1-s2.0-s0031938413001479-main

Upload: ale-rohmad

Post on 03-Apr-2018

222 views

Category:

Documents


0 download

TRANSCRIPT

  • 7/28/2019 1-s2.0-S0031938413001479-main

    1/8

    UNCORRE

    CTEDPR

    OOF

    1 Effect of skipping breakfast on subsequent energy intake

    2 David A. Levitsky , Carly R. Paconowski

    3 Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853, United States

    4

    5

    a b s t r a c ta r t i c l e i n f o

    6 Article history:

    7 Received 14 November 2012

    8 Accepted 3 May 2013

    9 Available online xxxx

    101112

    13 Keywords:

    14 Skipping breakfast

    15 Control of energy intake

    16 Energetic compensation

    17 Weight control

    18 Obesity

    19The objective was to examine the effect of consuming breakfast on subsequent energy intake.

    20Participants who habitually ate breakfast and those who skipped breakfast were recruited for two studies.

    21Using a randomized crossover design, the first study, examined the effect of having participants consume

    22either (a) no breakfast, (b) a high carbohydrate breakfast (335 kcals) or (c) a high fiber breakfast (360) kcals23on three occasions and measured ad libitum intake at lunch. The second study again used a randomized cross-

    24over design but with a larger, normal carbohydrate, breakfast consumed ad libtum. Intake averaged 624 kcals

    25and subsequent food intake was measured throughout the day. Participants ate only foods served from the

    26Cornell Human Metabolic Research Unit where all foods were weighed before and after consumption.

    27In the first study, neither eating breakfast nor the kind of breakfast consumed had an effect on the amount

    28consumed at lunch despite a reduction in hunger ratings. In thesecond study,intake at lunch as well as hunger

    29ratings was significantly increasedafter skipping breakfast, by 144 kcal,leaving a net caloric deficitof 408 kcal

    30by the end of the day. These data are consistent with published literature demonstrating that skipping a meal

    31does not result in accurate energy compensation at subsequent meals and suggests that skipping breakfast

    32may be an effective means to reduce daily energy intake in some adults.

    33 2013 Published by Elsevier Inc.

    3435

    36

    37

    38 1. Introduction

    39 Despite many scientific publications demonstrating nutritional

    40 benefits of eating breakfast [1,34,55,58,64,65,69,73,80,81,85], skip-

    41 ping breakfast is one of the first changes in feeding habits people

    42 make when they want to lose weight [8,1214,101,104]. About 25%

    43 of American adults report regularly not eating breakfast, a statistic

    44 that has increased from 14% observed in 1965 [37]. The major reason

    45 given for skipping breakfast is to control body weight [78,104].

    46 Skipping breakfast as a means of losing weight appears to contra-

    47 dict the scientific literature. Wyatt and colleagues found that one of

    48 the most consistent characteristics of people who were part of the

    49 National Weight Control Registry, a group of successful dieters who

    50 have maintained at least a 13.6 kg (30 lb) weight loss for one year

    51 or more, is that only 4% of the nearly 3000 participants reported

    52 that they skipped breakfast, [102] a frequency considerably lower

    53 than the 25% observed in the population [37].

    54 Scientific evidence supporting the contention that skipping break-

    55 fast is ineffective as a means of restricting energy intake is inferred

    56 from the frequently published observation that people who skip

    57 breakfast either have a higher Body Mass Index (BMI) or gain weight

    58 at a greater rate than people who regularly eat breakfast [24,6,7,

    59 9,10,12,13,15,16,18,2226,30,35,40,42,46,47,52,53,56,59,68,70,79,80,

    6082,87,89,90,93

    97,100], although there are reports where such rela-61tionships were not observed [1,30,31,54,76,83,86,98,99]. Despite

    62the preponderance of studies demonstrating the inverse relationship

    63between BMI and the frequency of eating breakfast, these observations

    64have been correlational. It is equally plausible to interpret these asso-

    65ciations as indicating that a high BMI causes one to skip breakfast as

    66it is to suggest that skipping breakfast causes an increased BMI. It is

    67also possible that breakfast eaters engage in other healthy behaviors,

    68such as reducing snacking, lowering total fat intake and engaging in

    69regular exercise, all of which will lead to a reduced BMI [38,102].

    70From this correlational evidence alone, we cannot conclude that eating

    71breakfast results in a reduced BMI or that skipping breakfast results in a

    72higher BMI.

    73To establish whether skipping breakfast results in an increase in

    74energy intake at succeeding meals to compensate for the lost energy

    75consumed at breakfast requires breakfast consumption to be experi-

    76mentally manipulated and its effects on resulting intake measured.

    77In one of the few studies that directly tests this idea, Kral and col-

    78leagues [57] demonstrated that when children skip breakfast, despite

    79increased hunger ratings, they do not compensate for the caloric def-

    80icit by eating more later in the day. To further investigate whether

    81skipping breakfast results in subsequent energetic compensation in

    82adults, the following two experimental studies were performed. The

    83first study examined the effect of skipping breakfast on the amount

    84consumed at lunch. The second study examined the effect of eating

    85a larger breakfast on the amount consumed at lunch and during the

    86rest of the day.

    Physiology & Behavior xxx (2013) xxxxxx

    Corresponding author at: 112 Savage Hall.

    E-mail address: [email protected] (D.A. Levitsky).

    PHB-10041; No of Pages 8

    0031-9384/$ see front matter 2013 Published by Elsevier Inc.

    http://dx.doi.org/10.1016/j.physbeh.2013.05.006

    Contents lists available at SciVerse ScienceDirect

    Physiology & Behavior

    j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / p h b

    Please cite this article as: Levitsky DA, Paconowski CR, Effect of skipping breakfast on subsequent energy intake, Physiol Behav (2013), http://dx.doi.org/10.1016/j.physbeh.2013.05.006

    http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006mailto:[email protected]://dx.doi.org/10.1016/j.physbeh.2013.05.006http://www.sciencedirect.com/science/journal/00319384http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://www.sciencedirect.com/science/journal/00319384http://dx.doi.org/10.1016/j.physbeh.2013.05.006mailto:[email protected]://dx.doi.org/10.1016/j.physbeh.2013.05.006
  • 7/28/2019 1-s2.0-S0031938413001479-main

    2/8

    UNCORRE

    CTEDPR

    OOF

    2. Study I

    2.1. Material and methods

    Participants were recruited from the undergraduate student

    population at Cornell University through posters and class announce-

    ments. The participants were told that the researchers were studying

    the cognitive effects of breakfast consumption. Volunteers were

    screened using a health questionnaire and the Stunkard Three FactorEating Questionnaire. From this pool, twenty-four participants were

    selected on the basis that (a) they exhibited low restraint scores

    (b15), (b) they did not have any aversions to the foods that would

    be served, (c) they were in good physical health (self-report), and

    (d) they did not take any medications. All participants were between

    18 and 23 years old (mean age of 21) with BMIs greater than 20 and

    less than 25. The study was approved by the Cornell Institutional

    Review Board.

    Participants were divided into three groups matched for age,

    restraint score, and gender. A randomized cross-over design was

    used. They were instructed to eat breakfast and lunch in the Cornell

    Human Metabolic Research Unit (HMRU) on three consecutive

    Wednesdays. They were instructed not to eat any food after 11:00 pm

    the night before and to arrive at the Unit between 7:45 and 9:20

    the next morning. According to which group the participants were

    assigned, they were given either (a) no breakfast, (b) a high carbohy-

    drate breakfast consisting of a plain bagel with1 tbs of strawberry or

    grape jelly and 1 cup of orange or apple juice, or (c) a high fiber break-

    fast consisting of 1 cup of Raisin Bran cereal with 1 cup of 1% milk. The

    energy content of the high carbohydrate breakfast was 335 kcals and

    the high fiber breakfast was 338 kcals. The nutrient composition of

    the two meals is provided in Table 1. The participants were asked to

    eat all the food given to them. At each testing session 1/3 of the partic-

    ipants received each of the three breakfasts. For each succeeding week,

    each group was rotated through the remaining treatments according

    to a balanced Latin square design.

    Participants were not permitted to eat anything between break-

    fast and lunch. One hour before lunch the participants, completed a

    6-point hunger rating scale. Lunch was served in the HMRU between11:30 am and 12:30 pm. When the participants arrived for lunch, they

    were given a 10 minute paper-and-pencil cognitive test to complete.

    Lunch was served from a buffet table (nutrient composition is

    presented in Table 2). The participants were instructed to eat as

    much or little as they wanted. After placing each food on separate

    paper plates, the participants carried the food to a weighing station

    where the investigators recorded the weight of each item. Data were

    recorded to the nearest gram. Just before eating, participants complet-

    ed a second hunger rating scale. After finishing the meal, the amount

    of food remaining on the plate was recorded. Energy values of the

    foods consumed were determined from standard food tables [50].

    134Amount consumed was the major dependent variable of interest.

    135Statistical analyses were performed on both the amount consumed (g)

    136and energy consumed (kcal). The results were identical.

    137Data were analyzed using a General Linear Model (GLM) with re-

    138peated measures in SPSS version 14. Gender, body weight and BMI

    139were included in the model as subject variables. Amount consumed

    140and hunger ratings were dependent variables and the kind of break-

    141fast was entered as the independent variable. The Bonferroni correc-

    142tion was used in the case of multiple comparisons and Tukey's HSD

    143were used to test differences between breakfast conditions.

    1442.2. Results

    145Characteristics of the participants are presented in Table 3. Eighteen

    146of the 24 participantswere regularbreakfast eaters and 19 of the partic-

    147ipants were female. Neither gender, body weight, BMI, nor whether

    148or not the participants were regular breakfast eaters had a statistically

    149significant effect on hunger ratings or energy consumption.

    150Fig. 1 displays the primary outcomes of Study 1. Panel A shows the

    151mean hunger ratings that were taken prior to eating lunch. Skipping

    152breakfast resulted in participants rating themselves significantly

    153more hungry(p b 0.01) than after eatingeither the high carbohydrate

    154or the highfiber breakfast. Consuming either the high carbohydrate or

    155the high fiber breakfast had no significant effect on the participant's

    156ratings of hunger just before lunch. The type of breakfast (high carbo-

    157hydrate or high fiber) did not have a significant effect on any parame-158ters measured.

    159Despite increased hunger ratings at lunch, when participants

    160skipped breakfast the amount of energy consumed at lunch was not

    161statistically different from the energy consumed on those days when

    162they atebreakfast, as shown in Panel B. Theinability to detectan effect

    163of skipping breakfaston lunch intakewas notdue to a lack of statistical

    164power.A power calculation of thesample indicatedthat a difference of

    16535 kcals could be statistically detected with an alpha set at 0.05 and

    166with a power of 0.8.

    167The energetic consequence of skipping breakfast on total daily

    168intake is depicted by Panel C. The accumulated energy consumed by

    169the end of lunch was significantly greater after having eaten the

    170high carbohydrate 955 42 kcal or the high fiber breakfast 930

    17165 kcal than when breakfast was skipped 600 50 kcal. Energetic172compensation at lunch failed to balance the reduction in energy

    173intake resulting from not eating breakfast.Table 1

    Composition of foods consumed at breakfast for Study 1.

    Breakfast Study 1 Weight Calories Protein Carbohydrate Fat Fiber

    Low fiber breakfast

    Plain bagel 125 200 12 68 1 1.6

    1 tbs of strawberry

    or grape jelly

    10 25 0 6.5 0 0

    1 cup of orange or

    apple juice

    249 110 1 30 0.5 0.3

    Total 335 13 104.5 1.5 1.9

    0 High fiber breakfast

    1 1 cup of raisin bran cereal 56 210 4 45 1.5 6

    2 1 cup of 1% milk 305 128 10.3 15 3 0

    3 Total 338 14.3 0 0 6

    Table 2 t2:1

    t2:2Composition of foods offered at lunch for Study 1.

    t2:3Lunch Study 1 Weight Calories Protein Carbohydrate Fat Fiber

    t2:4Fruit cocktail 248 181 1.0 46.9 1 2.5

    t2:5Plain yogurt 245 149 8.5 11.4 8 0

    t2:6Tuna sandwich 121.8 322 14.2 31.6 0.4 2.3

    t2:7Turkey sandwich 255 476 23 39 15.6 5

    t2:8Cheese sandwich 119 399 17.2 30 23.2 1.3

    t2:9Pasta & marinara sauce 226.8 168 7.2 34 3.2 3.2

    t2:

    10Iced tea 226.8 0 0 0 0 0

    Table 3 t3:1

    t3:2Study 1 Subject characteristics.

    t3:3Subject Characteristics

    t3:4Mean age (years) 22.1 2.7

    t3:5Mean height (m) 1.7 0.08

    t3:6Mean weight (kg) 61 17

    t3:7Mean BMI 21 5.2

    t3:8Female/Male 19/5

    t3:9Mean restraint score 8.8 0.89

    t3:10Number of regular breakfast eaters 18/24

    2 D.A. Levitsky, C.R. Paconowski / Physiology & Behavior xxx (2013) xxxxxx

    Please cite this article as: Levitsky DA, Paconowski CR, Effect of skipping breakfast on subsequent energy intake, Physiol Behav (2013), http://dx.doi.org/10.1016/j.physbeh.2013.05.006

    http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006
  • 7/28/2019 1-s2.0-S0031938413001479-main

    3/8

    UNCORRE

    CTEDPR

    OOF

    174 Neither gender, body weight, BMI, nor the participant's habitual175 breakfast eating pattern had any statistically significant effect on

    176 either the amount consumed or hunger ratings.

    177 2.3. Discussion

    178 This study demonstrated that skipping breakfast did not result in a

    179 significant increase in energy intake at the subsequent meal approxi-

    180 mately three hours later. This resulted in a caloric deficit on the occa-

    181 sions when breakfast was not eaten. However, the mean amount of

    182 energy consumed at breakfast was about 350 kcals. It is possible that

    183 the size of the breakfast used in this study was not sufficient to affect

    184 intake at lunch. It is also possible that energetic compensation for

    185 skipping breakfast may not occur at lunch, but later in the day. There-

    186 fore, the following study was performed to examine the effect of skip-187 ping an ad libitum breakfast on the energy consumed throughout the

    188 rest of the day.

    189 3. Study 2

    190 3.1. Material and methods

    191 Similar to Study 1, participants were undergraduate students at

    192 Cornell University. Eighteen healthy volunteers who showed no aver-

    193 sions or allergies to foods that would be served were chosen. BMIs

    194 ranged from 22 to 27 and the average age was 24. Eleven were regular

    195 breakfast eaters, five regularly skipped breakfast, and two ate break-

    196 fast irregularly. This study differed from the first in that one breakfast

    197 was served or not served and food intake was measured after lunch,

    198after mid-afternoon snack, after dinner, and after late night snack.199The study was approved by the University Institutional Review

    200Board. Participants consumed all breakfasts and lunches in the Cornell

    201Human Metabolic Research Unit (HMRU), but could take snacks and

    202dinners out from the unit. The snack and its weight were recorded

    203before the subject left the HMRU and the subject was asked to return

    204the wrapper along with any uneaten food. They were also asked to re-

    205cord the time when they ate the snack. Because of time constraints,

    206some participants ate their dinner meal outside the unit. They were

    207provided with more than ample food and asked to return all uneaten

    208food to the unit the next day.

    209Participants were recruited and screened in a manner similar to

    210that of the previous study. They were divided into two groups

    211matched on the basis of body weight. They were instructed to eat

    212only food provided by the HMRU on two consecutive Mondays.213They were asked not to eat anything after 11:00 pm the night before.

    214Breakfast was served buffet style between 8:45 am and 10:00 am.

    215Nutrient composition of the food offered is presented in Table 4.

    216After participants placed their food on separate plastic dishes and

    217bowls and took it to a weighing station, staff recorded the weights

    218of all their selected foods. At the end of the meal, plates were again

    219weighed and weights were recorded by the staff. Lunch was served

    220between 11:00 am and 1:00 pm. Like breakfast, the food was served

    221buffet style and weighed before and after eating. Dinner was served

    222between 5:00 and 7:00 pm. Nothing could be eaten between break-

    223fast and lunch. The diet composition of the food offered at lunch,

    224dinner and snacks is presented in Table 5.

    225All participants were tested twice, on the same day of the week

    226but one week apart. On the first testing session, half the participants

    Fig. 1. Panel A. Mean and standard error of hunger rating measured just prior to eating lunch. Groups designated by difference letters are significantly different (p b 0.001). Panel B.

    Mean and standard error of energy intake at lunch following no breakfast (NB), high carbohydrate breakfast (CB), and high fiber breakfast (FB). Panel C. Mean and standard error

    total energy intake (breakfast + lunch) following no breakfast (NB), high carbohydrate breakfast (CB), and high fiber breakfast (FB). Groups designated by different letters are

    significantly different (p b 0.001).

    3D.A. Levitsky, C.R. Paconowski / Physiology & Behavior xxx (2013) xxxxxx

    Please cite this article as: Levitsky DA, Paconowski CR, Effect of skipping breakfast on subsequent energy intake, Physiol Behav (2013), http://dx.doi.org/10.1016/j.physbeh.2013.05.006

    http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006
  • 7/28/2019 1-s2.0-S0031938413001479-main

    4/8

    UNCORRE

    CTEDPR

    OOF

    were given breakfast while the other half were not given breakfast

    and asked not to eat until lunch. On the second testing session, the

    situations were reversed.

    Participants were asked to complete a 6-point hunger rating scale

    at mid-morning, just prior to eating lunch, mid-afternoon, prior to

    eating dinner, and just before going to bed. Energy intake was calcu-

    lated by multiplying the amount of food removed from the partici-

    pants plate by the energetic value taken from the food item's label.

    Paired t-tests (one-tailed) were used to test the statistical significance

    of the within participants difference in caloric intake on the day when

    participants ate breakfast compared with the day when breakfast was

    skipped. Hunger ratings were also analyzed as a dependent variable.

    3.2. Results

    Eighteen participants began the study. One discontinued because

    of time conflicts, and one was removed for not following directions,

    leaving thirteen women and three men to complete the study. Partic-ipant characteristics are presented in Table 6. Similar to the previous

    study, neither gender, body weight, BMI, nor whether or not the par-

    ticipants were regular breakfast eaters had any statistically signifi-

    cant effect on either the amount consumed or hunger ratings. On

    one occasion, three participants ate dinner outside the unit, but

    food was prepared and measured in the laboratory under the same

    conditions as the meals served in the HMRU. Because their intake

    250out of the unit at dinner was within the range of the intake of the

    251other participants who ate dinner in the unit, their data was com-

    252bined with the other intake values for statistical analysis.

    253Unlike in Study 1, participants were served breakfast ad libitum.

    254Results of Study 2 are displayed in Fig. 2. The mean energy intake

    255at breakfast was 624 72 kcal. Panel A shows the hunger ratings

    256throughout the test day for both the day when participants ate break-

    257fast and on the day when breakfast was skipped. Skipping breakfast

    258produced significantly higher hunger ratings mid-morning (p b 0.01)

    259than when breakfast was consumed. This difference in hunger level

    260was still evident at the beginning of lunch (p b 0.05) though smaller.

    261By mid-afternoon, any difference in hunger ratings due to skipping

    262breakfast had disappeared.

    263Panel B of Fig. 2 displays the amount of food eaten throughout

    264the rest of the day categorized into different eating occasions. The

    265amount of energy consumed at lunch was statistically greater (p =

    2660.04) when breakfast was skipped than when it was eaten. However,

    267no significant effect of eating breakfast could be detected at any other

    268eating occasion.

    269The total daily energetic consequence of skipping breakfast can be

    270seen in panel C of Fig. 2. This figure shows that, despite the small in-

    271crease in consumption at lunch, total energy intake was significantly

    272depressed after skipping breakfast compared to when breakfast was

    273eaten. By the end of the day, the participants had consumed about

    274450 kcals fewer calories (p b 0.01) when they skipped breakfast

    275than when they ate it. Similar to the previous study, neither gender,

    276body weight, BMI, nor the participants' regular breakfast eating277pattern had any statistically significant effect on either the amount

    278consumed or hunger ratings.

    2793.3. Discussion

    280The results from these two studies demonstrate that skipping

    281breakfast does not result in an increase in energy intake sufficient to

    282counterbalance the energy deficit by not eating breakfast. In Study 1,

    283breakfast for all participants was limited to about 350 kcal and no in-

    284crease in intake at lunch was observed despite the increase in hunger

    285ratings. In study 2, the breakfast ingested was increased to 624 kcal

    286and skipping it resulted in a statistically significant increase in energy

    287intake at lunch. However, energy intake at lunch increased by only

    288174 kcal, leaving the participants with a net energy intake deficit of289450 kcal by the end of the day.

    290It is unlikely that the lack of compensation of energy intake at

    291lunch for skipping breakfast was due to the participants eating break-

    292fast outside the unit. The hunger ratings, in both studies, confirm

    293that skipping breakfast resulted in a significant increase in feelings

    294of hunger, indicating that the participants had, indeed, refrained

    295from eating prior to eating lunch. Moreover, participant debriefings

    296affirmed their high compliance with the protocol of the study.

    297Although this lack of energetic compensation after skipping break-

    298fast may contradict our intuition, it is consistent with published liter-

    299ature describing meals that were experimentally varied. In a study

    300close in design to the present one (study 2), ten healthy men were

    301given either a low-energy breakfast 100 kcal or high-energy breakfast

    302700 kcal for a two week period and energy consumed was observed

    Table 4

    Composition of foods offered at breakfast for Study 2.

    Breakfast Study 2 Weight

    (g)

    Calories

    (kcal)

    Protein

    (g)

    Carbohydrate

    (g)

    Fat

    (g)

    Fiber

    (g)

    Kix cereal 22.6 85 1.4 19.4 0.5 0.7

    All bran cereal 60 156 7.9 44.5 2.9 17.6

    Corn flakes cereal ALC 28 101.1 1.9 24.4 0.2 0.7

    Frosted flakes cereal

    ALC

    41.3 151.7 1.4 37.3 0.2 1.3

    Grape nuts cerealAFT.PC

    116 416.4 12.5 94.3 2.2 10.1

    Raisin bran cereal

    CMI.AR

    56 210 4 45 1.5 6

    0 Orange juice SHB.EF 236.4 120 0 29 0 0

    1 Apple juice HCG.WA. 248 110 0 29 0 0

    2 Plain bagel 125 330 12 68 1 3

    3 Cream cheese 85.1 296.8 6.4 2.3 29.7 0

    4 Jelly 6.3 16.9 0 4.4 0 0.7

    5 skim milk 245 83.3 8.3 12.2 0.2 0

    6 1%, milk 244 102.5 8.2 12.2 2.4 0

    7 Coffee 237 2.37 0.3 0 0 0

    Table 5

    Composition of foods offered at lunch, snack, and dinner for Study 2.

    Weight

    (g)

    Calories

    (kcal)

    Protein

    (g)

    Carbohydrate

    (g)

    Fat

    (g)

    Fiber

    (g)

    Lunch Study 2

    Plain yogurt 245 149.5 8.5 11.4 8 0Fruit cocktail 248 181 0.97 46.9 0.9 2.5

    Tuna sandwich 121.8 321.8 14.2 31.6 0.4 2.3

    Turkey sandwich 255 476 23 39 15.6 5

    Lemonade drink SBG 251.7 120 0 30 0 0

    0

    1 Snack study 2

    2 Plain yogurt 245 149.5 8.5 11.4 8 0

    3 Apple 110 57 0.3 15.2 0.2 2.6

    4 Animal crackers 85.1 379.3 5.9 63 11.7 0.9

    5 Pretzels 18 68.6 1.6 14.3 0.6 0.6

    6 Juice 250 130 0 34 0 0

    7

    8 Dinner Study 2

    9 Pasta & marinara sauce 226.8 168 7.2 34.4 3.2 0

    0 Dinner rolls 47 120 5 22 1.5 2

    1 Tossed Salad & dressing 99.2 80 3 6 5 1

    2 Lemonade drink SBG 251.7 120 0 30 0 0

    Table 6 t6:1

    t6:2Study 2 subject characteristics.

    t6:3Subject characteristics

    t6:4Mean age (years) 24.0 2.8

    t6:5Mean height (m) 1.7 0.16

    t6:6Mean weight (kg) 69 7.2

    t6:7Mean BMI 24.1 2.2

    t6:8Female/male 13/3

    t6:9Mean restraint score 8.2 0.93

    4 D.A. Levitsky, C.R. Paconowski / Physiology & Behavior xxx (2013) xxxxxx

    Please cite this article as: Levitsky DA, Paconowski CR, Effect of skipping breakfast on subsequent energy intake, Physiol Behav (2013), http://dx.doi.org/10.1016/j.physbeh.2013.05.006

    http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006
  • 7/28/2019 1-s2.0-S0031938413001479-main

    5/8

    UNCORRE

    CTEDPR

    OOF

    303 throughout the day using self-reported diaries [66]. No effect of the

    304 size of the breakfast was evident in the amount of energy consumed

    305 at lunch.1 In a study of the effects of skipping breakfast and of exer-

    306 cise on energy intake at lunch, Hubert et al. [48] found that reducing

    307 breakfast by about 450 kcals increased intake at lunch by about

    308 120 kcals, compensating for only 25% of the energy lost by not eating

    309 breakfast. Interestingly, the compensation in energy intake at lunch

    310 observed in the present study was very similar, about 20%.

    311 Halsey et al. [41] examined the effect of feeding or not feeding

    312 breakfast on young adults for a one week period. Although eating

    313 breakfast increased to total energy intake in both participants who

    314 regularly did not eat breakfast and those that did, only the effect in

    315 regular breakfast eaters reached statistical significance in those who

    316 regularly ate breakfast probably because of the small sample size317 and because intake was based on self-reported intake rather than

    318 measured intake.

    319 Although primarily concerned with fiber, Delargy et al. [21] exam-

    320 ined the effects of eating a small 390 kcal and large breakfast 555 kcal

    321 on subsequent intakeat lunch.They, too, observed no significant effect

    322 of the amount consumed at breakfast on the amount eaten at lunch.

    323 De Graff et al. [20] and Hulshof et al. [49] examined the effects of

    324feeding different levels of macronutrients at breakfast. Both studies

    325failed to find a change in energy intake at lunch despite the fact that

    326the amount of energy consumed at breakfast was 8 kcal, 100 kcal,

    327250 kcal, and 400 kcal in the de Graaf et al. [19] study and 100 kcal,

    328400 kcal, and 800 kcal in the Hulshof et al. [49] study. In a study

    329designed to examine the similarities and differences between fat and

    330carbohydrate, sixteen healthy young men were given either a small

    331breakfast (440 kcal) or the same breakfast supplemented with fat

    332(803 kcal) or carbohydrate (803 kcal). Again, no statistical difference

    333in theamount of energy consumed at lunch wasobserved [17]. Similar

    334findings were reported by Blundell et al. [11]. Finally, Holt et al. [45]

    335found no relationship between the energy consumed at breakfast

    336composed of different foods and the energy consumed at lunch.

    337Taylor and Garrow [91] performedone of themost intensiveexam-338inations of skipping breakfast on both subsequent ad libitum energy

    339intake and energy expenditure in the whole body calorimeter. Similar

    340to the studies cited above, skipping breakfast had no effect on subse-

    341quent energy intake (or energy expenditure) through the remaining

    34224 h in the calorimeter.

    343One of the few studies that tested the effects of skipping breakfast

    344in a clinical weight loss trial was performed by Schlundt et al. [88].

    345They divided a group of participants who wanted to lose weight into

    346people who regularly ate breakfast and those who skipped breakfast.

    347They further divided each of these two groups into a group that re-

    348ceived two meals a day (lunch and dinner) and those who received

    349three meals a day (breakfast, lunch, and dinner) for 12 weeks. Those

    350who regularly ate breakfast, who were then asked to skip breakfast

    351did not lose as much weight as those who ate breakfast, although

    1 Unlike the present study, the participants in this study were allowed to eat a

    midmorning snack. After eating the smaller breakfast, participants ate an average of

    138 kcal whereas they ate only 28 kcal after eating the larger breakfast. This is a differ-

    ence of 110 kcal whereas the difference in energy consumed between the different

    breakfasts was 600 kcal. A suppression of midmorning snack intake following the con-

    sumption of a breakfast supplemented with carbohydrate was also observed by

    Blundell et al. [11].

    Fig. 2. Panel A. Mean and standard error of hunger ratings measured at mid-morning, just prior to lunch, mid-afternoon, just prior to dinner, and during the evening following

    breakfast and without breakfast. **p b 0.01; *p b 0.05. Panel B. Mean and standard error of energy intake at lunch, mid-afternoon snack, dinner, and at the evening snack following

    breakfast and without breakfast. *p = 0.04. Panel C. Mean and standard error to total energy intake following breakfast and without breakfast. *p b 0.01.

    5D.A. Levitsky, C.R. Paconowski / Physiology & Behavior xxx (2013) xxxxxx

    Please cite this article as: Levitsky DA, Paconowski CR, Effect of skipping breakfast on subsequent energy intake, Physiol Behav (2013), http://dx.doi.org/10.1016/j.physbeh.2013.05.006

    http://-/?-http://-/?-http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://-/?-http://-/?-
  • 7/28/2019 1-s2.0-S0031938413001479-main

    6/8

    UNCORRE

    CTEDPR

    OOF

    the differences were not statistically significant. Those who regularly

    ate breakfast, however, lost more weight (though not statistically sig-

    nificant) when switched to the skip breakfast condition than those

    who were asked to eat breakfast. The interaction was marginally

    significant (p = 0.06). If eating breakfast impairs weight loss, it wasnot evident in this study.

    One exception to these findings is a recent study where Astbury

    et al. [5] observed an increase in energy intake at lunch that totally

    compensated for skipping a 200 kcal breakfast. However, because

    the study was primarily concerned with gastrointestinal hormones,

    the protocol incorporated the consumption of a 250 kcal pre-load

    consisting of a liquid diet between the breakfast and the testing

    at lunch. Consequently, it is difficult to compare the results of this

    study with the studies cited above because the increase in intake in

    the breakfast skippers could have occurred because of a counter-

    regulation effect of the preload [44] or the unusual effects of con-

    suming liquid preloads [92].

    Data from Studies 1 and 2, though collected in the laboratory, are

    consistent with 24-hour food recall data from the20032004 NationalHealth and Nutrition Examination Survey [74]. NHANES is a multi-

    stage probability sample of the US non-institutionalized population

    representing a broader population than those of Studies 1 and 2. The

    amount of energy consumed from lunch through the rest of the day

    was calculated for cases where the first meal of the day was breakfast

    andcomparedto thecaseswhere thefirst mealof the day was lunch.

    The results are shown in Fig. 3. Breakfast eaters consumed signifi-

    cantly more energy at each succeeding eating occasion than breakfast

    skippers (p b 0.001). However, as indicated by the upper right inset

    in Fig. 3, despite the fact that the breakfast eaters ate less than the

    breakfast skippers at each eating occasion, the cumulative daily intake

    of breakfast skippers was significantly less than that of breakfast

    eaters (p = 0.025). Similar results were found in other epidemio-

    logical studies [16,22,51,71,72,75,77]. As in Studies 1 and 2, breakfast

    385skippers in the NHANES dataset consumed more energy at lunch

    386than breakfast eaters.

    387If the results of the present studies can be confirmed in a more re-

    388alistic eating situation, skipping breakfast may be an effective way of

    389reducing daily energy intake. However, skipping breakfast has been390found to increase the risk of consuming an insufficient supply of

    391daily nutrients important for health [1,33,36,55,58,64,65,69,80,81,85].

    392The public's search for a clear answer as to whether or not to eat break-

    393fast can be expected to mount as the prevalence of overweight and obe-

    394sity increases [2729,32]. Health practitioners have expressed concern

    395that breakfast foods contain nutrients that are not consumed at eating

    396occasion later in the day (e.g. fiber). However, there is no reason why

    397foods that are usually consumed at breakfast, particularly whole grain,

    398fiber rich, cereals, and milk cannot be substituted for lunch or dinner.

    399In fact, there is evidence that substituting a ready-to-eat cereal for

    400lunch or dinner may result in a further decrease in total energy intake

    401[67].

    402These data are also consistent with recent research that shows

    403that a reduction in portion size at one meal does not result in an in-404crease in energy intake at subsequent meals[63]. There appears to

    405be accumulating evidence that human feeding behavior is less driven

    406by internal regulatory mechanisms such as small energy deficits

    407or surfeits [6062], but rather is vulnerable to external cues such as

    408advertising [39,43] or large portion sizes [84,103].

    409Although the data presented above are consistent with the scien-

    410tific literature on the effects of skipping breakfast, they challenge the

    411common belief that consumption of breakfast daily is essential for

    412good health and weight management. If skipping breakfast produces

    413a chronic deficit in daily energy intake, then the health benefits

    414derived from consuming a lower daily energy intake may be substan-

    415tially greater than consuming breakfast. Future research is needed to

    416investigate the effects of skipping breakfast on energy intake over

    417multiple days.

    Fig. 3. Data from the NHANES 20032004. The mean and standard error of the amount of energy consumed at lunch, dinner, snacks, or drinks as function of whether breakfast was

    consumed as the first meal of the day (Breakfast Eater) or lunch was the first meal (Breakfast Skipper). Inset represents the total daily energy consumed by Breakfast Eaters or

    Breakfast Skippers. All differences between pairs of bars are significant, p b 0.001.

    6 D.A. Levitsky, C.R. Paconowski / Physiology & Behavior xxx (2013) xxxxxx

    Please cite this article as: Levitsky DA, Paconowski CR, Effect of skipping breakfast on subsequent energy intake, Physiol Behav (2013), http://dx.doi.org/10.1016/j.physbeh.2013.05.006

    http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006
  • 7/28/2019 1-s2.0-S0031938413001479-main

    7/8

    UNCORRE

    CTEDPR

    OOF

    418 4. Conclusion

    419 The data collected from two experimental studies and an analysis

    420 of the HANES epidemiological data set indicate that skipping breakfast

    421 does not lead to overconsumption at lunch or any other eating occa-

    422 sion later in the day. Thesefindings suggest that occasionally skipping

    423 breakfast may be an effective strategy to reduce total daily energy

    424 intake.

    425 References

    426 [1] Abalkhail B, Shawky S. Prevalence of daily breakfast intake, iron deficiency anae-427 mia and awareness of being anaemic among Saudi school students. Int J Food Sci428 Nutr 2002;53:51928.429 [2] Albertson AM, Anderson GH, Crockett SJ, Goebel MT. Ready-to-eat cereal con-430 sumption: its relationship with BMI and nutrient intake of children aged 4 to431 12 years. J Am Diet Assoc 2003;103:16139.432 [3] Albertson AM, Franko DL, Thompson D, Eldridge AL, Holschuh N, Affenito SG,433 Bauserman R, Striegel-Moore RH. Longitudinal patterns of breakfast eating in434 black and white adolescent girls. Obesity (Silver Spring) 2007;15:228292.435 [4] Andersen LF, Lillegaard ITL, Overby N, Lytle L, Klepp KI, Johansson L. Overweight436 and obesity among Norwegian schoolchildren: changes from 1993 to 2000.437 Scand J Public Health 2005;33:99106.438 [5] Astbury NM, Taylor MA, Macdonald IA. Breakfast consumption affects appetite,439 energy intake, and the metabolic and endocrine responses to foods consumed440 later in the day in male habitual breakfast eaters. J Nutr 2011;141:13819.

    441 [6] Barton BA, Eldridge AL, Thompson D, Affenito SG, Striegel-Moore RH, Franko DL,442 et al. The relationship of breakfast and cereal consumption to nutrient intake443 and body mass index: the National Heart, Lung, and Blood Institute Growth444 and Health study. J Am Diet Assoc 2005;105:13839.445 [7] BazzanoLA, Song Y, Bubes V, Good CK,MansonJE, LiuS. Dietary intakeof wholeand446 refinedgrain breakfastcereals andweight gain in men. Obes Res2005;13:195260.447 [8] Bellisle F, Monneuse MO, Steptoe A, Wardle J. Weight concerns and eating pat-448 terns a survey of university-students in Europe. Int J Obes 1995;19:72330.449 [9] Bellisle F, Rolland-Cachera MF, Deheeger M, Guilloud-Bataille M. Obesity and450 food intake in children: evidence for a role of metabolic and/or behavioral451 daily rhythms. Appetite 1988;11:1118.452 [10] Berkey CS, Rockett HR, Gillman MW, Field AE, Colditz GA. Longitudinal study of453 skipping breakfast and weight change in adolescents. Int J Obes Relat Metab454 Disord 2003;27:125866.455 [11] Blundell JE, Burley VJ, Cotton JR, Lawton CL. Dietary fat and the control of energy456 intake: evaluating the effects of fat on meal size and postmeal satiety. Am J Clin457 Nutr 1993;57:772S7S.458 [12] Boutelle K, Neumari-Sztainer D, Story M, Resnick M. Weight control behaviors459 among obese, overweight, and nonoverweight adolescents. J Pediatr Psychol460 2002;27:53140.461 [13] Brugman E, Meulmeester JF, Spee-van der Wekke A, Beuker RJ, Zaadstra BM,462 Radder JJ, Verloove-Vanhorick PS. Dieting, weight and health in adolescents in463 the Netherlands. Int J Obes Relat Metab Disord 1997;21:5460.464 [14] Brugman E, Meulmeester JF, Spee-Van der, Verloove-Vanhorick SP. Breakfast-465 skipping in children and young adolescents in the netherlands. Eur J Public466 Health 1998;8:3258.467 [15] Cartwright M, Wardle J, Steggles N, Simon AE, Croker H, Jarvis MJ. Stress and468 dietary practices in adolescents. Health Psychol 2003;22:3629.469 [16] Cho S, Dietrich M, Brown CJ, Clark CA, Block G. The effect of breakfast type on total470 daily energyintake andbodymass index: results from thethirdnationalhealth and471 nutrition examination survey (NHANES III). J Am Coll Nutr 2003;22:296302.472 [17] Cotton JR, Burley VJ, Weststrate JA, Blundell JE. Dietary fat and appetite simi-473 larities and differences in the satiating effect of meals supplemented with either474 fat or carbohydrate. J Hum Nutr Diet 1994;7:1124.475 [18] Croezen S, VisscherTL, Ter BogtNC, Veling ML, Haveman-Nies A. Skipping break-476 fast, alcohol consumption and physical inactivity as risk factors for overweight477 and obesity in adolescents: Results of the E-MOVO project. Eur J Clin Nutr

    478 2009;63:405

    12.479 [19] de Graaf C, Hulshof T. The effect of non-absorbable fat on energy and fat intake.480 Eur J Med Res 1995;1:727.481 [20] de GraafC, Hulshof T, Weststrate JA, Jas P. Short-term effects of differentamounts482 of protein, fats, and carbohydrates on satiety. Am J Clin Nutr 1992;55:33 8.483 [21] Delargy HJ, Burley VJ, O'Sullivan KR, Fletcher RJ, Blundell JE. Effects of different484 soluble: insoluble fibre ratios at breakfast on 24-h pattern of dietary intake485 and satiety. Eur J Clin Nutr 1995;49:75466.486 [22] Deshmukh-Taskar PR, Radcliffe JD, Liu Y, Nicklas TA. Do breakfast skipping and487 breakfast type affect energy intake, nutrient intake, nutrient adequacy, and diet488 quality in young adults? NHANES 19992002. J Am Coll Nutr 2010;29:40718.489 [23] Dialektakou KD, Vranas PB. Breakfast skipping and body mass index among ad-490 olescents in Greece: whether an association exists depends on how breakfast491 skipping is defined. J Am Diet Assoc 2008;108:151725.492 [24] Dubois L, Girard M, Potvin Kent M, Farmer A, Tatone-Tokuda F. Breakfast skip-493 ping is associated with differences in meal patterns, macronutrient intakes and494 overweight among pre-school children. Public Health Nutr 2009;12:1928.495 [25] Dwyer JT, Evans M, Stone EJ, Feldman HA, Lytle L, Hoelscher D, Johnson C, Zive496 M, Yang M. Child and Adolescent Trial for Cardiovascular Health (CATCH)

    497Cooperative Research Group. Adolescents' eating patterns influence their nutri-498ent intakes. J Am Diet Assoc 2001;101:798802.499[26] Fabritius K, Rasmussen M. Breakfast habits and overweight in Danish500schoolchildren. the role of socioeconomic positions. Ugeskr Laeger 2008;170:501255963.502[27] Flegal KM, Carroll MD, Kuczmarski RJ, Johnson CL. Overweight and obesity in the503United States: prevalence and trends, 19601994. Int J Obes Relat Metab Disord5041998;22:3947.505[28] Flegal KM, Carroll MD, Ogden CL, Curtin LR. Prevalence and trends in obesity506among US adults, 19992008. JAMA 2010;303:23541.507[29] Flegal KM, Carroll MD, Ogden CL, Johnson CL. Prevalence and trends in obesity

    508among US adults, 1999

    2000. JAMA 2002;288:1723

    7.509[30] Forslund HB, Lindroos AK, Sjostrom L, Lissner L. Meal patterns and obesity in510Swedish women a simple instrument describing usual meal types, frequency511and temporal distribution. Eur J Clin Nutr 2002;56:7407.512[31] Fujiwara T. Skipping breakfast is associated with dysmenorrhea in young513women in Japan. Int J Food Sci Nutr 2003;54:5059.514[32] Galuska DA, Serdula M, Pamuk E, Siegel PZ, Byers T. Trends in overweight among515US adults from 1987 to 1993: a multistate telephone survey. Am J Public Health5161996;86:172935.517[33] Gibson EL,Wainwright CJ, Booth DA. Disguisedproteinin lunch after low-protein518breakfast conditions food-flavorpreferences dependent on recent lack of protein519intake. Physiol Behav 1995;58:36371.520[34] Gibson SA, O'Sullivan KR. Breakfast cereal consumption patterns and nutrient521intakes of British schoolchildren. J R Soc Health 1995;115:36670.522[35] Gikas A, Triantafillidis JK, Perdikaki P. Breakfast skipping and its association523with other unhealthy food habiits among Greek high school adolescents. Ann524Gastroenterol 2003;16:3217.525[36] Gittelsohn J, Wolever TM, Harris SB, Harris-Giraldo R, Hanley AJ, Zinman B. Spe-526cific patterns of food consumption and preparation are associated with diabetes

    527and obesity in a native Canadian community. J Nutr 1998;128:5417.528[37] Haines PS, Guilkey DK, Popkin BM. Trends in breakfast consumption of US adults529between 1965 and 1991. J Am Diet Assoc 1996;96:46470.530[38] Haire-Joshu D, Schwarz C, Budd E, Yount BW, Lapka C. Postpartum teens' break-531fast consumption is associated with snack and beverage intake and body mass532index. J Am Diet Assoc 2011;111:12430.533[39] Halford JC, Boyland EJ, Hughes G, Oliveira LP, Dovey TM. Beyond-brand effect of534television (TV) food advertisements/commercials on caloric intake and food535choice of 57-year-old children. Appetite 2007;49:2637.536[40] Hallstrom L, Labayen I, Ruiz JR, Patterson E, Vereecken CA, Breidenassel C,537Gottrand F, Huybrechts I, Manios Y, Mistura L, Widhalm K, Kondaki K, Moreno538LA, Sjostrom M. Breakfast consumption and CVD risk factors in European adoles-539cents: the HELENA (healthy lifestyle in Europe by nutrition in adolescence)540study. Public Health Nutr 2012:110.541[41] Halsey LG, Huber JW, Low T, Ibeawuchi C, Woodruff P, Reeves S. Does consuming542breakfast influence activity levels? An experiment into the effect of breakfast543consumption on eating habits and energy expenditure. Public Health Nutr5442012;15:23845.545[42] Harding S, Teyhan A, Maynard MJ, Cruickshank JK. Ethnic differences in over-546weight and obesity in early adolescence in the MRC DASH study: the role of547adolescent and parental lifestyle. Int J Epidemiol 2008;37:16272.548[43] Harris JL, Bargh JA, Brownell KD. Priming effects of television food advertising on549eating behavior. Health Psychol 2009;28:40413.550[44] Herman CP, Polivy J, Esses VM. The illusion of counter-regulation. Appetite5511987;9:1619.552[45] Holt SHA, Delargy HJ, Lawton CL, Blundell JE. The effects of high-carbohydrate vs553high-fat breakfasts on feelings of fullness and alertness, and subsequent food554intake. Int J Food Sci Nutr 1999;50:1328.555[46] Horikawa C, Kodama S, Yachi Y, Heianza Y, Hirasawa R, Ibe Y, et al. Skipping556breakfast and prevalence of overweight and obesity in Asian and Pacific regions:557a meta-analysis. Prev Med 2011;53:2607.558[47] Huang CJ, Hu HT, Fan YC, Liao YM, Tsai PS. Associations of breakfast skipping559with obesity and health-related quality of life: evidence from a national survey560in Taiwan. Int J Obes (Lond) 2010;34:7205.561[48] Hubert P, King NA, Blundell JE. Uncoupling the effects of energy expenditure and562energy intake: appetite response to short-term energy deficit induced by meal563omission and physical activity.Appetite Aug. 1998;vol. 31(1):919 [1998:199].

    564[49] Hulshof T, DeGraaf C, Weststrate JA. The effects of preloads varying in physical565state and fat content on satiety and energy intake. Appetite 1993;21:27386.566[50] EatRight analysis.Jones and Bartlett Publishers; 2002 [2].567[51] Kant AK, Andon MB, Angelopoulos TJ, Rippe JM. Association of breakfast energy568density with dietquality andbody mass index in American adults:National Health569and Nutrition ExaminationSurveys,19992004. Am J ClinNutr2008;88:1396404.570[52] Kapantais E, Chala E, Kaklamanou D, Lanaras L, Kaklamanou M, Tzotzas T. Break-571fast skipping and its relation to BMI and health-compromising behaviours572among Greek adolescents. Public Health Nutr 2011;14:1018.573[53] Keski-Rahkonen A, Viken RJ, Kaprio J, Rissanen A, Rose RJ. Genet Environ Factors574Eat Patterns 2004;34:50314.575[54] Kim JH, So WY. Association between frequency of breakfast eating and obesity in576Korean adolescents. Iran J Public Health 2012;41:507.577[55] Kleinman RE, Hall S, Green H, Korzec-Ramirez D, Patton K, Pagano ME, et al.578Diet, breakfast, and academic performance in children. Ann Nutr Metab5792002;46(Suppl. 1):2430.580[56] Kovarova M, Vignerova J, Blaha P, Osancova K. Bodily characteristics and lifestyle581of Czech children aged 7.00 to 10.99 years, incidence of childhood obesity. Cent582Eur J Public Health 2002;10:16973.

    7D.A. Levitsky, C.R. Paconowski / Physiology & Behavior xxx (2013) xxxxxx

    Please cite this article as: Levitsky DA, Paconowski CR, Effect of skipping breakfast on subsequent energy intake, Physiol Behav (2013), http://dx.doi.org/10.1016/j.physbeh.2013.05.006

    http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0090http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0075http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0060http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0185http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0180http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0010http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0010http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0010http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0010http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0010http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0475http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0475http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0475http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0475http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0475http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0015http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0015http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0015http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0015http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0015http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0020http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0020http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0020http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0020http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0020http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0030http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0030http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0030http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0030http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0030http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0030http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0035http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0035http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0035http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0035http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0035http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0035http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0040http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0040http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0040http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0040http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0040http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0045http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0045http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0045http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0045http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0045http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0050http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0050http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0050http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0050http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0050http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0055http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0055http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0055http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0055http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0055http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0060http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0060http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0060http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0060http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0060http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0480http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0480http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0480http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0480http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0480http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0070http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0070http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0070http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0070http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0075http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0075http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0075http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0075http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0075http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0090http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0090http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0090http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0090http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0095http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0095http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0095http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0095http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0115http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0115http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0115http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0115http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0115http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0490http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0490http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0490http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0490http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0490http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0135http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0135http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0135http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0135http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0135http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0135http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0140http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0140http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0140http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0140http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0140http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0140http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0150http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0150http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0150http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0150http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0495http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0495http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0495http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0495http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0495http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0165http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0165http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0165http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0165http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0180http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0180http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0180http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0180http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0185http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0185http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0185http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0185http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0185http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0200http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0200http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0200http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0200http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0200http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0205http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0205http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0205http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0205http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0210http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0210http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0210http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0210http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0215http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0215http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0215http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0215http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0215http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0505http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0505http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0505http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0505http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0505http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0225http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0225http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0225http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0225http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0515http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0235http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0235http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0235http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0235http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0235http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0240http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0240http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0240http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0240http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0245http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0245http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0245http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0245http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0250http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0250http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0250http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0250http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0250http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0255http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0255http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0255http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0255http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0255http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://dx.doi.org/10.1016/j.physbeh.2013.05.006http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0255http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0255http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0255http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0250http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0250http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0250http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0245http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0245http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0240http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0240http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0235http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0235http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0235http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0230http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0515http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0225http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0225http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0510http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0505http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0505http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0505http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0220http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0215http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0215http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0215http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0210http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0210http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0205http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0205http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0200http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0200http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0200http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0195http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0500http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0190http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0185http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0185http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0185http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0180http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0180http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0175http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0170http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0165http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0165http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0160http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0495http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0495http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0495http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0150http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0150http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0145http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0140http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0140http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0135http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0135http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0130http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0490http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0490http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0490http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0485http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0115http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0115http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0115http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0110http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0105http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0100http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0095http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0095http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0090http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0090http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0085http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0080http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0075http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0075http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0075http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0070http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0070http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0480http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0480http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0480http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0060http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0060http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0060http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0055http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0055http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0055http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0050http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0050http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0050http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0045http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0045http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0045http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0040http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0040http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0040http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0035http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0035http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0030http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0030http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0025http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0020http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0020http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0020http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0015http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0015http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0015http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0475http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0475http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0475http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0010http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0010http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0010http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0005
  • 7/28/2019 1-s2.0-S0031938413001479-main

    8/8

    UNCORRE

    CTEDPR

    OOF

    [57] Kral TV, Whiteford LM, Heo M, Faith MS. Effects of eating breakfast comparedwith skipping breakfast on ratings of appetite and intake at subsequent mealsin 8- to 10-y-old children. Am J Clin Nutr 2011;93:28491.

    [58] Kunimoto M, Nishi M, Sasaki K. The relation between irregular bowel movementand the lifestyle of working women. Hepatogastroenterology 1998;45:95660.

    [59] Lee CJ, Templeton S, Wang C. Meal skipping patterns and nutrient intakes ofrural southern elderly. J Nutr Elder 1996;15:114.

    [60] Levitsky DA. The non-regulation of food intake in humans: hope for reversingthe epidemic of obesity. Physiol Behav 2005;86:62332.

    [61] Levitsky DA. The control of food intake and the regulation of body weight inhumans. In: Harris RBS, Mattes RD, editors. Appetite and food intake: behavioral

    and physiological considerations. Boca Raton: CRC Press; 2008. p. p21

    42.[62] Levitsky DA, Pacanowski C. Losing weight without dieting. use of commercialfoods as meal replacements for lunch produces an extended energy deficit.Appetite 2011;57:3117.

    [63] Levitsky DA, Pacanowski CR. Free will and the obesity epidemic. Public HealthNutr 2011:116.

    [64] LiuS, SessoHD, Manson JE,WillettWC, BuringJE. Isintake ofbreakfast cereals re-latedto total andcause-specific mortality inmen?Am J Clin Nutr 2003;77:5949.

    [65] Lloyd HM, Rogers PJ, Hedderley DI, Walker AF. Acute effects on mood and cogni-tive performance of breakfasts differing in fat and carbohydrate content. Appe-tite 1996;27:15164.

    [66] Martin A, Normand S, Sothier M, Peyrat J, Louche-Pelissier C, Laville M. Is advicefor breakfast consumption justified? Results from a short-term dietary andmetabolic experiment in young healthy men. Br J Nutr 2000;84:33744.

    [67] Mattes RD. Ready-to-eat cereal used as a meal replacement promotes weightloss in humans. J Am Coll Nutr 2002;21:5707.

    [68] Matthys C, DeHenauwS, Bellemans M, DeMaeyer M, DeBackerG. Breakfasthabitsaffect overall nutrient profiles in adolescents. Public Health Nutr 2007;10:41321.

    [69] McNeill G, Vyvyan J, Peace H, McKie L, Seymour G, Hendry J, et al. Predictors of

    micronutrient status in men and women over 75 years old living in the commu-nity. Br J Nutr 2002;88:55561.

    [70] Merten MJ, Williams AL, Shriver LH. Breakfast consumption in adolescenceand young adulthood: parental presence, community context, and obesity. J AmDiet Assoc 2009;109:138491.

    [71] Morgan KJ, ZabikME. Theinfluence of ready-to-eat cereal consumption at break-fast on nutrient intakes of individuals 62 years and older. J Am Coll Nutr 1984;3:2744.

    [72] Morgan KJ, Zabik ME, Leveille GA. The role of breakfast in nutrient intake of 5- to12-year-old children. Am J Clin Nutr 1981;34:141827.

    [73] Morgan KJ, Zabik ME, Stampley GL. The role of breakfast in diet adequacy of theU.S. adult population. J Am Coll Nutr 1986;5:55163.

    [74] NHANES. National health and nutrition examination survey. 20032004; 2007.[75] Nicklas TA, Bao W, Webber LS, Berenson GS. Breakfast consumption affects

    adequacy of total daily intake in children. J Am Diet Assoc 1993;93:88691.[76] Nicklas TA, Morales M, Linares A, Yang SJ, Baranowski T, De Moor C, et al.

    Children's meal patterns have changed over a 21-year period: the BogalusaHeart Study. J Am Diet Assoc 2004;104:75361.

    [77] Nicklas TA, Myers L, Berenson GS. Impact of ready-to-eat cereal consumption ontotal dietary intake of children: the Bogalusa Heart Study. J Am Diet Assoc1994;94:3168.

    [78] Nicklas TA, Myers L, Reger C, Beech B, Berenson GS. Impact of breakfast con-sumption on nutritional adequacy of the diets of young adults in Bogalusa,Louisiana: ethnic and gender contrasts. J Am Diet Assoc 1998;98:14328.

    [79] Ortega RM, Redondo MR, Lopez-Sobaler AM, Quintas ME, Zamora MJ, Andres P,et al. Associations between obesity, breakfast-time food habits and intake ofenergy and nutrients in a group of elderly Madrid residents. J Am Coll Nutr1996;15:6572.

    [80] Ortega RM, Requejo AM, Lopez-Sobaler AM, Quintas ME, Andres P, Redondo MR,et al. Difference in the breakfast habits of overweight/obese and normal weightschoolchildren. Int J Vitam Nutr Res 1998;68:12532.

    [81] Preziosi P, Galan P, Deheeger M, Yacoub N, Drewnowski A, Hercberg S. Breakfasttype, daily nutrient intakes and vitamin and mineral status of French children,adolescents and adults. J Am Coll Nutr 1999;18:1718.

    647[82] Purslow LR, Sandhu MS, Forouhi N, Young EH, Luben RN, Welch AA, et al. Energy648intake at breakfast and weight change: prospective study of 6,764 middle-aged649men and women. Am J Epidemiol 2008;167:18892.650[83] Resnicow K. The relationship between breakfast habits and plasma cholesterol651levels in schoolchildren. J Sch Health 1991;61:815.652[84] Rolls BJ. The supersizing of America: portion size and the obesity epidemic. Nutr653Today 2003;38:4253.654[85] Ruxton CH, Kirk TR. Breakfast: a review of associations with measures of dietary655intake, physiology and biochemistry. Br J Nutr 1997;78:199213.656[86] Sampson AE, Dixit S, Meyers AF, Houser Jr R. The nutritional impact of breakfast657consumption on the diets of inner-city African-American elementary school

    658children. J Natl Med Assoc 1995;87:195

    202.659[87] Sanchez-Henriquez P, Doreste Alonso J, Lainez Sevillano P, Estevez Gonzalez MD,660Iglesias Valle M, Lopez Martin G, Sosa Iglesias I, Serra Majem L. Prevalence of661obesity and overweight in adolescents from Canary Islands, Spain. Relationship662with breakfast and physical activity. Med Clin (Barc) 2008;130:60610.663[88] SchlundtDG, Hill JO,SbroccoT, Pope-CordleJ, SharpT. Theroleof breakfastin the664treatment of obesity: a randomized clinical trial. Am J Clin Nutr1992;55:64551.665[89] Schusdziarra V, Hausmann M, Wittke C, Mittermeier J, Kellner M, Naumann A,666et al. Impact of breakfast on daily energy intake an analysis of absolute versus667relative breakfast calories. Nutr J 2011;10:512.668[90] Song WO, Chun OK, Kerver J, Cho S, Chung CE, Chung SJ. Ready-to-eat breakfast669cereal consumption enhances milk and calcium intake in the US population.670J Am Diet Assoc 2006;106:17839.671[91] Taylor MA, Garrow JS. Compared with nibbling, neither gorging nor a morning672fast affect short-term energy balance in obese patients in a chamber calorimeter.673Int J Obes Relat Metab Disord 2001;25:51928.674[92] Tieken SM, Leidy HJ, Stull AJ, Mattes RD, Schuster RA, Campbell WW. Effects of675solid versus liquid meal-replacement products of similar energy content on hun-676ger, satiety, and appetite-regulating hormones in older adults. Horm Metab Res

    6772007;39:38994.678[93] Timlin MT, Pereira MA, Story M, Neumark-Sztainer D. Breakfast eating and weight679change in a 5-year prospective analysis of adolescents: Project EAT (eating among680teens). Pediatrics 2008;121:e63845.681[94] Tin SP, Ho SY, Mak KH, Wan KL, Lam TH. Breakfast skipping and change in body682mass index in young children. Int J Obes (Lond) 2011;35:899906.683[95] vander HeijdenAA, Hu FB,Rimm EB,van DamRM. A prospective study of breakfast684consumption and weight gain among U.S. men. Obesity (Silver Spring) 2007;15:68524639.686[96] Vanelli M, Iovane B, Bernardini A, Chiari G, Errico MK, Gelmetti C, et al. Breakfast687habits of 1,202 northern Italian children admitted to a summer sport school.688Breakfast skipping is associated with overweight and obesity. Acta Biomed6892005;76:7985.690[97] Williams BM, O'Neil CE, Keast DR, Cho S, Nicklas TA. Are breakfast consumption691patterns associated with weight status and nutrient adequacy in African-692American children? Public Health Nutr 2009;12:48996.693[98] Williams P. Breakfast and the diets of Australian adults: an analysis of data from694the 1995 national nutrition survey. Int J Food Sci Nutr 2005;56:6579.695[99] Williams P. Breakfast and the diets of Australian children and adolescents: an696analysis of data from the 1995 national nutrition survey. Int J Food Sci Nutr6972007;58:20116.698[100] Wolfe WS, Campbell CC, Frongillo Jr EA, Haas JD, Melnik TA. Overweight699schoolchildren in New York state: prevalence and characteristics. Am J Public700Health 1994;84:80713.701[101] Wong YC, Chen SL, Chan YC, Wang MF, Yamamoto S. Weight satisfaction and702dieting practices among college males in Taiwan. J Am Coll Nutr 1999;18:2238.703[102] Wyatt HR,Grunwald GK,Mosca CL,KlemML, Wing RR,Hill JO.Long-term weight704loss and breakfast in subjects in the national weight control registry. Obes Res7052002;10:7882.706[103] Young LR, Nestle M. The contribution of expanding portion sizes to the US obe-707sity epidemic. Am J Public Health 2002;92:2469.708[104] Zullig K, Ubbes VA, Pyle J, Valois RF. Self-reported weight perceptions, dieting709behavior, and breakfast eating among high school adolescents. J Sch Health7102006;76:8792.711

    8 D.A. Levitsky, C.R. Paconowski / Physiology & Behavior xxx (2013) xxxxxx

    Please cite this article as: Levitsky DA, Paconowski CR, Effect of skipping breakfast on subsequent energy intake, Physiol Behav (2013), http://dx.doi.org/10.1016/j.physbeh.2013.05.006

    http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0370http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0365http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0360http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0355http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0350http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0430http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0540http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0535http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0425http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0420http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0415http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0410http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0405http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0260http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0260http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0260http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0260http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0260http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0265http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0265http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0265http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0265http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0270http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0270http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0270http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0270http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0275http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0275http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0275http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0275http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0280http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0280http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0280http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0280http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0280http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0285http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0285http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0285http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0285http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0285http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0285http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0285http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0520http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0520http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0520http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0520http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0290http://refhub.elsevier.com/S0031-9384(13)00147-9/rf0290http://refhub.elsevier.com/S0031-9