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Long-term changes in dietary intake and its association with eating-related problems after gastric bypass in adolescents

Open AccessPublished:August 22, 2022DOI:https://doi.org/10.1016/j.soard.2022.08.008

      Abstract

      Background

      Roux-en-Y gastric bypass (RYGB) surgery is an established, effective treatment for severe adolescent obesity. Long-term dietary intake and the relationship to eating-related problems are scarcely evaluated in this population.

      Objectives

      Assess changes in dietary intake in adolescents after RYGB and explore associations between dietary intake and eating-related problems.

      Setting

      : Multicenter study in Swedish university hospitals.

      Method

      Diet history, binge eating scale (BES), and Three-Factor Eating Questionnaire were assessed preoperatively and 1, 2, and 5 years after RYGB in 85 adolescents (67% female) aged 16.5 ± 1.2 years with a body mass index (BMI) of 45.5 ± 6.0 kg/m2 and compared with control individuals at 5 years.

      Results

      Five-year BMI change was –28.6% ± 12.7% versus +9.9% ± 18.9% in RYGB patients versus control individuals (P < .001). Through 5 years, RYGB adolescents reported reduced energy intake, portion size of cooked meals at dinner, and milk/yoghurt consumption (P < .01). The BES scores were 9.3 ± 8.3 versus 13.4 ± 10.5 in RYGB patients versus control individuals (P = .04). Association between BES score and energy intake was stronger in control individuals (r = .27 versus r = .62 in RYGB patients versus control individuals, P < .001). At 5 years, lower energy intake was associated with greater BMI loss in all adolescents (r = .33, P < .001). Higher scores in BES and uncontrolled and emotional eating were associated with higher energy intake, cooked meals, candies/chocolates, cakes/cookies, desserts, and sugary drinks (r > .23, P < .04) and lower intake of fruits/berries (r = –.32, P = .044). A higher score in cognitive restraint was associated with a higher intake of cereals and fruits/berries (r > .22, P < .05) and a lower intake of sugary drinks (r = –.24, P < .03).

      Conclusion

      To support optimization of long-term outcomes in adolescent RYGB patients, it is important to provide management strategies to reduce energy intake. Monitoring eating-related problems could identify potential individuals at risk of poor weight loss and to initiate treatment interventions.

      Keywords

      Adolescent bariatric surgery is an efficacious and durable intervention for patients with severe obesity, with long-term weight loss, remission or improvement of co-morbidities, and improvement in physical and weight-related quality of life [
      • Chalklin C.G.
      • Ryan Harper E.G.
      • Beamish A.J.
      Metabolic and bariatric surgery in adolescents.
      ]. The mechanisms behind Roux-en-Y gastric bypass (RYGB) surgery are complex and involve gut hormones, altered neural responses, and increased gut bacterial variety, which together reduce food intake and increase weight loss by decreasing hunger and increasing satiety and energy expenditure [
      • Chalklin C.G.
      • Ryan Harper E.G.
      • Beamish A.J.
      Metabolic and bariatric surgery in adolescents.
      ]. The first couple of years after RYGB, when the greatest amount of the weight loss is achieved, dietary intake is altered with reduced energy intake and shifts in food choices, with lower intake of cooked meals, vegetables, milk and yoghurt, sugary drinks, desserts, and candy, while the intake of fruits and berries is higher [
      • Abdeen G.
      • le Roux C.W.
      Mechanism underlying the weight loss and complications of Roux-en-Y gastric bypass.
      ,
      • Miller G.D.
      • Norris A.
      • Fernandez A.
      Changes in nutrients and food groups intake following laparoscopic Roux-en-Y gastric bypass (RYGB).
      ,
      • Laurenius A.
      • Larsson I.
      • Melanson K.J.
      • et al.
      Decreased energy density and changes in food selection following Roux-en-Y gastric bypass.
      ,
      • Ernst B.
      • Thurnheer M.
      • Wilms B.
      • Schultes B.
      Differential changes in dietary habits after gastric bypass versus gastric banding operations.
      ,
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Five-year changes in dietary intake and body composition in adolescents with severe obesity undergoing laparoscopic Roux-en-Y gastric bypass surgery.
      ].
      Eating-related problems such as binge eating (BE), eating an objectively large amount of food during a limited time with the sense of loss of control, can influence an individual’s ability to regulate energy intake [
      • Treasure J.
      • Duarte T.A.
      • Schmidt U.
      Eating disorders.
      ]. Eating-related problems are reduced after bariatric surgery, but they may resurge or increase long term and are linked to poor weight loss or weight regain [
      • Williams-Kerver G.A.
      • Steffen K.J.
      • Mitchell J.E.
      Eating pathology after bariatric surgery: an updated review of the recent literature.
      ,
      • Järvholm K.
      • Olbers T.
      • Peltonen M.
      • et al.
      Binge eating and other eating-related problems in adolescents undergoing gastric bypass: results from a Swedish nationwide study (AMOS).
      ].
      There are not many reports on the relationship between dietary intake and eating-related problems after bariatric surgery. In adults, eating-related problems were decreased and portion sizes were reduced 2 years after RYGB surgery [
      • Laurenius A.
      • Larsson I.
      • Bueter M.
      • et al.
      Changes in eating behaviour and meal pattern following Roux-en-Y gastric bypass.
      ]. In adolescents after bariatric surgery, eating-related problems had greater reductions compared with adolescents on nonsurgical treatment at 1 year, but there was no difference in energy intake between the groups [
      • Sarwer D.B.
      • Dilks R.J.
      • Spitzer J.C.
      • et al.
      Changes in dietary intake and eating behavior in adolescents after bariatric surgery: an ancillary study to the Teen-LABS Consortium.
      ].
      In this study, we aim to investigate long-term changes in dietary intake after RYGB and explore the relationship between dietary intake and eating-related problems in adolescents after RYGB and nonsurgical lifestyle treatment for weight loss. We hypothesize that higher scores in eating-related problems after RYGB are associated with more unhealthy traits of dietary intake. Understanding the relationship between dietary intake and eating-related problems provides useful information and helps advance strategies to support optimization of long-term outcome of RYGB in adolescents.

      Materials and methods

      Study design

      This study is part of the Swedish nationwide multicenter study Adolescent Morbid Obesity Surgery (AMOS) study, which is a prospective, nonrandomized, comparative observational study examining the long-term safety and efficacy of RYGB in adolescents versus a matched cohort of adolescents on nonsurgical lifestyle treatment identified from the Swedish Childhood Obesity Treatment Register (BORIS) [
      • Hagman E.
      • Danielsson P.
      • Lindberg L.
      • Marcus C.
      Paediatric obesity treatment during 14 years in Sweden: lessons from the Swedish Childhood Obesity Treatment Register-BORIS.
      ]. The AMOS cohort and the matched control group have been described in detail elsewhere [
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Five-year changes in dietary intake and body composition in adolescents with severe obesity undergoing laparoscopic Roux-en-Y gastric bypass surgery.
      ]. The regional ethics committee approved the study protocol (523-04), and the study was conducted according to the Declaration of Helsinki and registered in ClinicalTrials.gov (NCT00289705). Informed consent was obtained from adolescents and parents/caregivers. All treatments were subsidized by the Swedish healthcare system.

      Procedure

      Inclusion in the AMOS study ran between 2006 and 2009 via the 3 largest childhood obesity centers in Sweden: Stockholm, Gothenburg, and Malmo. Laparoscopic RYGB was performed according to protocol, described in detail elsewhere [
      • Olbers T.
      • Gronowitz E.
      • Werling M.
      • et al.
      Two-year outcome of laparoscopic Roux-en-Y gastric bypass in adolescents with severe obesity: results from a Swedish Nationwide Study (AMOS).
      ]. All adolescents had participated in nonsurgical lifestyle treatment for weight loss for at least 1 year prior to inclusion [
      • Olbers T.
      • Gronowitz E.
      • Werling M.
      • et al.
      Two-year outcome of laparoscopic Roux-en-Y gastric bypass in adolescents with severe obesity: results from a Swedish Nationwide Study (AMOS).
      ]. This treatment consisted of individualized or family-based counseling and lifestyle support concerning dietary intake and physical activity [
      • Danielsson P.
      • Svensson V.
      • Kowalski J.
      • Nyberg G.
      • Ekblom O.
      • Marcus C.
      Importance of age for 3-year continuous behavioral obesity treatment success and dropout rate.
      ]. After RYGB, adolescents received nutritional recommendations based on international guidelines [
      • Pratt J.S.A.
      • Browne A.
      • Browne N.T.
      • et al.
      ASMBS pediatric metabolic and bariatric surgery guidelines, 2018.
      ]. Adolescents were assessed in person at a local study site for baseline inclusion and at 1-, 2-, and 5-year follow-up research visits. For control individuals, anthropometric data were retrieved from the BORIS registry for baseline inclusion and assessed at an in-person research visit at 5 years. Thus, the control group was not treated according to a prospective protocol. Research coordinators performed anthropometric measurements and collected eating-related problem questionnaires. Trained dieticians completed dietary assessments by interview.

      Measurements

      Anthropometric measurements. Height was measured to the closest .5 cm using a wall-mounted stadiometer in standing position. Weight was measured in light clothing to the nearest .1 kg on electronic scales calibrated at regular intervals. BMI was calculated as weight (in kilograms) by height (in meters squared).
      Dietary intake. Dietary intake was assessed with an interviewer-administered structured diet history questionnaire validated for energy intake in normal-weight adolescents [
      • Sjoberg A.
      • Slinde F.
      • Arvidsson D.
      • et al.
      Energy intake in Swedish adolescents: validation of diet history with doubly labelled water.
      ], described in detail elsewhere [
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Five-year changes in dietary intake and body composition in adolescents with severe obesity undergoing laparoscopic Roux-en-Y gastric bypass surgery.
      ]. The diet history questionnaire is divided into sections to capture intake during different time periods of the day: main meals (i.e., breakfast, lunch, and dinner) and snacks in-between meals (i.e., before noon, afternoon, evening, and night) (Supplementary Table 1). Food choices were divided into 13 categories (Supplementary Table 1). Dietary intake was assessed by energy intake (in kilocalories) and food weight (in grams), including food and beverages and excluding energy-free drinks such as water, bottled water, and diet sodas.
      Eating-related problems. Eating-related problems were assessed with 2 self-report questionnaires, the binge eating scale (BES) and the Three-Factor Eating Questionnaire (TFEQ-R21). The BES consists of 16 items assessing behaviors, cognitions, and feelings related to BE (eating an objectively large amount of food during a limited time with a sense of loss of control) [
      • Gormally J.
      • Black S.
      • Daston S.
      • Rardin D.
      The assessment of binge eating severity among obese persons.
      ]. The BES is considered a valid screener for BE in bariatric surgery samples using a score >17 as a cutoff [
      • Grupski A.E.
      • Hood M.M.
      • Hall B.J.
      • Azarbad L.
      • Fitzpatrick S.L.
      • Corsica J.A.
      Examining the binge eating scale in screening for binge eating disorder in bariatric surgery candidates.
      ]. The TFEQ-R21 is comprised of 21 items and assesses 3 aspects of eating-related problems: uncontrolled eating (UE; difficulties with regulating eating in relation to food exposure or hunger), emotional eating (EE; eating as a response to negative emotions), and cognitive restraint (CR; trying consciously to restrict eating) [
      • Karlsson J.
      • Persson L.O.
      • Sjostrom L.
      • Sullivan M.
      Psychometric properties and factor structure of the Three-Factor Eating Questionnaire (TFEQ) in obese men and women: results from the Swedish Obese Subjects (SOS) study.
      ]. Scaled scores range from 0 to 100, and higher scores indicate more of the respective eating-related problem.

      Statistics

      Mean ± standard deviation, median (range), and percentage were used to describe data. Body weight change and BMI changes were calculated as body weight (or BMI) change = ([baseline weight (or BMI) – current weight (or BMI)] ÷ baseline weight (or BMI)) × 100. Excess BMI change was calculated as % excess BMI change = ([baseline BMI – current BMI] ÷ [baseline BMI – 25]) × 100. Energy intake was calculated as energy intake (kcal/kg ideal body weight/day) = total energy intake (kcal/day) ÷ weight (kg) at BMI 25. Significance was set at P < .05 (2-sided). Data were checked for normality by the Shapiro–Wilk test. A paired-samples t test and a Wilcoxon signed-rank test were used to compare continuous variables within groups, and an independent-samples t test (Student t test) and a Mann–Whitney U test were used to compare continuous variables between groups, as appropriate. Correlation coefficients were calculated using Pearson’s and Spearman’s rho, as appropriate. A χ2 test was applied on categorical data. A general linear model was used to test the relationship between energy intake and BE, UE, EE, and CR, respectively. Energy intake was adjusted for sex, age, and height. Variables were transformed to normality using Box–Cox transformation expressed as z scores. Model validity was ascertained by residual analysis. The statistical calculations were performed using IBM SPSS Statistical Software for Mac (version 23; IBM, Armonk, NY, USA).

      Results

      Dietary assessment/eating-related problem assessments were completed in 98%/95% of the RYGB adolescents at baseline, 93%/98% at 1 year, 87%/87% at 2 years, and 75%/88% at 5 years and in 65%/65% of the adolescent control individuals at 5 years.

      Participants

      The study group consisted of 85 participants (67% female) aged 16.5 ± 1.2) years with a BMI of 45.5 ± 6.0 kg/m2 undergoing RYGB. The control group consisted of 62 adolescents (58% female) aged 15.6 ± 1.4 years with a BMI of 40.2 ± 6.6 kg/m2. Despite matching, adolescents in the control group were younger and had lower baseline BMIs (P < .001) [
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Five-year changes in dietary intake and body composition in adolescents with severe obesity undergoing laparoscopic Roux-en-Y gastric bypass surgery.
      ]. For 5-year characteristics and comparison between self-reported dietary intake and eating-related problems between RYGB adolescents and control individuals, see Table 1. Patient characteristics, energy intake, and total food weight have been reported previously [
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Five-year changes in dietary intake and body composition in adolescents with severe obesity undergoing laparoscopic Roux-en-Y gastric bypass surgery.
      ,
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Micronutrient intake and biochemistry in adolescents adherent or nonadherent to supplements 5 years after Roux-en-Y gastric bypass surgery.
      ].
      Table 1Patient characteristics, self-reported dietary intake, and eating-related problems in adolescents 5 years after gastric bypass surgery and in adolescent control individuals at 5 years
      FactorSurgery (n = 64)Control (n = 40)P value, surgery versus control
      Patient characteristics
       Female, n (%)
      Surgery: n = 85, control: n = 62.
      6758.264
      Pearson χ2.
       Age (yr), median (range)
      Surgery: n = 85, control: n = 62.
      21.9 (19–25)20.7 (18–24)<.001
       Body weight (kg)
      Surgery: n = 85, control: n = 62.
      96.1 ± 22.1130.4 ± 27.6<.001
       Body weight change (%)
      Surgery: n = 85, control: n = 62.
      –27.5 ± 12.7+13.0 ± 19.5<.001
      Adjusted for sex, baseline body weight, BMI, and age.
       BMI (kg/m2)
      Surgery: n = 85, control: n = 62.
      32.3 ± 6.343.9 ± 9.1<.001
       BMI change (%)
      Surgery: n = 85, control: n = 62.
      –28.6 ± 12.7+9.9 ± 18.9<.001
      Adjusted for sex, baseline body weight, BMI, and age.
       Excess BMI change (%)
      Surgery: n = 85, control: n = 62.
      –65.7 ± 29.2+52.5 ± 129.3<.001
      Adjusted for sex, baseline body weight, BMI, and age.
      Total intake
       Energy intake (kcal/kg IBW/d)31 ± 1345 ± 19<.001
       Total energy intake (kcal/d)2300 ± 8973317 ± 1426<.001
       Total food weight (g)2257 ± 11562654 ± 1037.021
      Food choices
       Cooked meals (g/d)587 ± 261764 ± 324.003
       Vegetables (g/d)188 ± 145247 ± 158.051
       Sandwiches (g/d)209 ± 150311 ± 274.084
       Cereals (g/d)22 ± 5321 ± 35.108
       Fruits and berries (g/d)134 ± 26499 ± 116.793
       Milk and yoghurt (g/d)173 ± 214355 ± 447.007
       Sugary drinks (g/d)287 ± 592465 ± 583.003
       Alcoholic drinks (g/d)203 ± 45388 ± 217.089
       Desserts (g/d)16 ± 6640 ± 107.099
       Salty snacks (g/d)32 ± 3928 ± 41.483
       Candies and chocolates (g/d)35 ± 4270 ± 103.092
       Cakes and cookies (g/d)6 ± 1918 ± 56.167
       Coffee and tea (g/d)359 ± 497139 ± 210.001
      Eating-related problems
       Binge eating (BES score)9.3 ± 8.313.4 ± 10.5
      n = 40. Higher BES scores represent more binge eating (range: 0–46). Higher TFEQ scores represent more uncontrolled eating, emotional eating, or cognitive restraint (range: 0–100). Variables were transformed to normality for analysis. The Student t test and Mann–Whitney U test were used to compare groups. Values are shown in number, percentage, median (range), mean ± standard deviation.
      .035
       Uncontrolled eating (TFEQ score)27.9 ± 20.637.5 ± 27.5.057
       Emotional eating (TFEQ score)25.2 ± 27.234.7 ± 30.0.087
       Cognitive restraint (TFEQ score)50.2 ± 23.752.4 ± 22.6.639
      BMI = body mass index; IBW = ideal body weight; BES = binge eating scale; TFEQ = three Factor Eating Questionnaire.
      Surgery: n = 85, control: n = 62.
      Pearson χ2.
      Adjusted for sex, baseline body weight, BMI, and age.
      § n = 40. Higher BES scores represent more binge eating (range: 0–46). Higher TFEQ scores represent more uncontrolled eating, emotional eating, or cognitive restraint (range: 0–100). Variables were transformed to normality for analysis. The Student t test and Mann–Whitney U test were used to compare groups. Values are shown in number, percentage, median (range), mean ± standard deviation.

      Dietary intake

      Energy intake was lower in RYGB adolescents at 5 years than in control individuals (Table 1). Relative BMI change (%) was associated with energy intake at 5 years, expressed as total daily energy intake (kcal/day; r = .31, P = .001) or energy intake per ideal body weight (kcal/kg ideal body weight/day; r = .33, P < .001) (Table 1). However, there was no significant association between BMI change (%) and energy intake when analyzing the RYGB and control groups separately. Through 5 years after RYGB, adolescents reported reduced intake of cooked meals and milk and yoghurt, whereas consumption of alcoholic drinks and coffee and tea was increased (P < .05, for all) (Supplementary Fig. 1). At 5 years, RYGB adolescents reported a lower intake of cooked meals, milk and yoghurt, and sugary drinks and a higher intake of coffee and tea compared with control individuals (Table 1). RYGB adolescents reported consuming sugary drinks at 55% versus 80% in control individuals (P = .006), including 8% consuming ≥1 L of sugary drinks per day versus 18% in controls. Through 5 years after RYGB, portion size of dinner was reduced, and both lunch and dinner were smaller than in control individuals (Fig. 1A, 1B).
      Figure thumbnail gr1
      Figure 1Longitudinal changes in self-reported portion size (g) of main meals (A) and snacks in-between meals (B) in adolescents after gastric bypass, and differences in portion size at 5 years compared with adolescent controls. g = grams. Solid green, red, blue, and purple lines denote mean group measurements in adolescents after gastric bypass. ♦ denote mean group measurements in controls for breakfast (A), and before noon snack (B). ▪ denote mean group measurements in controls for lunch (A), and afternoon snack (B). ○ denote mean group measurements in controls for dinner (A), and evening snack (B). ✖ denote mean group measurements in controls for night snack (B). ∗P < .05, ∗∗P < .01, ∗∗∗P < .001, +changes from baseline, #between-group difference

      Dietary intake and eating-related problems

      RYGB adolescents reported lower BES scores than control individuals (Table 1). Table 2 shows the associations between eating-related problems and energy intake in adolescents before and 5 years after RYGB and in control individuals at 5 years. The BES score was associated with energy intake in adolescents before and 5 years after RYGB (r = .39, P < .001 and r = .27, P = .044) and in control individuals at 5 years (r = .62, P < .001), with a significant difference between groups at 5 years (P < .001) (Table 2). Proportion of adolescents screening positive for BE (BES score >17) at 5 years was lower than before surgery (12% versus 37%; P = .010) and lower than in control individuals at 5 years (30%; P = .050) (Table 3). Screening positive for BE or not before surgery did not predict differences in any of the weight or dietary intake parameters after surgery (P > .2, for all). At 5 years, the BES score was associated with cooked meals (r = .29; P = .011, RYGB), candies and chocolates (r = .23, P = .037 and r = .48, P = .004, RYGB and control, respectively), cakes and cookies (r = .26, P = .021 and r = .38, P = .022, RYGB and control, respectively), and fruits and berries (r = –.32, P = .044, control). UE was associated with desserts (r = .50, P = .005, control), candies and chocolates (r = .29, P = .026 and r = .54, P = .002, RYGB and control, respectively), and milk and yoghurt (r = –.35, P = .005 and r = .41, P = .026, RYGB and control, respectively). EE was associated with cooked meals (r = .32, P = .013, RYGB) and sugary drinks (r = .31, P = .052, control). CR was associated with cereals (r = .22, P = .047, RYGB), fruits and berries (r = .30, P = .009 and r = .33, P = .038, RYGB and control, respectively), and sugary drinks (r = –.24, P = .029, RYGB).
      Table 2Associations between self-reported energy intake and eating-related problems (binge eating, uncontrolled eating, emotional eating, and cognitive restraint) in adolescents before gastric bypass surgery and 5 years after and compared with adolescent control individuals at 5 years
      Eating-related problemSurgery, baseline (n = 80)Surgery, 5 yr (n = 60)Difference between baseline and 5-yr correlationDifference between baseline and 5-yr slopeControl individuals, 5 yr (n = 31)Difference between groups at 5 yr
      R2
      Coefficient of determination in univariate model.
      Beta
      Energy intake kcal/day (adjusted for sex, age, and height) per standard deviation of eating-related problem score.
      (kcal/d)
      P valueR2
      Coefficient of determination in univariate model.
      Beta
      Energy intake kcal/day (adjusted for sex, age, and height) per standard deviation of eating-related problem score.
      (kcal/d)
      P valueP valueP valueR2
      Coefficient of determination in univariate model.
      Beta
      Energy intake kcal/day (adjusted for sex, age, and height) per standard deviation of eating-related problem score.
      (kcal/d)
      P valueBeta
      Energy intake kcal/day (adjusted for sex, age, and height) per standard deviation of eating-related problem score.
      (kcal/d)
      P value
      Binge eating.154411<.001.075282.044.785.453.381698<.001416<.001
      Uncontrolled eating.144402<.001.107332.013.542.682.453846<.001514.015
      Emotional eating.093324.006.155365.006.109.805.128475.012110.628
      Cognitive restraint.080–301.011.061–252.103.689.785.00028.906280.323
      Coefficient of determination in univariate model.
      Energy intake kcal/day (adjusted for sex, age, and height) per standard deviation of eating-related problem score.
      Table 3Patient characteristics, self-reported dietary intake (energy intake, food weight, meal frequency, portion sizes, and food choices) in adolescents before gastric bypass surgery and 5 years after and in adolescent control individuals at 5 years split by binge eating (binge eating scale score >17) and no binge eating (binge eating scale score ≤17)
      FactorSurgery, baseline (n = 81)Surgery, 5 yr (n = 75)Control individuals, 5 yr (n = 41)
      Binge eating (37%)No binge eating (63%)P valueBinge eating (12%)No binge eating (88%)P valueBinge eating (30%)No binge eating (70%)P value
      Patient characteristics
       Sex (female/male)22/832/19.3297/242/24.40311/110/18.001
       Age (yr)16.6 ± 1.216.5 ± 1.2.69922.0 ± 1.022.0 ± 1.2.89520.9 ± 1.420.1 ± 1.3.743
       Age (yr), median (range)16.5 (15–19)16.8 (14–18)22.2 (21–23)22.1 (19–25)20.8 (18–23)20.9 (18–23)
       Body weight (kg)131.6 ± 23.7133.4 ± 21.4.737100.4 ± 19.695.6 ± 22.4.293132.6 ± 28.4133.4 ± 22.5.921
       Body weight change (%)–24.6 ± 12.2–28.0 ± 12.9.438+14.3 ± 18.1+10.7 ± 18.3.502
       BMI (kg/m2)45.0 ± 6.345.7 ± 6.0.48733.9 ± 6.732.0 ± 5.9.42444.8 ± 10.244.3 ± 6.6.864
       BMI change (%)–25.3 ± 12.6–29.2 ± 13.0.366+12.9 ± 17.9+7.1 ± 17.1.309
       Excess BMI change (%)–58.0 ± 31.3–66.6 ± 28.3.404+38.1 ± 51.6+21.5 ± 49.6.358
      Total intake
       Energy intake (kcal/kg IBW/d)38 ± 1733 ± 12
      n = 50.
      .37140 ± 14
      n = 6.
      30 ± 13
      n = 55.
      .08153 ± 21
      n = 10.
      42 ± 19
      n = 19.
      .170
       Total energy intake (kcal/d)2747 ± 12552437 ± 980
      n = 50.
      .2662881 ± 1103
      n = 6.
      2232 ± 875
      n = 55.
      .1144014 ± 1495
      n = 10.
      3172 ± 1515
      n = 19.
      .165
       Total food weight (g)2288 ± 10942233 ± 870
      n = 50.
      .9602337 ± 446
      n = 6.
      2273 ± 1235
      n = 55.
      .3123084 ± 1231
      n = 10.
      2486 ± 961
      n = 19.
      .160
      Meal pattern and portion size
       Breakfast (g/d)397 ± 285493 ± 279
      n = 50.
      .086436 ± 189
      n = 6.
      531 ± 382
      n = 55.
      .753927 ± 1017
      n = 10.
      486 ± 323
      n = 19.
      .168
       Lunch (g/d)797 ± 370755 ± 273
      n = 50.
      .599974 ± 308
      n = 6.
      666 ± 342
      n = 55.
      .031953 ± 405
      n = 10.
      842 ± 399
      n = 19.
      .291
       Dinner (g/d)896 ± 375875 ± 336.773912 ± 272
      n = 6.
      753 ± 244
      n = 55.
      .1461008 ± 465
      n = 10.
      1074 ± 307
      n = 19.
      .680
       Snack (before noon) (g/d)90 ± 15789 ± 128
      n = 50.
      .990186 ± 201
      n = 6.
      167 ± 252
      n = 55.
      .617203 ± 275
      n = 10.
      177 ± 347
      n = 19.
      .752
       Snack (afternoon) (g/d)189 ± 252170 ± 164
      n = 50.
      .725177 ± 175
      n = 6.
      186 ± 222
      n = 55.
      .788307 ± 329
      n = 10.
      283 ± 406
      n = 19.
      .402
       Snack (evening) (g/d)236 ± 237234 ± 211
      n = 50.
      .964214 ± 143
      n = 6.
      260 ± 223
      n = 55.
      .884331 ± 349
      n = 10.
      355 ± 322
      n = 19.
      .890
       Snack (night) (g/d)1.5 ± 8.620 ± 83
      n = 50.
      .11987 ± 213
      n = 6.
      22 ± 136
      n = 55.
      .40113 ± 32
      n = 10.
      78 ± 237
      n = 19.
      .592
      Food choices
       Cooked meals (g/d)801 ± 343737 ± 224
      n = 50.
      .633872 ± 383
      n = 6.
      556 ± 235
      n = 55.
      .028678 ± 317
      n = 10.
      762 ± 335
      n = 19.
      .573
       Vegetables (g/d)231 ± 238225 ± 109
      n = 50.
      .164381 ± 288
      n = 6.
      165 ± 105
      n = 55.
      .034253 ± 167
      n = 10.
      246 ± 161
      n = 19.
      .839
       Sandwiches (g/d)231 ± 185237 ± 169
      n = 50.
      .658231 ± 140
      n = 6.
      195 ± 139
      n = 55.
      .562317 ± 193
      n = 10.
      376 ± 352
      n = 19.
      .982
       Cereals (g/d)14 ± 4816 ± 43
      n = 50.
      .27046 ± 112
      n = 6.
      21 ± 45
      n = 55.
      .56220 ± 31
      n = 10.
      22 ± 40
      n = 19.
      .982
       Fruits and berries (g/d)51 ± 7572 ± 108
      n = 50.
      .34358 ± 97
      n = 6.
      146 ± 282
      n = 55.
      .455109 ± 104
      n = 10.
      94 ± 128
      n = 19.
      .735
       Milk and yoghurt (g/d)375 ± 447405 ± 349
      n = 50.
      .43596 ± 112
      n = 6.
      187 ± 224
      n = 55.
      .427595 ± 757
      n = 10.
      308 ± 281
      n = 19.
      .804
       Sugary drinks (g/d)375 ± 521291 ± 465
      n = 50.
      .380134 ± 276
      n = 6.
      314 ± 629
      n = 55.
      .399552 ± 517
      n = 10.
      357 ± 554
      n = 19.
      .138
       Alcoholic drinks (g/d)67 ± 12671 ± 154
      n = 50.
      .66792 ± 185
      n = 6.
      224 ± 482
      n = 55.
      .20080 ± 64
      n = 10.
      111 ± 309
      n = 19.
      .228
       Desserts (g/d)28 ± 7211 ± 23
      n = 50.
      .1879 ± 10
      n = 6.
      18 ± 71
      n = 55.
      .427112 ± 198
      n = 10.
      13 ± 25
      n = 19.
      .735
       Salty snacks (g/d)38 ± 4820 ± 28
      n = 50.
      .12023 ± 27
      n = 6.
      31 ± 38
      n = 55.
      .69737 ± 41
      n = 10.
      33 ± 51
      n = 19.
      .636
       Candies and chocolate (g/d)53 ± 5839 ± 39
      n = 50.
      .38288 ± 66
      n = 6.
      30 ± 35
      n = 55.
      .020151 ± 166
      n = 10.
      34 ± 49
      n = 19.
      .008
       Cakes and cookies (g/d)3 ± 72 ± 8
      n = 50.
      .84127 ± 44
      n = 6.
      4 ± 14
      n = 55.
      .48546 ± 105
      n = 10.
      5 ± 13
      n = 19.
      .138
       Coffee and tea (g/d)22 ± 51108 ± 182
      n = 50.
      .014280 ± 304
      n = 6.
      378 ± 527
      n = 55.
      .823134 ± 180
      n = 10.
      120 ± 213
      n = 19.
      .769
      BMI = body mass index; IBW = ideal body weight.
      Pearson’s χ2 test was used to compare relationships between categorical variables. The independent-samples t test (Student t test) and Mann–Whitney U test were used to compare continuous variables between groups, and the paired-samples t test and Wilcoxon signed-rank test were used to compare continuous variables within groups. Values are shown in number, percentage, mean ± standard deviation, and median (range).
      n = 50.
      n = 6.
      n = 55.
      § n = 10.
      n = 19.

      Discussion

      This study is the first to investigate long-term changes in dietary intake and the associations between dietary intake and eating-related problems after RYGB in adolescents and marks the beginning of the exploration of how dietary and behavioral counseling strategies can help improve long-term outcomes for bariatric surgery. Long-term dietary intake in adolescents after RYGB is accentuated by reduced energy intake, portion size of cooked meals at dinner, and milk and yoghurt and increased intake of alcoholic drinks and coffee. Eating-related problems before surgery do not predict dietary intake after surgery. An association between BES score and energy intake is more pronounced in adolescents on nonsurgical lifestyle treatment at 5 years. As hypothesized, BE, UE, and EE are associated with more unhealthy food-choice traits, whereas CR is associated with healthier food choices.
      Short-term results confirm the changes seen in adults after RYGB with reduced energy intake and lower intake of cooked meals, vegetables, milk and yoghurt, sugary drinks, desserts, and candy, whereas intake of fruits and berries is higher [
      • Miller G.D.
      • Norris A.
      • Fernandez A.
      Changes in nutrients and food groups intake following laparoscopic Roux-en-Y gastric bypass (RYGB).
      ,
      • Laurenius A.
      • Larsson I.
      • Melanson K.J.
      • et al.
      Decreased energy density and changes in food selection following Roux-en-Y gastric bypass.
      ,
      • Ernst B.
      • Thurnheer M.
      • Wilms B.
      • Schultes B.
      Differential changes in dietary habits after gastric bypass versus gastric banding operations.
      ].
      Reported energy intake in adolescents 5 years after RYGB is similar to that in Swedish adolescents [
      • Moraeus L.
      • Lemming E.W.
      • Hursti U.K.
      • et al.
      Riksmaten Adolescents 2016–17: a national dietary survey in Sweden—design, methods, and participation.
      ] and approximately 1000 calories less than that in control individuals, also reported earlier [
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Five-year changes in dietary intake and body composition in adolescents with severe obesity undergoing laparoscopic Roux-en-Y gastric bypass surgery.
      ]. This study reveals that the dietary composition behind the differences in energy intake between surgically treated adolescents and control individuals is mainly driven by less intake of milk and yoghurt and sugary drinks and smaller portions of cooked meals at lunch and dinner.
      Adolescents after RYGB report consuming about half as much milk and yoghurt than control individuals, which is about 40% lower than what has been reported in Swedish adolescents with normal weight [
      • Moraeus L.
      • Lemming E.W.
      • Hursti U.K.
      • et al.
      Riksmaten Adolescents 2016–17: a national dietary survey in Sweden—design, methods, and participation.
      ]. Decreased milk consumption after RYGB also has been reported in adults up to 2 years after surgery [
      • Silver H.J.
      • Torquati A.
      • Jensen G.L.
      • Richards W.O.
      Weight, dietary and physical activity behaviors two years after gastric bypass.
      ]. The reason for the decreased consumption was not investigated in this study, but others have found more frequently reported gastrointestinal complaints after dairy consumption in RYGB patients [
      • Westerink F.
      • Beijderwellen H.
      • Huibregtse I.L.
      • et al.
      Lactose after Roux-en-Y gastric bypass for morbid obesity, is it a problem?.
      ]. The low consumption of milk is a concern in relation to previous findings reported from this sample showing low adherence to calcium/vitamin D supplementation [
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Micronutrient intake and biochemistry in adolescents adherent or nonadherent to supplements 5 years after Roux-en-Y gastric bypass surgery.
      ] and a substantial decrease in bone mineral density after surgery [
      • Beamish A.J.
      • Gronowitz E.
      • Olbers T.
      • Flodmark C.E.
      • Marcus C.
      • Dahlgren J.
      Body composition and bone health in adolescents after Roux-en-Y gastric bypass for severe obesity.
      ]. Hence adherence to calcium/vitamin D supplementation is extremely important.
      Adolescents after surgery consume fewer sugary drinks than both control individuals and what has been reported in Swedish adolescents with normal weight [
      • Moraeus L.
      • Lemming E.W.
      • Hursti U.K.
      • et al.
      Riksmaten Adolescents 2016–17: a national dietary survey in Sweden—design, methods, and participation.
      ]. Silver et al. [
      • Silver H.J.
      • Torquati A.
      • Jensen G.L.
      • Richards W.O.
      Weight, dietary and physical activity behaviors two years after gastric bypass.
      ] reported avoidance of sugary drinks in 100% of adults after RYGB. In the present study, 45% of RYGB adolescents and 20% of control individuals did not consume sugary drinks at 5 years. Nevertheless, control individuals consumed 2 servings daily, with 1 in 5 individuals consuming more than 1 L (>33.8 fluid ounces) daily. This is concerning because adolescents in the control group already had severe obesity and a high prevalence of vitamin and mineral deficiencies [
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Micronutrient intake and biochemistry in adolescents adherent or nonadherent to supplements 5 years after Roux-en-Y gastric bypass surgery.
      ].
      There was no difference in the prevalence of hazardous consumption and heavy episodic drinking of alcohol between the RYGB adolescents and control individuals [
      • Henfridsson P.
      • Laurenius A.
      • Wallengren O.
      • et al.
      Five-year changes in dietary intake and body composition in adolescents with severe obesity undergoing laparoscopic Roux-en-Y gastric bypass surgery.
      ]. However, this research reveals that RYGB adolescents consume nearly 4 times more than the average Swedish adolescent [
      • Moraeus L.
      • Lemming E.W.
      • Hursti U.K.
      • et al.
      Riksmaten Adolescents 2016–17: a national dietary survey in Sweden—design, methods, and participation.
      ]. Previous research has found an association between BE before surgery and alcohol consumption after surgery [
      • Miller-Matero L.R.
      • Hamann A.
      • LaLonde L.
      • et al.
      Predictors of alcohol use after bariatric surgery.
      ]. Our results show no difference in consumption of alcoholic drinks between adolescents screening positive for BE before or after surgery. Nevertheless, given the greater sensitivity to alcohol and the risks of addiction after RYGB, directed information and long-term follow-up are essential [
      • Pratt J.S.A.
      • Browne A.
      • Browne N.T.
      • et al.
      ASMBS pediatric metabolic and bariatric surgery guidelines, 2018.
      ].
      As we have previously reported and discussed, RYGB adolescents had consistent improvements in eating-related problems, with 77% remission of BE after 5 years [
      • Jarvholm K.
      • Bruze G.
      • Peltonen M.
      • et al.
      5-year mental health and eating pattern outcomes following bariatric surgery in adolescents: a prospective cohort study.
      ]. Higher scores in BE, UE, and EE after RYGB were associated with less weight loss, whereas CR after surgery was not related to weight loss, but an increase in CR between baseline and 5 years after surgery was noted [
      • Jarvholm K.
      • Bruze G.
      • Peltonen M.
      • et al.
      5-year mental health and eating pattern outcomes following bariatric surgery in adolescents: a prospective cohort study.
      ]. A novel finding is the strong association between BE and energy intake in the non–surgically treated control group, again highlighting the co-occurrence between obesity and loss of control over eating and the necessity of addressing eating-related problems in patients with severe obesity.
      In this study, more CR at the 5-year follow-up is associated with reporting healthier eating (i.e., lower intake of sugary drinks and higher intake of cereals and fruits and berries). CR is often conceptualized as a symptom of disordered eating, where restriction is followed by loss of control over eating. Our results are in line with research showing that some degree of deliberate restriction can be positive for individuals with obesity [
      • Johnson F.
      • Pratt M.
      • Wardle J.
      Dietary restraint and self-regulation in eating behavior.
      ]. However, loss of control over eating is negative, and the relationship between CR and weight loss for individuals with obesity has been contradictory [
      • Liu X.
      • Hanseman D.J.
      • Champagne C.M.
      • et al.
      Predicting weight loss using psychological and behavioral factors: the POUNDS LOST Trial.
      ].
      Eating-related problems before surgery do not predict dietary intake after surgery in adolescents, as also reported in adults [
      • Livhits M.
      • Mercado C.
      • Yermilov I.
      • et al.
      Preoperative predictors of weight loss following bariatric surgery: systematic review.
      ]. This adds on to previous findings suggesting little prognostic value of eating-related problems before surgery on postoperative outcomes [
      • Marek R.J.
      • Ben-Porath Y.S.
      • Heinberg L.J.
      Understanding the role of psychopathology in bariatric surgery outcomes.
      ]. In line with our hypothesis, higher scores in eating-related problems (i.e., BE, UE, and EE) are associated with more unhealthy traits of dietary intake (e.g., higher energy intake with more cooked meals, candies and chocolates, cakes and cookies, desserts, and sugary drinks and less fruits and berries). However, in RYGB adolescents, there is only a weak association between BE and energy intake postoperatively, whereas the association is much stronger in control individuals. This supports the idea that it is much more important to assess loss of control than amount of food after bariatric surgery in adolescents to capture eating-related problems [
      • Marek R.J.
      • Ben-Porath Y.S.
      • Heinberg L.J.
      Understanding the role of psychopathology in bariatric surgery outcomes.
      ].
      Some potential limitations must be addressed. First, the diet history method depends on the individual’s memory and willingness and ability to visualize portion size, which risks participants’ not reporting actual dietary intake [
      • Subar A.F.
      • Freedman L.S.
      • Tooze J.A.
      • et al.
      Addressing current criticism regarding the value of self-report dietary data.
      ]. Second, adolescent control individuals were not under a standardized program. Third, our study does not cover the dropouts from initiated nonsurgical lifestyle treatment in the control group. Fourth, the groups might have been too small to detect relevant differences. Fifth, comparison over studies can be difficult and biased by different ways of classification and quantification of dietary intake and eating-related problems [
      • Williams-Kerver G.A.
      • Steffen K.J.
      • Mitchell J.E.
      Eating pathology after bariatric surgery: an updated review of the recent literature.
      ]. Sixth, caution must be taken when interpreting eating-related problems assessed with noninterviewed questionnaires, especially in adolescents [
      • Decaluwé V.
      • Braet C.
      Assessment of eating disorder psychopathology in obese children and adolescents: interview versus self-report questionnaire.
      ]. Finally, long-term data on dietary intake and its association with eating-related problems after other bariatric surgery procedures are to date unknown and hence should not be expected to be similar to long-term data based on outcome after RYGB. Strengths of the study are that the diet history method captures habitual intake and provides consumption at meal level, collecting the data by interviewing reduces the bias of self-reporting dietary intake, and a good retention rate of participants over 5 years as well as the assessment of several eating-related problems.
      Long-term changes in dietary intake after RYGB in adolescents reveal reduced energy intake, portion size of cooked meals at dinner, and milk and yoghurt and increased intake of alcoholic drinks and coffee. Associations between self-reported energy intake and eating-related problems appear to be weak after surgery. Adolescents who experience eating-related problems should be studied regarding whether dietary and psychological interventions lead to a better outcome.

      Disclosures

      This article is part of the Swedish nationwide 10-year prospective multicenter study Adolescent Morbid Obesity Surgery (AMOS), conducted at 3 childhood obesity centers: Stockholm, Gothenburg, and Malmö. The AMOS study is funded by the Swedish Research Council ( 521-2012-319 ), a Vinnova: Sweden Intervention Bureau Grant ( 2013-01339 ), the Swedish Heart-Lung Foundation , the Research Council of Västra Götalands Regionen ( VGFOUREG-307531 ), and the Swedish Freemason Child foundation, Stockholm.

      Supplementary materials

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