequent eating occasions (ie gt3occasions) several only include part of the day by comparingthe influence of a single breakfast meal vs dividing the energyintake into 5-EO consumed every hour over the course of themorning (18) Tus it is difficult to ascertain whether the dif-ferences in appetite control would be maintained throughout anentire day Of those that monitor appetitive responses and foodintake throughout an entire day (10ndash24 h) several incorporateeating frequencies beyond what could practically be followedin daily living (ie eating frequency of 12ndash17 eating occasions

day eating every 30ndash40 min) (2627) Te experimental designsof these studies limit the ability to develop feasible recommen-dations for better weight management Regardless of these

varying experimental designs very little if any differenceshave been observed with perceived hunger or satiety hormonalresponses or subsequent food intake when comparing single(or few) vs multiple eating occasions Besides the current studyonly one other study has examined the effect of providing 6-EO(eating every 2 h) vs 2-EO (eating every 8 h) Te study indi-rectly accessed appetite control by incorporating an ad libitum feeding regiment throughout the evening (15) No differencein evening andor daily energy intake was observed between

the 6-EO vs 2-EO (15) Over the past 10 years many adultAmericans have transitioned from the typical ldquothree-mealsdayrdquo dietary pattern to eating more frequently throughout thedaymdasheating ~43 timesday (26) Based on the current and previous evidence-based studies the overall findings suggest thateating beyond the typical three mealsday pattern does not leadto better appetite control in overweight and obese individuals

Although appetite control as assessed through perceived hun-ger satiety PYY and ghrelin responses was negatively alteredwith greater eating frequency frequent eating led to reduced glu-cose and insulin responses throughout the day Tese findingssuggest that overweight and obese adults who typically exhibita higher risk for type 2 diabetes and metabolic syndrome mayexperience improved glycemic control potentially reducing therisk for diabetes cardiovascular disease and additional weightgain when smaller more frequent meals are consumed (28)

Limitations

Te current study did not include any acclimation days to thedifferent eating patterns or protein intakes Tus it is unclearas to whether any habitualization to these treatments wouldhave led to differential responses Additionally this was anacute study with only four testing days and no follow-up ordocumentation regarding any changes in subsequent dailyenergy intake Although these findings are a relevant step to




ARTICLES


identify the influence of these dietary factors further researchinvolving a long-term intervention is necessary to confirm thepresent findings document changes in chronic food intakeand to identify the long-term implications for appetite controlenergy regulation and body weight

In summary the findings that higher protein intake and

lower eating frequency independently promote daily per-ceived satiety in conjunction with comparable differences inthe satiety hormone PYY suggest that overweight and obesemen might achieve better appetite control by consuming threehigher protein meals per day

ACKNOWLEDGMENTS

The authors thank the study participants for their dedication and compliance

during the testing days Trent Wisehart Carmen Martin Matt Greiser Laura

Hass and Amanda Sands for their efforts in performing the testing day

procedures sample processing and data entry Janice Green for preparing

all study foods Arthur Rosen MD who provided medical coverage and

Doug Maish EMT-P who performed all catheter insertions and provided

clinical laboratory services This study was funded by the National Pork

Board and the American Egg BoardmdashEgg Nutrition Center with additional

support provided by the Purdue University Ingestive Behavior Research

Center (postdoctoral fellowship to HJL) and the NIH-sponsored Building

Interdisciplinary Research Careers in Womenrsquos Health (BIRCWH) NIH-5

K12 HD052027-04

DISCLOSURE

The authors declared no conflict of interest

copy 2010 The Obesity Society

REFERENCES1 Ogden CL Carroll MD Curtin LR et al Prevalence of overweight and obesity

in the United States 1999-2004 JAMA 20062951549ndash1555

2 Wang Y Beydoun MA Liang L Caballero B Kumanyika SK Will all

Americans become overweight or obese estimating the progression

and cost of the US obesity epidemic Obesity (Silver Spring) 200816

2323ndash2330

3 httpwwwgooglecomsearchhl=enampq=6+meals+and+high+protein+for+

weight+loss Eat 6 meals a day with increased protein 2009

4 Dietary Reference Intakes for Energy Carbohydrate Fiber Fat Fatty Acids

Cholesterol Protein and Amino Acids Washington DC National Academy

Press 2002

5 Halton TL Hu FB The effects of high protein diets on thermogenesis

satiety and weight loss a critical review J Am Coll Nutr 200423

373ndash385

6 Westerterp-Plantenga MS Nieuwenhuizen A Tomeacute D Soenen S

Westerterp KR Dietary protein weight loss and weight maintenance

Annu Rev Nutr 20092921ndash41

7 Layman DK Evans E Baum JI et al Dietary protein and exercise have

additive effects on body composition during weight loss in adult women

J Nutr 20051351903ndash1910

8 Leidy HJ Carnell NS Mattes RD Campbell WW Higher protein intakepreserves lean mass and satiety with weight loss in pre-obese and obese

women Obesity (Silver Spring) 200715421ndash429

9 Leidy HJ Mattes RD Campbell WW Effects of acute and chronic protein

intake on metabolism appetite and ghrelin during weight loss Obesity

(Silver Spring) 2007151215ndash1225

10 Veldhorst M Smeets A Soenen S et al Protein-induced satiety effects

and mechanisms of different proteins Physiol Behav 200894300ndash307

11 Smeets AJ Soenen S Luscombe-Marsh ND Ueland Oslash Westerterp-

Plantenga MS Energy expenditure satiety and plasma ghrelin glucagon-

like peptide 1 and peptide tyrosine-tyrosine concentrations following a

single high-protein lunch J Nutr 2008138698ndash702

12 Leidy HJ Bossingham MJ Mattes RD Campbell WW Increased dietary

protein consumed at breakfast leads to an initial and sustained feeling

of fullness during energy restriction compared to other meal times

Br J Nutr 2009101798ndash803

13 Batterham RL Heffron H Kapoor S et al Critical role for peptide YY

in protein-mediated satiation and body-weight regulation Cell Metab

20064223ndash233

14 Bellisle F McDevitt R Prentice AM Meal frequency and energy balance

Br J Nutr 199777 Suppl 1S57ndashS70

15 Taylor MA Garrow JS Compared with nibbling neither gorging nor a

morning fast affect short-term energy balance in obese patients in a

chamber calorimeter Int J Obes Relat Metab Disord 200125519ndash528

16 Smeets AJ Westerterp-Plantenga MS Acute effects on metabolism and

appetite profile of one meal difference in the lower range of meal frequency


17 Jackson SJ Leahy FE Jebb SA et al Frequent feeding delays the gastric

emptying of a subsequent meal Appetite 200748199ndash205

18 Speechly DP Rogers GG Buffenstein R Acute appetite reduction

associated with an increased frequency of eating in obese males Int J Obes

Relat Metab Disord 1999231151ndash1159

19 Stote KS Baer DJ Spears K et al A controlled trial of reduced meal

frequency without caloric restriction in healthy normal-weight middle-aged

adults Am J Clin Nutr 200785981ndash988

20 Harris JL Bargh JA Television viewing and unhealthy diet implications for

children and media interventions Health Commun 200924660ndash673

21 Hill AJ Blundell JE Nutrients and behaviour research strategies for the

investigation of taste characteristics food preferences hunger sensations

and eating patterns in man J Psychiatr Res 198217203ndash212

22 Wolever TM Bolognesi C Prediction of glucose and insulin responses of

normal subjects after consuming mixed meals varying in energy protein fat

carbohydrate and glycemic index J Nutr 19961262807ndash2812

23 Lejeune MP Westerterp KR Adam TC Luscombe-Marsh ND Westerterp-

Plantenga MS Ghrelin and glucagon-like peptide 1 concentrations 24-h

satiety and energy and substrate metabolism during a high-protein diet and

measured in a respiration chamber Am J Clin Nutr 20068389ndash94

24 Westerterp-Plantenga MS Lejeune MP Smeets AJ Luscombe-Marsh ND

Sex differences in energy homeostatis following a diet relatively high in

protein exchanged with carbohydrate assessed in a respiration chamber in

humans Physiol Behav 200997414ndash419

25 Diepvens K Haumlberer D Westerterp-Plantenga M Different proteins and

biopeptides differently affect satiety and anorexigenicorexigenic hormones

in healthy humans Int J Obes (Lond) 200832510ndash518

26 Solomon TP Chambers ES Jeukendrup AE Toogood AA Blannin AK

The effect of feeding frequency on insulin and ghrelin responses in human

subjects Br J Nutr 2008100810ndash819

27 Jenkins DJ Wolever TM Vuksan V et al Nibbling versus gorging metabolic

advantages of increased meal frequency N Engl J Med 1989321

929ndash934

28 Bloomgarden ZT Approaches to treatment of pre-diabetes and obesityand promising new approaches to type 2 diabetes Diabetes Care

2008311461ndash1466




ARTICLES


equation by examining the impact of eating frequency onappetite control and food intake In some (1517) but not all(161819) studies greater eating frequency has led to reducedhunger increased satiety and decreased food intake (15ndash19)Te discrepant findings may stem from the wide range of eat-ing frequencies that have been arbitrarily defined as frequent

eating when consisting of 4ndash17 eating occasionsday and infre-quent eating when consisting of one to three mealsdayAlthough the overall message in the mainstream media

proposes an ldquoeat six times a dayrdquo strategy for better appetitecontrol and food intake regulation very little if any scientificevidence exists to evaluate the efficacy of this approach Tusa second aim of this study was to compare the effects of eatingthree timesday which has been the standard dietary pattern inthe past vs six timesday on these outcomes Tis study designalso permitted investigation of a possible synergistic effect ofhigher protein intake and greater eating frequency on per-ceived appetite and hormonal responses throughout the day

METHODS AND PROCEDURES

SubjectsPotential participants were recruited through newspaper advertise-ments Eligibility was based on the following criteria (i) men agege21 years (ii) BMI 250ndash349 kgm2 (iii) percent body fat gt25assessed through skinfold measurements (iv) not dieting and noweight loss or gain (ge45 kg) within the past 6 months (v) nonsmok-ing (vi) nondiabetic (vii) clinically normal blood profiles (normal liver

and kidney function fasting blood glucose lt110 mgdl) (viii) consist-ent habitual activity patterns over the past 3 months and (ix) habitualdietary pattern of consuming three mealsday for the past 3 monthswenty-five men were screened 21 gave informed consent 16 beganand 13 completed all study procedures Reasons for the three dropoutswere military duty relocation and nonstudy compliance Participantssigned an informed consent form approved by the Purdue UniversityBiomedical Institutional Review Board and received monetary com-

pensation for completing all study procedures Clinical testing occurredbetween January 2008 and July 2008 Subject characteristics for thecompleted participants are displayed in Table 1

Experimental designTis study incorporated a randomized crossover design consisting offour 11-h trials On separate days the participants consumed eucaloricdiets containing either normal protein (79 plusmn 2 g proteinday 08 g kgday) or higher protein (138 plusmn 3 g proteinday 14 gkgday) equallydivided among three eating occasions (3-EO provided every 4 h) orsix eating occasions (6-EO provided every 2 h) in a randomized orderPre- and postprandial hunger satiety plasma glucose and hormonalresponses (plasma insulin ghrelin and PYY) were assessed throughouteach 11-h trial

Specific testing day proceduresOn the evening prior to each trial participants were provided with astandardized normal protein dinner to be consumed at home between5 and 7 983152983149 Te participants then fasted until their arrival at the labo-ratory between 7 and 8 983137983149 the following morning Upon arrival theparticipants were placed in a supine position on a bed and a catheterwas inserted in an antecubetal vein of the nondominant arm and keptpatent for the remainder of the testing period by saline drip For the next30 min the participants acclimated to the room and were familiarizedwith the testing day procedures At time 0 a baseline (fasting) bloodsample was taken questionnaires were completed and the first eatingoccasion was provided to the participants Over the remaining 11 hblood sampling and questionnaires were repeated every 20 min Teremaining eating occasions were provided to the participants at set timesand in specific quantities according to the treatment randomization

For each eating occasion the participants were required to consume allfoods and water provided to them within 15 min No additional foodor drink was provided to the participants During the testing periodparticipants remained in a semi-supine position and were permittedto watch television read or use computers At the end of the 11 h thecatheter was removed and the participants were permitted to leave thelaboratory Tere were 1ndash2 weeks between each of the four trials

Eating occasionsTe characteristics of the diets are shown in Table 2 Te participantswere fed according to their daily energy needs Due to the reducedactivity of the volunteers during the 11-h testing days daily energy need

Table 1 Subject characteristics of 13 overweight and obese

men

Subject characteristics Mean plusmn sem

Age (year) 51 plusmn 4

Height (cm) 178 plusmn 2

Weight (kg) 996 plusmn 24

BMI (kgm2 ) 313 plusmn 08

Body fat () 31 plusmn 3

Fasting glucose (mgdl) 97 plusmn 1

Fasting insulin (pmoll) 75 plusmn 16

Habitual meal pattern ( mealsday) 29 plusmn 03

Data expressed as mean plusmn sem

Table 2 Dietary characteristics of the test day diets

Dietary

characteristics

Normal protein testing day Higher protein testing day

3 Eating occasions (3-EO) 6 Eating occasions (6-EO) 3 Eating occasions (3-EO) 6 Eating occasions (6-EO)

Average

eating


Average

eating


Average

eating


Average

eating


Energycontent (kcal)

710 plusmn 30a 2130 plusmn 80b 352 plusmn 15c 2110 plusmn 90b 728 plusmn 28a 2180 plusmn 80b 360 plusmn 15b 2160 plusmn 90b

PRO (g) 26 plusmn 1a 79 plusmn 2b 13 plusmn 0c 78 plusmn 2b 46 plusmn 1d 139 plusmn 4e 23 plusmn 1a 137 plusmn 4e

CHO (g) 109 plusmn 6a 331 plusmn 15b 55 plusmn 3c 327 plusmn 15b 91 plusmn 4d 272 plusmn 13e 45 plusmn 2f 270 plusmn 13e

Fat (g) 21 plusmn 1a 63 plusmn 2b 10 plusmn 0c 62 plusmn 3b 21 plusmn 1a 64 plusmn 3b 11 plusmn 1c 63 plusmn 3b

Data presented as mean plusmn sem Different letters denote significance across rows significance P lt 005 repeated measures ANOVA within and between treatmentsEating occasion columns include the average for each of the eating occasions consumed during the testing day Total (sum) columns include the sum of all of the eatingoccasions consumed during the testing dayCHO carbohydrate PRO protein




ARTICLES





Perceived appetitea

b Perceived satiety

0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)

H u n g e r ( m m )

H u n g e r A U C

( times 1 0

3 ( m m middot

2 4 0 m i n ) )

Period II

H u n g e r A U C

( x 1 0

3 ( m m middot

2 4 0 m i n ) )

Period III


H u n g e r A U C (

x 1 0

3 ( m m middot

1 4 0 m i n ) )


NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

0

10

20

30

40

50

60

70

80

90

100

0 60 120 180 240 300 360 420 480 540 600

Time (min)


0

10

20

30

40

50

60

70

80

90

100

0

2

4

6

8

10

12


( times 1 0

3 ( m m middot

2 4 0 m i n ) )


( times 1 0

3 ( m m middot

2 4 0 m i n ) )

3-EO vs 6-EO


3-EO vs 6-EO

NP vs HP

0

2

4

6

8

10

12

14

16

18

20

0

2

4

6

8

10

12

14

16

18

20


( times 1 0

3 ( m m middot

1 4 0 m i n ) )

0

2

4

6

8

10

12

14

16

18

20

0

2

4

6

8

10

12

0

2

4

6

8

10

12

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO






ARTICLES





0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)



3 ( m g d l middot 2 4 0 m i n ) )



NP HP 3-EO 6-EO

80

100

120

140

160

180

200

a

0 60 120 180 240 300 360 420 480 540 600

Time (min)

I n s u

l i n ( p m o l l )

0

400

200

600

800

1200

1000

1400

b

Plasma glucose

Plasma insulin

0

5

10

15

20

25

30

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 1 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175


3 ( m g d l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

20

25

30


3 ( m g d l middot 1 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

20

25

303-EO vs 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

3-EO vs 6-EO

3-EO vs 6-EO

3-EO vs 6-EO






ARTICLES


RESULTS


Perceived appetite



0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)


l )



NP HP 3-EO 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

ndash10

ndash5

0

5

10

15

20

25

30

35

40

a

0 60 120 180 240 300 360 420 480 540 600

Time (min)



0

15

10

5

20

25

35

30

40

45

50

b

Active ghrelin

Total PYY

0

5

10

15

NP HP 3-EO 6-EO0

5

10

15

P Y Y A U C



5

10

15

20

25

P Y Y A U C


0

5

10

15

20

25



0

5

10

15

20

25

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 1 4 0 m i n ) )

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP vs HP

NP vs HP

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

NP vs HPNP vs HP

NP vs HP


3-EO vs 6-EO






ARTICLES


Perceived satiety




Glucose


Insulin




Active ghrelin



Total PYY









Hormonal responses








ARTICLES



DISCUSSION














Limitations





ARTICLES





ACKNOWLEDGMENTS












K12 HD052027-04

DISCLOSURE








2323ndash2330





Press 2002



373ndash385






J Nutr 20051351903ndash1910


















20064223ndash233









































929ndash934


2008311461ndash1466




ARTICLES





Perceived appetitea

b Perceived satiety

0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)

H u n g e r ( m m )

H u n g e r A U C

( times 1 0

3 ( m m middot

2 4 0 m i n ) )

Period II

H u n g e r A U C

( x 1 0

3 ( m m middot

2 4 0 m i n ) )

Period III


H u n g e r A U C (

x 1 0

3 ( m m middot

1 4 0 m i n ) )


NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

0

10

20

30

40

50

60

70

80

90

100

0 60 120 180 240 300 360 420 480 540 600

Time (min)


0

10

20

30

40

50

60

70

80

90

100

0

2

4

6

8

10

12


( times 1 0

3 ( m m middot

2 4 0 m i n ) )


( times 1 0

3 ( m m middot

2 4 0 m i n ) )

3-EO vs 6-EO


3-EO vs 6-EO

NP vs HP

0

2

4

6

8

10

12

14

16

18

20

0

2

4

6

8

10

12

14

16

18

20


( times 1 0

3 ( m m middot

1 4 0 m i n ) )

0

2

4

6

8

10

12

14

16

18

20

0

2

4

6

8

10

12

0

2

4

6

8

10

12

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO






ARTICLES





0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)



3 ( m g d l middot 2 4 0 m i n ) )



NP HP 3-EO 6-EO

80

100

120

140

160

180

200

a

0 60 120 180 240 300 360 420 480 540 600

Time (min)

I n s u

l i n ( p m o l l )

0

400

200

600

800

1200

1000

1400

b

Plasma glucose

Plasma insulin

0

5

10

15

20

25

30

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 1 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175


3 ( m g d l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

20

25

30


3 ( m g d l middot 1 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

20

25

303-EO vs 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

3-EO vs 6-EO

3-EO vs 6-EO

3-EO vs 6-EO






ARTICLES


RESULTS


Perceived appetite



0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)


l )



NP HP 3-EO 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

ndash10

ndash5

0

5

10

15

20

25

30

35

40

a

0 60 120 180 240 300 360 420 480 540 600

Time (min)



0

15

10

5

20

25

35

30

40

45

50

b

Active ghrelin

Total PYY

0

5

10

15

NP HP 3-EO 6-EO0

5

10

15

P Y Y A U C



5

10

15

20

25

P Y Y A U C


0

5

10

15

20

25



0

5

10

15

20

25

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 1 4 0 m i n ) )

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP vs HP

NP vs HP

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

NP vs HPNP vs HP

NP vs HP


3-EO vs 6-EO






ARTICLES


Perceived satiety




Glucose


Insulin




Active ghrelin



Total PYY









Hormonal responses








ARTICLES



DISCUSSION














Limitations





ARTICLES





ACKNOWLEDGMENTS












K12 HD052027-04

DISCLOSURE








2323ndash2330





Press 2002



373ndash385






J Nutr 20051351903ndash1910


















20064223ndash233









































929ndash934


2008311461ndash1466




ARTICLES





0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)



3 ( m g d l middot 2 4 0 m i n ) )



NP HP 3-EO 6-EO

80

100

120

140

160

180

200

a

0 60 120 180 240 300 360 420 480 540 600

Time (min)

I n s u

l i n ( p m o l l )

0

400

200

600

800

1200

1000

1400

b

Plasma glucose

Plasma insulin

0

5

10

15

20

25

30

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175

I n s u l i n A U C

( times 1 0

3 ( p m o l l middot 1 4 0 m i n ) )

NP HP 3-EO 6-EO0

50

25

75

100

125

150

175


3 ( m g d l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

20

25

30


3 ( m g d l middot 1 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

20

25

303-EO vs 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

3-EO vs 6-EO

3-EO vs 6-EO

3-EO vs 6-EO






ARTICLES


RESULTS


Perceived appetite



0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)


l )



NP HP 3-EO 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

ndash10

ndash5

0

5

10

15

20

25

30

35

40

a

0 60 120 180 240 300 360 420 480 540 600

Time (min)



0

15

10

5

20

25

35

30

40

45

50

b

Active ghrelin

Total PYY

0

5

10

15

NP HP 3-EO 6-EO0

5

10

15

P Y Y A U C



5

10

15

20

25

P Y Y A U C


0

5

10

15

20

25



0

5

10

15

20

25

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 1 4 0 m i n ) )

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP vs HP

NP vs HP

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

NP vs HPNP vs HP

NP vs HP


3-EO vs 6-EO






ARTICLES


Perceived satiety




Glucose


Insulin




Active ghrelin



Total PYY









Hormonal responses








ARTICLES



DISCUSSION














Limitations





ARTICLES





ACKNOWLEDGMENTS












K12 HD052027-04

DISCLOSURE








2323ndash2330





Press 2002



373ndash385






J Nutr 20051351903ndash1910


















20064223ndash233









































929ndash934


2008311461ndash1466




ARTICLES


RESULTS


Perceived appetite



0 60 120 180 240 300 360 420 480 540 600

Period I

Time (min)


l )



NP HP 3-EO 6-EO

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

ndash10

ndash5

0

5

10

15

20

25

30

35

40

a

0 60 120 180 240 300 360 420 480 540 600

Time (min)



0

15

10

5

20

25

35

30

40

45

50

b

Active ghrelin

Total PYY

0

5

10

15

NP HP 3-EO 6-EO0

5

10

15

P Y Y A U C



5

10

15

20

25

P Y Y A U C


0

5

10

15

20

25



0

5

10

15

20

25

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP HP 3-EO 6-EO0

5

10

15

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 1 4 0 m i n ) )

G h r e l i n A U C

( times 1 0

3 ( p g m l middot 2 4 0 m i n ) )

NP vs HP

NP vs HP

NPndash3-EO

NPndash6-EO

HPndash3-EO

HPndash6-EO

NP vs HPNP vs HP

NP vs HP


3-EO vs 6-EO






ARTICLES


Perceived satiety




Glucose


Insulin




Active ghrelin



Total PYY









Hormonal responses








ARTICLES



DISCUSSION














Limitations





ARTICLES





ACKNOWLEDGMENTS












K12 HD052027-04

DISCLOSURE








2323ndash2330





Press 2002



373ndash385






J Nutr 20051351903ndash1910


















20064223ndash233









































929ndash934


2008311461ndash1466




ARTICLES


Perceived satiety




Glucose


Insulin




Active ghrelin



Total PYY









Hormonal responses








ARTICLES



DISCUSSION














Limitations





ARTICLES





ACKNOWLEDGMENTS












K12 HD052027-04

DISCLOSURE








2323ndash2330





Press 2002



373ndash385






J Nutr 20051351903ndash1910


















20064223ndash233









































929ndash934


2008311461ndash1466




ARTICLES



DISCUSSION














Limitations





ARTICLES





ACKNOWLEDGMENTS












K12 HD052027-04

DISCLOSURE








2323ndash2330





Press 2002



373ndash385






J Nutr 20051351903ndash1910


















20064223ndash233









































929ndash934


2008311461ndash1466




ARTICLES





ACKNOWLEDGMENTS












K12 HD052027-04

DISCLOSURE








2323ndash2330





Press 2002



373ndash385






J Nutr 20051351903ndash1910


















20064223ndash233









































929ndash934


2008311461ndash1466

Efecto de Las Modificaciones de La Dieta

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