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Nielsen Et Al-2018-Obesity
Nielsen Et Al-2018-Obesity
Objective: Using an ad libitum buffet meal targeting direct behavior, the authors of the current study previ-
ously reported no effect of Roux-en-Y gastric bypass (RYGB) and sleeve gastrectomy (SG) surgery on food
preferences 6 months after surgery. The current study investigated changes in food preferences at 18
months after surgery and whether changes in food preferences at 6 months predicted weight loss.
Methods: Twenty food items separated into the following food categories were served at the buffet meal:
high-fat, low-fat, sweet, savory, high-fat savory, high-fat sweet, low-fat savory, and low-fat sweet. Energy
intake and intake from each of the food items were registered. Energy intake prior to the meal was
standardized.
Results: Thirty-nine subjects completed visits before surgery and 18 months following RYGB (n = 29) and
SG (n = 10) surgery. Energy intake decreased 41% (4,470 ± 209 kJ vs. 2,618 ± 209 kJ, P < 0.001), but no change
occurred in relative energy intake from any of the food categories (all P ≥ 0.23), energy density (P = 0.20), or
macronutrient intake (all P ≥ 0.28). However, changes in high-fat food intake, protein intake, energy intake,
and energy density at 6 months predicted weight loss at 18 months (P ≤ 0.02).
Conclusions: RYGB surgery and SG surgery do not affect food preferences. However, changes in food
preferences seem to be predictive of weight loss.
Obesity (2018) 0, 00-00. doi:10.1002/oby.22272
1
Department of Nutrition, Exercise and Sports, Faculty of Science (Obesity Research), University of Copenhagen, Copenhagen, Denmark.
Correspondence: Mette Søndergaard Nielsen (msn@nexs.ku.dk) 2 The Danish Diabetes Academy, Odense University Hospital, Odense,
Denmark 3 Department of Food and Resource Economics, Faculty of Science, University of Copenhagen, Copenhagen, Denmark 4 Investigative
Science, Imperial College London, London, UK 5 Diabetes Complications Research Centre, Conway Institute, University College Dublin, Dublin,
Ireland.
Funding agencies: This study was carried out as part of the research program “Governing Obesity” funded by the University of Copenhagen Excellence Programme for
Interdisciplinary Research (www.go.ku.dk). Furthermore, the Danish Diabetes Academy supported by the Novo Nordisk Foundation, the Lundbeck Foundation, and the
Aase and Ejnar Danielsens Foundation funded this study.
Disclosure: CWlR was supported by grants from Science Foundation Ireland (ref 12/YI/B2480), the Health Research Board (USIRL-2016-2), and the Irish Research Council
during the conduct of the study. Furthermore, CWlR reported being on the advisory boards for Novo Nordisk and GI Dynamics, receiving a research grant from AnaBio,
and receiving honoraria for lectures and advisory work from Eli Lily, Johnson and Johnson, Sanofi Aventis, Astra Zeneca, Janssen, Bristol-Myers Squibb, and Boehringer-
Ingelheim. The other authors declare no conflict of interest.
Clinical trial registration: ClinicalTrials.gov identifier NCT02070081.
Additional Supporting Information may be found in the online version of this article.
Received: 3 May 2018; Accepted: 22 June 2018. Published online 0 Month 2018. doi:10.1002/oby.22272
changes in food preferences, macronutrient intake, or energy density preferences and for as long as they wanted. They ate unmonitored
of the selected meal (13). and unaccompanied, in order to diminish social desirability bias. The
staging and placement on the table of the 20 food items were identi-
The prevailing view is that changes in food preferences following bar- cal at each visit.
iatric surgery are due to a learned adjustment to postingestive responses
following intake of high-fat and sweet foods, commonly termed “con- The 20 food items varied along two dimensions associated with food
ditioned taste avoidance” (21). At 6 months, patients might still be in a choices, fat (high or low) and taste (sweet or savory) (23), thereby
“learning period,” in which they adjust food intake to avoid postinges- making it possible to organize the food items into separate catego-
tive responses (22). Thus, we speculate whether 6 months postsurgery ries (high-fat and low-fat or sweet and savory) or combined food cat-
was too early for behavioral changes to set in. egories (high-fat savory, low-fat savory, high-fat sweet, and low-fat
sweet) (13). Total energy intake, intake from each of the food cate-
The aim of this study was to investigate food preferences using an gories, and the duration of the meal were registered. The participants
ad libitum buffet meal targeting direct behavior 18 months following were unaware of this registration. In order to divert the attention of
RYGB and SG surgery. We hypothesized that energy intake at 18 the participants away from making food choices to please the investi-
months after surgery was increased compared with 6 months after gators, a blood sample was drawn after the meal, and the participants
surgery, thereby reaching a threshold at which enough postinges- were informed that the aim was to investigate how “eating as much as
tive responses could be generated, resulting in a relative reduction they wished of the food they liked best” affected gut hormone levels
in intake of high-fat and sweet foods and a corresponding rela- in the blood.
tive increase in intake of low-fat and savory foods. Furthermore,
because of the large variation we observed in food preferences at Picture display test. Participants were presented with standardized
6 months, we investigated whether changes in food preferences for pictures of the following 20 food items: pork rib roast, turkey strips,
high-fat and sweet foods, macronutrient intake, energy density, and nuggets, Danish omelet, French fries, crispbread, salty crackers, skyr
total energy intake at 6 months predicted weight loss outcomes 18 with berries, carrots, cut fruit, cheese, smoked fillet (cold cuts), vanilla
months after surgery. ice cream, cocoa meringues, sweet licorice, Danish pastries, milk choc-
olate, pound cake, cookies, and wine gum. Pictures were displayed in
a randomized order, and the participants were instructed to choose the
food item they would most like to eat.
Methods
The study population, design, and methods have been described Previous experience of unpleasant postingestive responses. Previous
previously (13). Briefly, food preferences were assessed approxi- experience of unpleasant postingestive responses was assessed by a sem-
mately 3 months before surgery (prior to a mandatory 8% presur- istructured qualitative interview 6 weeks, 6 months and 18 months after
gical weight loss), as well as 6 months and 18 months following surgery. Data from the interviews were quantified into a 4-point score
RYGB and SG surgery. Data from the visits before surgery and 6 (0-3), with 0 indicating no experience of discomfort related to eating after
months after surgery have been reported previously (13). At each surgery, while 1, 2 and 3 indicate low, medium and high levels of discom-
visit, anthropometric data were collected in the fasted state at 9:00 fort, respectively.
am. At 3:30 pm, a picture display test was carried out, and at 4:30
pm, an ad libitum buffet meal was served. Energy intake prior to Premeal hunger. Premeal hunger was assessed by a visual analog
the test meal was standardized (a 954 kJ meal and a 1,675 kJ liquid scale (100 mm) approximately 15 minutes prior to the buffet meal.
meal were served at 10:00 am and 1:15 pm, respectively; Cambridge
Weight Plan). The liquid meal came in five different flavors: choc-
olate, chocolate mint, strawberry, wild berry, and caramel and Anthropometric measures. Body weight and height were measured
walnut. after an overnight fast. Percent total weight loss (%TWL) was defined
as the presurgical weight minus the weight at 18 months after surgery,
divided by the presurgical weight, and multiplied by 100.
The study was approved by the Scientific Ethic Committees of
the Capital Region of Denmark (Journal number H-3-2013-138)
and registered in the database www.ClinicalTrials.gov (identi- Statistical analysis
fier NCT02070081). All study participants gave written informed
Descriptive data summaries are presented as mean ± SD. Premeal hun-
consent.
ger, total energy intake, energy density, eating time, eating rate, and
weight changes were analyzed using linear mixed models with visit as
Outcomes fixed effect. Intake from the buffet meal was analyzed using a two-stage
Buffet meal test. The following 20 food items were served at the approach to accommodate for semicontinuous data (consisting of zero
buffet meal: pork rib roast, chicken fillet strips, fish cakes, nuggets, intake and positive intake; (24)): First, a logistic mixed-effects model
Danish omelet, French fries, creamy potato gratin, bread (rye bread, was fitted to the binary data indicating if intake was 0 or not. Second, a
baguette, and crispbread), ketchup, remoulade, mayonnaise, skyr linear mixed model was fitted to the square root–transformed positive
with berries, cut raw vegetables, cut fruit, vanilla ice cream, choc- intake values only. Both models included the food category-visit in-
olate sauce, cocoa meringues, biscuit cones with chocolate, sweet teraction as fixed effect. Estimates from these two analyses were then
licorice, and Danish pastries. The only liquid served at the meal combined and back-transformed to obtain unconditional estimates of
was water. The participants were instructed to eat according to their mean intakes per category and visit and differences in mean intakes
TABLE 2 Intake, eating time, and eating rate at buffet meal (n = 39)
www.obesityjournal.org
Food Preferences Assessed by Buffet Meal Test Søndergaard Nielsen et al.
TABLE 4 Body weight and intake, eating time, and eating rate at buffet meal in subjects with high energy intake and low energy intake at buffet meal 18 mo after
surgery
Low energy intake group (n = 13) High energy intake group (n = 13)
www.obesityjournal.org
RYGB/SG surgery 7/6 - - 11/2 - - -
Body weight (kg) 124.0 ± 4.1 83.8 ± 4.1 < 0.001 135.9 ± 5.6 96.1 ± 5.6 < 0.001 > 0.99
Premeal hunger (cm) 5.5 ± 0.8 4.6 ± 0.8 0.43 5.6 ± 0.8 6.0 ± 0.8 0.62 0.32
Total energy intake (kJ) 3,463 ± 292 1,295 ± 292 < 0.001 5,513 ± 407 3,931 ± 407 < 0.01 0.37
CLINICAL TRIALS AND INVESTIGATIONS
Energy intake (kJ/kg body 31.5 ± 4.1 19.2 ± 4.0 < 0.001 42.1 ± 4.0 43.6 ± 4.0 0.79 0.02
weight)
Energy density (kJ/g) 6.6 ± 0.4 6.0 ± 0.4 0.16 7.6 ± 0.5 9.0 ± 0.5 < 0.01 < 0.01
Eating time (min) 19.9 ± 1.8 9.7 ± 1.8 < 0.001 19.7 ± 2.0 19.2 ± 2.0 0.79 < 0.01
Eating rate (kJ/min) 186 ± 17 150 ± 17 0.06 299 ± 33 238 ± 33 0.18 0.61
Intake from combined categories
High-fat savory (%) 41 ± 4 27 ± 6 0.048 48 ± 4 57 ± 5 0.20 < 0.01
High-fat sweet (%) 4 ± 1 2 ± 1 0.20 9 ± 2 16 ± 3 0.05
Low-fat savory (%) 48 ± 4 65 ± 6 0.02 40 ± 4 22 ± 4 < 0.001
Low-fat sweet (%) 7 ± 2 6 ± 3 0.75 3 ± 1 6 ± 2 0.21
Intake from separate categories
High-fat (%) 46 ± 5 33 ± 8 0.16 59 ± 5 73 ± 5 0.048 0.03
Low-fat (%) 54 ± 5 67 ± 8 41 ± 5 27 ± 5
Sweet (%) 17 ± 3 13 ± 4 0.40 15 ± 3 24 ± 4 0.10 0.39
Savory (%) 83 ± 3 87 ± 4 85 ± 3 76 ± 4
Intake macronutrients
E% carbohydrate 37 ± 3 42 ± 5 0.39 35 ± 3 36 ± 3 0.81 < 0.001
E% fat 42 ± 3 38 ± 5 0.52 45 ± 3 48 ± 3 0.47
E% protein 22 ± 3 20 ± 4 0.78 20 ± 2 16 ± 2 0.21
Data are shown as mean ± SE.
aChanges compared with presurgery were compared using linear mixed models adjusted for age and gender and with subject as random effect.
E%, energy percentage; RYGB, Roux-en-Y gastric bypass; SG, sleeve gastrectomy.
TABLE 5 Mean frequency of food choices at picture display test from each combined food category
Figure 1 Associations between percent total weight loss (%TWL) at 18 mo after surgery and changes in (A) energy intake from before surgery to 6 mo after surgery, (B)
energy density from before surgery to 6 mo after surgery, (C) relative intake of protein from before surgery to 6 mo after surgery, (D) relative intake of high-fat food from
before surgery to 6 mo after surgery, and (E) relative intake of high-fat food from before surgery to 18 mo after surgery. Associations were evaluated using simple linear
regressions adjusted for age and gender.
No postoperative changes were observed in relative energy intake for changes between presurgery and 18 months postsurgery for
from the combined food categories (high-fat savory, high-fat sweet, total energy intake (P = 0.09, R 2 = 0.18) and energy density (P = 0.07.
low-fat savory, and low-fat sweet), the separate food categories (high- R 2 = 0.20). No associations were found between intake of sweet foods
fat versus low-fat and sweet versus savory), the different macronutri- and %TWL at 18 months after surgery (P ≥ 0.35) or between intake
ents (Table 2), or from any of the 20 food items served at the buffet from the remaining macronutrients and %TWL at 18 months after
(Supporting Information Table S1). surgery (all P ≥ 0.19).
Prediction of weight loss outcomes We hypothesized that 18 months after surgery, energy intake at
Changes between presurgery and 6 months postsurgery for total the buffet meal would increase compared with 6 months after sur-
energy intake (P = 0.02, R 2 = 0.24), energy density (P < 0.001, gery, thereby potentially reaching a threshold at which postinges-
R 2 = 0.39), protein intake (P = 0.01, R 2 = 0.26), and intake of high-fat tive responses would be sufficient to lead to a substantial shift in
foods (P = 0.01, R 2 = 0.26) predicted %TWL at 18 months (Figure 1). food preferences for most patients. This hypothesis was based on
Furthermore, changes between presurgery and 18 months postsur- the view that the effect of RYGB and SG surgery on food prefer-
gery for intake of high-fat foods (P = 0.01, R 2 = 0.26) were associated ences is caused by a learned adjustment to postprandial visceral sig-
with %TWL at 18 months (Figure 1). A tendency was also found nals rather than by a change in experienced palatability (35). This
learned adjustment was hypothesized to be caused by conditioned decrease in intake from before surgery to after surgery was compa-
taste avoidance in which the triggering foods can still be consumed, rable between RYGB and SG patients (41% and 43% respectively).
as long as the patients learn to reduce consumption to avoid certain Studies comparing the effect of RYGB and SG surgery on food
postingestive signals or responses (36). Thus, one possibility was preferences are scarce. In a pilot study, El Labban et al. did not
that energy intake at 6 months was too low to trigger these postpran- detect any major differences in food intake and preferences between
dial visceral signals and, consequently, a shift in food chosen at the RYGB and SG operated patients (37). Nance et al. compared pre-
buffet meal or that learned adjustment to conditioned taste avoidance to postoperative changes in eating behavior and detected similar
progresses over time so that 6 months postsurgery was too early for changes after RYGB and SG surgery (30). Thus, in spite of different
behavioral changes to set in. However, we were not able to confirm anatomic changes following RYGB and SG surgery, these proce-
our hypothesis, even though energy intake increased 25% between 6 dures seem to have similar outcomes on dietary intake and food
and 18 months after surgery. preferences.
To fully explore our hypothesis, we divided the subjects into tertiles When measuring food preferences by means of verbal report, we
according to total energy consumed after surgery. Food preferences found no change in subjects’ choice of picture from the different
changed in both the low and high energy intake group in opposite direc- food categories between presurgery and 18 months postsurgery.
tions. However, these changes were contrary to our hypotheses. In the However, at the assessment 6 months after surgery, patients reported
high energy intake group, patients consumed more food from the high- an increased preference for low-fat savory foods compared with
fat category; hence, this group may either have had a higher threshold before surgery, which is in line with the dietary advice received as
for triggering postprandial visceral signals or a less profound biological part of the bariatric surgical program. These results could indicate
response to these visceral signals compared with the group with lower that patients are more aware of the nutritional recommendations in
energy intake. the early postoperative period, whereas this awareness seems to fade
with time after surgery.
Thus, we can preclude that our previous findings 6 months after sur-
gery were caused by a low energy intake or an early assessment of Assessing food preferences by targeting direct behavior is a major
food preferences occurring before adaptation to conditioned taste strength of this study. However, the experimental setting of the meal
avoidance. has some limitations, which have previously been described (13).
Briefly, we cannot preclude that the social desirability of healthy
We found no associations between postoperative experiences of nega- eating might influence the choice of food at the buffet meal, and
tive responses related to eating and food preferences at the buffet meal. whether the assessed behavior at the buffet meal test reflects actual
This result is not caused by a low incidence of subjects reporting post- behavior outside the experimental setting can be questioned. The
prandial discomfort since all patients reported one or more experiences standardized liquid meals consumed prior to the buffet meal were
with unpleasant physiological responses to food after surgery. As early predominantly “sweet meals” (e.g., chocolate and chocolate mint
as 6 weeks after surgery, 95% of the subjects reported postprandial flavor). This could have reduced intake of sweet foods at the buf-
discomfort, indicating that patients, despite receiving nutritional coun- fet meal because of reduced liking for sweetness caused by sen-
seling as part of the bariatric surgery program, encountered food that sory-specific satiety (38). Such an effect would be present at all
caused visceral malaise. visits, and also before surgery, potentially limiting the ability to
detect a decrease in preference for sweet foods following surgery.
Additionally, the low number of SG participants (n = 10) limited the
Even though we found no consistent changes in food preferences
ability to make specific conclusions regarding the effect of SG sur-
for the entire cohort of patients, changes in high fat intake, protein
gery on food preferences.
intake, total energy intake, and energy density seem to be predic-
tive of the postoperative weight loss. The decrease in energy intake,
energy density, and intake of high-fat foods and the increase in pro-
tein intake from before surgery to 6 months after surgery predicted Conclusion
the extent of %TWL at 18 months. The association between changes Data from this 18-month follow-up study confirmed our previous
in high-fat food and %TWL at 18 months after surgery was still sig- findings that RYGB surgery and SG surgery do not consistently af-
nificant when analyzing changes in intake from before surgery to fect food preferences in humans. Energy intake was still consider-
18 months after surgery. These results suggest that changes in food ably decreased; however, we found no overall changes in relative
preferences, especially in the early postoperative period, could be intake of high-fat, low-fat, sweet, and savory foods; macronutrient
important markers for weight loss success following surgery because intake; or energy density of the meal. These results conflict with
they explained up to 39% of the variability in later weight loss. With previous results based on verbal report measures, emphasizing the
the potential of identifying patients in need of additional support to need for further studies investigating changes in food preferences by
improve their weight loss success, this association should be further targeting direct behavior. This is especially important if changes in
investigated. energy intake and food preferences can predict postoperative weight
loss, as our data indicate, because this will strengthen identification
In spite of a larger weight loss in RYGB compared with SG patients, of subjects in need of additional early support to optimize weight
we found no changes in food preferences when stratifying subjects loss.O
according to surgery or differences between surgical groups. Energy
consumed at the meal was higher in RYGB patients; however, the © 2018 The Obesity Society
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