Nutrient Intake, Diet Quality, and Diet Diversity in Irritable Bowel Syndrome and the Impact of the Low FODMAP Diet Heidi M

RESEARCH Original Research

Nutrient Intake, Diet Quality, and Diet Diversity in Irritable Bowel Syndrome and the Impact of the Low FODMAP Diet Heidi M. Staudacher, PhD, RD*; Frances S. E. Ralph, RD*; Peter M. Irving, MA, MD, FRCP; Kevin Whelan, PhD, RD*; Miranda C. E. Lomer, PhD, RD*

ARTICLE INFORMATION ABSTRACT Article history: Background Individuals with irritable bowel syndrome (IBS) may modify their diet, Submitted 21 August 2018 which may pose nutritional risk. Further, some dietary approaches, such as a diet low in Accepted 23 January 2019 fermentable oligosaccharides, disaccharides, monosaccharides, and polyols (FODMAPs), Available online 24 April 2019 are restrictive and may contribute to nutritional inadequacy. Keywords: Objective Our aim was to evaluate habitual nutrient intake, diet quality, and diversity FODMAP in IBS and the effect of a 4-week low FODMAP diet on these parameters compared with Nutrient controls. Diet quality Diet diversity Design Data from two randomized controlled trials were included for this secondary Irritable bowel syndrome analysis. Participants were randomized to low FODMAP diet (n¼63) or control diet (sham diet n¼48, habitual diet n¼19). 2212-2672/Copyright ª 2020 by the Academy of Participants/setting Participants included 130 individuals with IBS referred to a ter- Nutrition and Dietetics. tiary center in London, UK between January 2010 to June 2011 and January 2013 to https://doi.org/10.1016/j.jand.2019.01.017 November 2014. Intervention Participants in one trial were randomized to receive either low FODMAP *Certiﬁed in the United Kingdom. dietary counseling or sham control dietary counseling. In the other, they were randomized to receive low FODMAP dietary counseling or to continue habitual diet. All advice was provided by a specialist dietitian. Main outcome measures Habitual (usual) dietary intake at baseline (n¼130) and after a 4-week intervention period was measured using 7-day food records. Statistical analyses performed Analysis of covariance and c2 tests evaluated differences across groups at 4 weeks. Results When examining habitual intake of individuals with IBS, ﬁber intake was low, with only 6 (5%) achieving the target (30 g/day). In those receiving low FODMAP advice, there was no difference in intake of most nutrients compared with controls. However, there was lower intake of starch (109 g/day) vs habitual control diet (128 g/day; P¼0.030), and higher intake of vitamin B-12 (6.1 mg/day) vs habitual (3.9 mg/day) and sham control diets (4.7 mg/day; P<0.01). Overall scores for diet quality were lower after low FODMAP advice vs habitual control diet (P<0.01). Conclusion This study demonstrates many individuals with IBS fail to meet dietary reference values for multiple nutrients. A 4-week low FODMAP diet, when delivered by a specialist dietitian, does not impact on intake of most nutrients or diet diversity but decreases diet quality compared with control diets. J Acad Nutr Diet. 2020;120(4):535-547.

The Continuing Professional Education (CPE) quiz for this article is available RRITABLE BOWEL SYNDROME (IBS) IS CHARACTERIZED for free to Academy members through the MyCDRGo app (available for iOS and Android devices) and through www.jandonline.org (click on “CPE” in the by recurrent abdominal pain related to defecation or 1 2 menu and then “Academy Journal CPE Articles”). Log in with your Academy altered bowel habit. It affects 11% of individuals and of Nutrition and Dietetics or Commission on Dietetic Registration username negatively impacts health-related quality of life.3 Many and password, click “Journal Article Quiz” on the next page, then click the I “ ” perceive diet is responsible for IBS symptoms and self- Additional Journal CPE quizzes button to view a list of available quizzes. 4 Non-members may take CPE quizzes by sending a request to journal@ restrict multiple foods, often without seeking profes- eatright.org. There is a fee of $45 per quiz (includes quiz and copy of article) sional advice.5 for non-member Journal CPE. CPE quizzes are valid for 1 year after the issue The diet of individuals with IBS has predominantly been date in which the articles are published. evaluated in cross-sectional studies using validated food

ª 2020 by the Academy of Nutrition and Dietetics. JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 535 RESEARCH

frequency questionnaires,6-9 unvalidated food frequency questionnaires,10 and tools that assess self-reported RESEARCH SNAPSHOT intolerance and exclusions.4,5 Two studies assessed di- Research Question: What is the habitual nutrient intake, diet etary intake of individuals with IBS using food records,11,12 quality, and diet diversity in individuals with IBS without a more valid method of assessment than food frequency 13 constipation and does the low FODMAP diet impact on these questionnaires. Both reported lower intakes of fiber compared with national recommendations, but findings parameters compared with control diets? were variable regarding micronutrients such as iron and B Key Findings: In this secondary analysis of two randomized 11,12 vitamins. Foods commonly excluded in the diet of in- controlled trials in IBS, many individuals failed to meet dividuals with IBS are cereals,4 dairy products,4,5,10 and/or 5,10 national recommendations for a number of nutrients, fruits and vegetables. In addition, higher intakes of fast fi 10,14 including fat, ber, iodine, and selenium. A low FODMAP diet, food have been reported, suggesting an overall poorer when delivered by a specialist dietitian, did not significantly quality diet than the healthy population. impact the intake of most nutrients or diet diversity, Dietary restriction of fermentable oligosaccharides, di- however, it led to lower diet quality compared with controls. saccharides, monosaccharides, and polyols (FODMAPs) im- proves symptoms in 50% to 80% of patients with IBS.15,16 Restriction of FODMAPs is based on the principle that after were included and constipation-predominant IBS was incomplete hydrolysis/absorption in the small intestine, excluded, considering the potential impact of restricting these molecules exacerbate symptoms due to their effect on carbohydrates that increase intestinal water.17 Written small intestinal water and colonic gas production.17 informed consent was obtained before study-related pro- Exclusion diets can potentially lead to nutritional in- cedures. Demographic data were collected. adequacy, as demonstrated with a gluten-free diet for celiac Nutrient intake, FODMAP intake, diet quality, and diet di- disease18 or a milk-free diet for allergy.19 There is limited versity are reported at baseline in 130 individuals with IBS. research on the effect of a low FODMAP diet on micronutrient The effect of the low FODMAP diet on these outcomes is re- intake. One 4-week randomized controlled trial of the low ported in a subgroup of 63 individuals who had been ran- FODMAP diet in IBS measured intake of iron and calcium and domized and completed the low FODMAP intervention. This demonstrated lower calcium intake compared with controls was compared with the dietary data for individuals ran- following a habitual diet. 20 Another study used a food fre- domized to the control diets (sham diet n¼48, habitual diet quency questionnaire and found that intake of a range of n¼19) (Figure). micronutrients at 6 to 18 months after low FODMAP dietary Participants were advised to continue their habitual diet advice were adequate,21 although in contrast, a small study while completing an unweighed 7-day food record showed that fiber intake at 3 months was lower than base- throughout a baseline recording period. Participants received line.22 Intake of a broader range of micronutrients during the detailed instruction on how to record their dietary intake, restrictive phase of the low FODMAP diet has not been and were advised to include detail on brand and type of all evaluated. Furthermore, the assessment of single nutrients food and fluids consumed, as well as estimated portions can fail to capture the complexity of dietehealth relation- consumed using pack size, household measures, or stan- ships. Higher diet quality and diet diversity scores—indices dardized food photographs. To improve accuracy of dietary that attempt to describe the “healthiness” of a diet23—have intake data, all food records were checked in detail for been associated with lower all-cause mortality.24,25 The completeness by the same research dietitian. impact of the low FODMAP diet on diet quality and diet di- At the first trial visit, participants were randomized in a 1:1 versity has not been investigated in IBS. The objectives of this ratio either to a control diet or to receive low FODMAP di- study were 1) to evaluate habitual nutrient intake, diet etary counseling. Counseling was provided at the first visit by quality, and diet diversity in 130 individuals with IBS; and 2) one of two experienced dietitians and written material was to evaluate the effect of a low FODMAP diet on these pa- provided. Participants randomized to the control diets were rameters in a subgroup of 63 individuals participating in a either randomized to receive counseling to follow a sham dietary intervention trial compared with individuals under- exclusion diet, an exclusion diet that was designed bespoke taking control diets. for the trial and requiring similar difficulty of dietary change to the low FODMAP diet,26 or counseled to continue their METHODS habitual diet. Participants randomized to the low FODMAP diet were counseled to restrict their dietary intake of fructans Experimental Design, Treatments, and Participants (eg, wheat, onion, garlic), galacto-oligosaccharides (eg, pul- Data from individuals with IBS referred to a tertiary center ses), lactose (eg, milk), fructose in excess of glucose (eg, in London, UK, that were recruited to two previously honey), and polyols (eg, apples, pears), and to substitute their published randomized controlled trials were included in intake of these dietary components with appropriate low this secondary analysis.26,27 Participants were recruited FODMAP foods.16 All low FODMAP and control participants between January 2010 to June 2011 and January 2013 to were contacted once weekly during the 4-week intervention November 2014. Participants were diagnosed with IBS to assess adverse events and answer any questions related to using Rome III criteria,28 were aged 18 to 65 years, and had undertaking the allocated diet. A 7-day food record was no other major gastrointestinal conditions or organ repeated during the final week of the intervention and dysfunction, recent weight loss, or other specificdietary returned at the final trial visit. Dietary compliance in low needs (eg, iron deficiency, eating disorder). Participants FODMAP and control groups was assessed by measurement with diarrhea-predominant, mixed, or unsubtyped IBS of FODMAP intake from food records.

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Participants randomized n=145

Sham diet controlled RCT n=104 Habitual diet-controlled RCT n=41

Withdrawn n=15

Habitual diet-controlled RCT n=6 n=2 antibioticsb n=2 protocol violation n=1 loss to follow up n=1 poor symptom control

Sham diet-controlled RCT n=9 n=6 antibioticsb n=1 protocol violation n=1 loss to follow up n=1 personal reasons

Participants completed n=130a

Sham diet controlled RCT n=95 Habitual diet-controlled RCT n=35

Randomized to low FODMAPc advice n=63d Randomized to control diet advice n=67d

Sham diet-controlled RCT n=47 Sham diet-controlled RCT n=48 Habitual diet-controlled RCT n=16 Habitual diet-controlled RCT n=19

Figure. Flow diagram of participants with irritable bowel syndrome recruited to two 4-week randomized controlled trials (RCTs) comparing low FODMAP diet with control arms (sham diet, habitual diet). aNutrient intake, FODMAP intake, diet quality, and diet diversity are reported at baseline in 130 individuals. bCommencement of antibiotic therapy considered an exclusion as the impact of dietary intervention on the microbiome was an end point in both RCTs. cFODMAP¼fermentable oligosaccharides, disaccharides, monosaccharides, and polyols. dNutrient intake, FODMAP intake, diet quality, and diet diversity are compared between low FODMAP and control diet groups.

Both randomized controlled trials were approved by and where recommendations were available. FODMAP intake was conducted in accordance with local Research Ethics Com- evaluated using dietary software34 populated with compre- mittees (Guy’s Hospital [09/H0804/89] and Fulham Research hensive FODMAP composition data.35-37 Ethics Committee [12/LO/1402]). Diet quality, a measure of how closely the diet aligns with dietary guidelines, and diet diversity, relating to nutrient Nutrient and FODMAP Intake, Diet Quality, and Diet adequacy and dietary variety, were calculated. There is a lack Diversity Analysis of consensus regarding the gold standard for measuring diet All dietary analyses were performed by a dietitian. Daily quality and diet diversity and therefore two indices were intake of energy, macronutrients, and 19 micronutrients was calculated to allow a more comprehensive characterization calculated from diet record data using dietary software and comparison to other literature. The Healthy Diet Indica- comprising UK food and drink composition data from tor and Healthy Diet Score were calculated to measure diet McCance and Widdowson’s Nutrient databank.29 Energy and quality (Table 1). The Healthy Diet Indicator measures diet nutrient intake from food and ﬂuid excluding vitamin and quality relating to dietary intake of nine food groups or nu- mineral supplements were evaluated. Where information in a trients based on World Health Organization dietary guide- diet record was ambiguous, an average was estimated using lines for the prevention of chronic disease, with a maximum standardized values.30 Where a novel food was consumed score of nine for best diet quality.38 The Healthy Diet Score is that was absent from the database (eg, wheat-free bread), a modeled on the Healthy Diet Indicator, but modiﬁed to new food was created using available composition data from comply with recommendations by the UK Committee on food packaging. Nutrient intakes were compared with Di- Medical Aspects of Food Policy, measures diet quality based etary Reference Values (DRV) for the United Kingdom, the on the intake of 12 foods and nutrients.39 national recommendations for nutrient intake,31-33 and the The Diet Quality Index-Revised Dietary Diversity Score40 proportion of individuals meeting these was calculated and Dietary Diversity Score were used to measure diet

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Table 1. Scores used to assess diet quality in two 4-week Table 2. Scores used to assess diet diversity in two 4-week randomized controlled trials comparing low FODMAPa diet randomized controlled trials comparing low FODMAPa diet with control arms (sham diet, habitual diet) with control arms (sham diet, habitual diet)

Healthy Diet Healthy Component Componentsb Indicatorc Diet Scored Component Foods criteria, g/db

% energy! Diet Quality Index-Revised Dietary Diversity Scorec! Saturated fat 0-10 0-10 Grains Nonewhole-grain breads 18 Polyunsaturated fat 3-7 6-10 Quick breads 18 Protein 10-15 10-15 Whole-grain breads 18 Total carbohydrate NAe 50-70 Nonewhole-grain cereals 63 Complex carbohydrate 50-70 NA Rice 63 g/d! Whole-grain cereals 63 Dietary ﬁber 27-40 18-32 Pasta 63 % energy! Vegetables Dark green and leafy 113 Nonmilk extrinsic sugars NA 0-10 Potatoes 63 Mono- and disaccharides 0-10 NA Tomato products 63 mg/d! Starchy 63 Cholesterol 0-300 0-245 Dry peas and beans 63 Calcium NA 700 Deep yellow and orange 63 g/d! Other 63 Fish NA 32 Fruit Fruit and fruit juices 83 Red meat and meat products NA 90 Citrus fruits, melon, and 63 Fruit and vegetables >400 400 berries Pulses, nuts, and seeds >30 30 Meat/dairy Beef, pork, organ meats, 35 luncheon meats aFODMAP¼fermentable oligosaccharides, disaccharides, monosaccharides, and polyols. bEach component carries a score of 1. Poultry 35 cMaximum score for Healthy Diet Indicator¼9. Fish 35 dMaximum score for Healthy Diet Score¼12. eNA¼not applicable. Milk 113 Cheese 21 Eggs 25 diversity41 (Table 2). The Diet Quality Index-Revised Dietary Diversity Score and Dietary Diversity Score are based on US Yogurt 113 dietary guidelines and mortality risk from a large US cohort Dietary Diversity Scored! study, respectively. For all indices, a higher score repre- Dairy All milk, milk products >30 sented greatest quality or diversity. Each component of the > diet quality and diversity indices was calculated using food Meat All and includes non-meat 30 and nutrient intake data from the 7-day food records. Daily protein sources nutrient intake was converted into proportion of energy Grain All except cakes, cookies, >30 where required. Healthy Diet Indicator required data on mufﬁns, pastry complex carbohydrate intake, which was calculated by Fruit Canned, fresh, dried, and >30 subtracting total daily sugar intake from total daily carbohydrate intake. Healthy Diet Score required data on nonmilk juice, except fruit drinks extrinsic sugar intake, which was calculated by subtracting Vegetables All >30 total lactose intake from total sugar intake. For the diversity aFODMAP¼fermentable oligosaccharides, disaccharides, monosaccharides, and polyols. scores and for some components of the diet quality scores, b 1 42 foods were manually coded into food groups (eg, fruit and All servings are /2 standard serve as per the US Food Guide Pyramid ; imperial converted to metric units where required and adjusted for density (1 oz¼28.35 g; 1 vegetables) to calculate daily intake (g/day). Data are pre- cup¼250 mL). sented as the mean diet quality and diet diversity scores for cEach component carries a score of 1. Each food group carries a maximum weighted the 7 days of dietary data collected. The proportion of par- score of 2.5, maximum score¼10. ticipants achieving a cutoff score equal to the baseline dEach component carries a score of 1, maximum score¼5.

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Table 3. Baseline demographic data for patients with irritable bowel syndrome recruited to two 4-week randomized controlled trials comparing low FODMAPa diet with control arms (sham diet, habitual diet)

Variable Low FODMAP diet (n[63) Sham diet (n[48) Habitual diet (n[19)

meanstandard deviation! Age, y 3712 3412 359 n (%)! Female 44 (70) 30 (63) 12 (63) meanstandard deviation! Weight kg 6913 7419 7415 Body mass indexb 244255264 n (%)! Symptom duration <5y 42 (67) 37 (77) 15 (79) IBS-Dc subtype 41 (65) 31 (65) 8 (42) Current medications Antidiarrheal 4 (6) 2 (4) 4 (21) Laxative 1 (2) 1 (2) 1 (5) Bulking agent 2 (3) 0 (0) 0 (0) Analgesic 5 (8) 0 (0) 2 (11) Antispasmodic 7 (11) 5 (10) 1 (5) Antidepressant 3 (5) 1 (2) 1 (5) Reﬂux medication 3 (5) 2 (4) 3 (16) Smoker 7 (11) 3 (6) 4 (21) Vegetarian 1 (2) 1 (2) 2 (11)

aFODMAP¼fermentable oligosaccharides, disaccharides, monosaccharides, and polyols. bCalculated as kg/m2. cIBS-D¼diarrhea-predominant irritable bowel syndrome. median score was calculated for all diet quality and diet Habitual Dietary Intake in IBS diversity indices. The energy and nutrient intake of the 130 individuals with IBS consuming habitual (usual) diet at baseline is presented Statistical Analysis in Table 4. Mean intakes for the sample exceeded the DRV for Demographic data and habitual dietary data (n¼130) are pre- most vitamins and minerals, including for folate and calcium. sented as mean (standard deviation) or number (percent) for Conversely, mean intake of sodium exceeded the DRV of categorical data (objective 1). Continuous data at the 4-week 1,600 mg/day, and mean intakes for the sample did not reach time point were compared between groups using analysis of the DRV for fiber selenium or iodine. covariance with baseline measures as a covariate, and the data The proportion of participants meeting age and sex-specific are presented as estimated marginal means and 95% CI energy and nutrient DRVs is also presented in Table 4.A (objective 2). Data were tested for equality of variances using majority of participants consuming their baseline habitual Levene’s test and, where necessary, data were transformed. diet failed to meet the recommended intake for several nu- Planned comparisons to evaluate differences between low trients. Recommended intakes were only achieved in 6 (5%) FODMAP diet and each control diet were conducted using for fiber. While most participants achieved targets for vita- simple planned contrasts. A c2 test was used to compare cate- mins, only 39 (30%) met the recommendation for iodine, 51 gorical data and data are presented as number (percent). (39%) for magnesium, 63 (48%) for iron, and 20 (15%) for Differences were considered significant where P<0.05. selenium. A number of nutrients were consumed in excess of Statistical analysis was performed using IBM SPSS Statistics recommended intakes. Only 47 (24%) participants reported for Windows, version 22.0.43 fat intake that did not exceed the guidelines, and 12 (9%) and 2 (2%) did not exceed the recommendation for sodium and RESULTS total sugars, respectively. Diet records for 130 participants were included in the anal- Diet quality and diversity scores are presented in Table 5. ysis of habitual diet in individuals with IBS. Most participants Scores for diet quality of baseline habitual diet were low were female with a diarrhea-predominant IBS subtype and compared with maximum possible score for both the most did not take IBS medications (Table 3). Healthy Diet Indicator (mean¼2.5; 95% CI 2.3 to 2.7 vs

April 2020 Volume 120 Number 4 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 539 RESEARCH 540 Table 4. Energy and nutrient intake of patients with irritable bowel syndrome during habitual diet (n¼130) and after 4 weeks of a low FODMAPa or control arms (sham diet, habitual diet) of a dietary intervention trial and proportion meeting national guidelines ORA FTEAAEYO URTO N DIETETICS AND NUTRITION OF ACADEMY THE OF JOURNAL

Proportion Meeting Dietary Nutrient Intake Reference Value After Completing Dietary Intervention Trial After Completing Dietary (n[130) Intervention Trial (n[130) Habitual diet Habitual Low at baseline Population Dietary diet at FODMAP Sham Habitual Dietary (n[130), Low FODMAP Sham diet Habitual diet ANCOVA, intake, Reference baseline diet diet diet P component mean (95% CI) diet (n[63) (n[48) (n[19) P valueb medianc Valued (n[130) (n[63) (n[48) (n[19) valuee

estimated marginal means (95% CI)! n (%)! Energyf 1,967 1,869 1,853 1,876 0.960 2,784 —————— (kcal/d) (1,877-2,056) (1,784-1,954) (1,756-1,950) (1,721-2,030) Protein 77 77 74 73 0.432 74 —————— (g/d) (73-81) (73-81) (69-78) (67-80) Fat 81 78 78 72 0.581 67 35% 47 18 17 13 0.007* (g/d) (77-85) (73-83) (72-83) (64-82) energy (24) (29) (35) (68) Carbohydrate, 222 201 202 226 0.057 216 50% 36 14 6 11 <0.001* total (g/d) (212-223) (190-211) (191-214) (207-205) energy (28) (22) (13) (58) Starch 124 109 112 128 0.046* —— ————— (g/d) (117-130) (103-117) (104-120) (115-141) Total sugars, 88 77 84 89 0.093 47 5% energy 2 0 2 1 0.228 total (g/d)g (82-95) (71-83) (76-91) (78-99) (2) (0) (4) (5) Fiber 18 17 17 19 0.343 18 30 6 2 2 1 0.908 (g/d) (17-19) (16-19) (15-18) (16-21) (5) (3) (4) (5) Sodium 2,749 2,517 2,491 2,467 0.961 — 1,600 12 11 10 2 0.607 (mg/d) (2,603-2,895) (2,332-2,702) (2,279-2,703) (2,130-2,703) (9) (17) (21) (11) Potassium 2,902 2,951 2,791 2,812 0.296 2,784 3,500 12 11 7 3 0.919 pi 00Vlm 2 ubr4 Number 120 Volume 2020 April (mg/d) (2,749-2,895) (2,811-3,091) (2,630-2,951) (2,558-3,066) (18) (17) (15) (16) Calcium 814 739 784 719 0.403 766 700 80 26 29 12 0.074 (mg/d) (762-866) (686-792) (724-845) (622-815) (62) (41) (60) (63) Magnesiumf 278 272 254 260 0.109 255 270-300 51 24 22 7 0.664 (mg/d) (262-296) (258-286) (238-270) (235-285) (39) (38) (46) (37) Phosphorous 1,252 1,204 1,170 1,140 0.228 — 550 130 63 47 19 0.423 (mg/d) (1,189-1,315) (1,146-1,262) (1,104-1,237) (1,035-1,245) (100) (100) (98) (100)

(continued on next page) pi 00Vlm 2 ubr4 Number 120 Volume 2020 April Table 4. Energy and nutrient intake of patients with irritable bowel syndrome during habitual diet (n¼130) and after 4 weeks of a low FODMAPa or control arms (sham diet, habitual diet) of a dietary intervention trial and proportion meeting national guidelines (continued)

estimated marginal means (95% CI)! n (%)! Iron 11.5 10.0 11.2 10.5 0.057 10 8.7-14.8 63 23 23 8 0.481 (mg/d) (10.9-12.1) (9.4-10.7) (10.5-12.0) (9.4-11.7) (48) (37) (48) (42) Copper 1.3 1.2 1.2 1.1 0.906 — 1.2 62 23 23 6 0.344 (mg/d) (1.2-1.4) (1.0-1.3) (1.0-1.3) (0.9-1.3) (48) (37) (48) (32) Zinc 8.5 8.2 7.8 7.9 0.670 8.3 7.0-9.5 72 29 23 9 0.980 (mg/d) (8.0-9.0) (7.6-8.8) (7.1-8.5) (6.9-9.0) (55) (46) (48) (47) Chloride 3,965 3,509 3,535 3,601 0.944 — 2,500 113 48 35 15 0.857 (mg/d) (3,748-4,182) (3,251-3,768) (3,238-3,831) (3,131-4,072) (87) (76) (73) (79) ORA FTEAAEYO URTO N DIETETICS AND NUTRITION OF ACADEMY THE OF JOURNAL Seleniumf 45 52 42 47 0.026* 46 60-75 20 12 3 2 0.132 (mg/d) (42-49) (48-56) (37-47) (39-54) (15) (19) (6) (11) Iodine 117 129 112 111 0.264 142 140 39 24 15 7 0.749 (mg/d) (107-126) (114-144) (95-129) (84-138) (30) (38) (31) (37) Vitamin Af 1,037 1,144 1,041 825 0.302 625 600-700 94 43 36 12 0.581 (mg/d) (897-1,177) (985-1,303) (860-1,223) (537-1,114) (72) (68) (75) (63) Thiaminf 1.5 1.3 1.4 1.6 0.505 — 0.7-1.0 122 45 39 17 0.192 (mg/d) (1.3-1.6) (1.2-1.5) (1.2-1.6) (1.3-1.9) (94) (71) (81) (90) Riboﬂavin 1.5 1.4 1.5 1.4 0.267 1.5 1.1-1.3 94 40 34 11 0.549 (mg/d) (1.4-1.6) (1.3-1.5) (1.4-1.6) (1.2-1.5) (72) (64) (71) (58) Niacin 20 21 20 20 0.357 — 12-17 10 53 35 15 0.353 (mg/d) (19-21) (20-22) (18-21) (19-23) (83) (84) (73) (79) RESEARCH (continued on next page) 541 RESEARCH 542 Table 4. Energy and nutrient intake of patients with irritable bowel syndrome during habitual diet (n¼130) and after 4 weeks of a low FODMAPa or control arms (sham diet, habitual diet) of a dietary intervention trial and proportion meeting national guidelines (continued) ORA FTEAAEYO URTO N DIETETICS AND NUTRITION OF ACADEMY THE OF JOURNAL

estimated marginal means (95% CI)! n (%)! Vitamin B-6 1.9 2.0 1.9 2.0 0.176 — 1.2-1.4 110 61 43 17 0.264 (mg/d) (1.8-2.0) (1.9-2.1) (1.7-2.0) (1.8-2.2) (85) (97) (90) (90) Vitamin B-12 5.1 6.1 4.7 3.9 <0.001* — 1.5 126 63 47 18 0.244 (mg/d) (4.6-5.7) (5.5-6.6) (4.1-5.3) (2.9-3.9) (97) (100) (98) (95) Folate 231 227 237 214 0.375 233 200 78 35 31 9 0.390 (mg/d) (216-247) (211-242) (219-255) (186-243) (60) (56) (65) (47) Vitamin C 97 105 95 97 0.503 — 40 119 57 43 16 0.739 (mg/d) (87-107) (94-117) (82-108) (76-119) (91) (91) (90) (84)

aFODMAP¼fermentable oligosaccharides, disaccharides, monosaccharides, and polyols. bANCOVA¼analysis of covariance with planned comparisons using simple planned contrasts; starch low FODMAP diet vs habitual diet P¼0.030; selenium low FODMAP diet vs sham diet P¼0.022; vitamin B-12 low FODMAP diet vs sham diet p¼0.001 and low FODMAP diet vs habitual diet P<0.001. cPopulation intake median for adults aged 19 to 64 years.44 Dietaryd reference value not reported for energy as physical activity was not measured. Dietary reference value reported for macronutrients and their subcomponents (eg, sugar); reference nutrient intake is reported for micronutrients. Some vary depending on sex and/or age.31-33 c2etest. fTransformation required for ANCOVA. gPopulation median and dietary reference value is for free sugars but data presented are calculated based on nonmilk extrinsic sugars, as this was able to be accurately extracted. *P<0.05. pi 00Vlm 2 ubr4 Number 120 Volume 2020 April pi 00Vlm 2 ubr4 Number 120 Volume 2020 April Table 5. Diet quality and diet diversity scores of patients with irritable bowel syndrome during habitual diet (n¼130) and after 4 weeks of a low FODMAPa or control arms (sham diet, habitual diet) of a dietary intervention trial and proportion achieving cutoff values

Diet Quality and Diversity Scores Achieving Cutoff Valueb After Completing Dietary Intervention Trial After Completing Dietary Intervention Habitual diet at (n[130) Habitual Trial (n[130) Maximum baseline Low diet at Low Sham Habitual possible (n[130), mean FODMAP Sham diet Habitual ANCOVA Cutoff baseline FODMAP diet diet Index score (95% CI) diet (n[63) (n[48) diet (n[19) P valuec scorea (n[130) diet (n[63) (n[48) (n[19) P valued

Diet quality estimated marginal means (95% CI)! n(%)! Healthy Diet 9 2.5 (2.3-2.7) 2.2 (1.8-2.5) 2.4 (2.1-2.8) 3.0 (2.5-3.6) 0.031* 2 104 (80) 40 (64) 34 (71) 16 (84) 0.219 Indicator Healthy Diet Score 12 4.9 (4.6-5.3) 4.3 (4.0-4.8) 5.0 (4.5-5.4) 5.7 (4.9-6.5) 0.008* 5 73 (56) 25 (40) 29 (60) 16 (84) 0.002* Diet Diversity Diet Quality Index- 10 4.6 (4.3-4.8) 4.1 (3.9-4.4) 4.1 (3.8-4.5) 4.0 (3.5-4.8) 0.948 4.5 68 (52) 32 (51) 21 (44) 12 (63) 0.353 Revised Dietary Diversity Score Dietary Diversity 5 4.7 (4.6-4.8) 4.6 (4.5-4.7) 4.8 (4.6-4.9) 4.5 (4.2-4.7) 0.078 5 94 (72) 41 (65) 38 (79) 10 (53) 0.079 Score ORA FTEAAEYO URTO N DIETETICS AND NUTRITION OF ACADEMY THE OF JOURNAL aFODMAP¼ fermentable oligosaccharides, disaccharides, monosaccharides, and polyols. bMedian score at baseline. cAnalysis of covariance with planned comparisons using simple planned contrasts; Healthy Diet Indicator Low FODMAP diet vs habitual diet P¼0.018; Healthy Diet Score Low FODMAP diet vs habitual diet P¼0.006. dc2 test. *P<0.05. RESEARCH 543 RESEARCH

Table 6. FODMAPa intake of patients with irritable bowel syndrome during habitual diet (n¼130) and after 4 weeks of low FODMAP or control arms (sham diet, habitual diet) of a dietary intervention trial

After Completing Dietary Intervention Trial (n[130) Planned Contrasts Low Low Habitual diet at Low FODMAP FODMAP diet baseline (n[130), FODMAP Sham diet Habitual ANCOVA,b diet vs vs habitual FODMAP mean (95% CI) diet (n[63) (n[48) diet (n[19) P value sham diet diet

estimated marginal mean (95% CI) ! Total FODMAP 17.0 8.6 17.5 16.0 <0.001 <0.001 <0.001 intake (g/d) (5.4-18.5) (6.9-10.4) (15.6-19.5) (12.8-19.1) Fructans 4.0 2.1 4.8 4.2 <0.001 <0.001 <0.001 (g/d)c (3.3-4.8) (1.5-2.6) (4.1-5.5) (3.2-5.2) Galacto- 1.0 0.8 0.9 1.7 0.004 0.095 0.001 oligosaccharides (0.9-1.2) (0.7-1.0) (0.7-1.2) (1.4-2.0) (g/d)c Lactose 8.8 4.2 8.8 7.5 <0.001 <0.001 0.030 (g/d) (7.5-10.1) (2.8-5.6) (7.1-10.4) (4.9-10.1) Excess fructose 1.6 12.6 16.4 19.5 0.009 0.011 0.015 (g/d)c (1.3-1.9) (10.7-14.6) (14.2-18.7) (15.8-23.2) Sorbitol 0.8 0.2 1.0 0.5 <0.001 <0.001 <0.001 (g/d)c (0.6-0.9) (0.1-0.4) (0.8-1.2) (0.2-0.8) Mannitol 0.4 0.1 0.3 0.3 0.007 0.011 0.100 (g/d)c (0.3-0.4) (0.1-0.2) (0.2-0.4) (0.2-0.4)

maximum 9) and the Healthy Diet Score (mean¼4.9; 95% CI for baseline differences (P¼0.435). Total starch intake was 4.6 to 5.3 vs maximum 12). Scores for diet diversity in in- lower after the low FODMAP diet (mean¼109 g/day; 95% CI dividuals following baseline habitual diet were also low 103 to 117 g/day) compared with habitual control diet compared with the maximum possible score for the Diet (mean¼128 g/day; 95% CI 115 to 141 g/day; P¼0.030). Total Quality Index-Revised Dietary Diversity Score (mean¼4.6; carbohydrate, fat, and protein intake remained unchanged, 95% CI 4.3 to 4.8 vs maximum 10), whereas the Dietary Di- although fewer individuals after the low FODMAP diet did not versity Score score achieved was close to the maximum exceed the guidelines for fat (n¼18 [29%]) compared with possible score (ie, 5). sham diet (n¼17 [35%]) and habitual control diets (n¼13 [68%]; P¼0.007), and fewer were able to meet the guidelines for carbohydrate (n¼14 [22%] vs n¼6[13%]vsn¼11 [58%]; The Effect of a Low FODMAP Diet on Dietary Intake P<0.001). Intake of micronutrients was not different between in IBS groups, except for the intake of selenium and vitamin B-12, Data are presented for 63 participants who were randomized which were both higher after the low FODMAP diet compared to low FODMAP diet, 48 participants randomized to sham diet, with the sham control diet (P<0.01), and vitamin B-12 was and 19 participants randomized to habitual diet (Figure). En- also higher compared with habitual control diet (P<0.001). ergy and nutrient intakes at baseline habitual diet and after The low FODMAP diet led to lower diet quality scores low FODMAP diet, sham control, or habitual control diet are compared with habitual control diet, but not the sham con- presented in Table 4 and FODMAP intake presented in Table 6. trol diet, according to both the Healthy Diet Indicator There was a lower FODMAP intake in the low FODMAP group (mean¼2.2; 95% CI 1.8 to 2.5 vs mean¼3.0; 95% CI 2.5 to 3.6; (8.6 g/day) compared with both sham diet (17.5 g/day) and P¼0.018) and the Healthy Diet Score (mean¼4.3; 95% CI 4.0 to habitual control diets 16.0 g/day; P<0.001), conﬁrming that, in 4.8 vs mean¼5.7; 955% CI 4.9 to 6.5; P¼0.006), and fewer general, participants complied with the dietary intervention. individuals met the median cutoff score for the Healthy Diet There was no difference in energy intake between low FOD- Score compared with the control diets (P¼0.002). There was MAP diet and sham or habitual control diets, nor were there no difference in diet diversity according to the Diet Quality any differences in body weight between groups after adjusting Index-Revised Dietary Diversity Score (P¼0.948) or the

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Dietary Diversity Score (P¼0.078; Table 5), or for the pro- guidelines when following a short-term low FODMAP diet is portion of individuals meeting the cutoff score. reduced. The clinical importance of a 1- to 1.5-point difference in these scores is unclear, especially in the context of a background low-quality habitual diet in the entire IBS cohort. DISCUSSION Long-term assessment of diet quality in individuals using this This is the most comprehensive evaluation of the habitual diet for extended periods is required. energy and nutrient intake of individuals with IBS, including While this is the most comprehensive evaluation of the an assessment of diet quality and diet diversity. Many in- nutrient intake of individuals with IBS and the largest and dividuals reported dietary intakes that did not meet recom- most robust assessment of the effect of the low FODMAP diet mendation for various nutrients; however, overall nutrient on nutrient intake, it is recognized there are a number of intake was comparable to the general population. For limitations. Attempts were made to utilize the most example, mean fiber intake was 18 g/day, which is the same commonly used and best validated tools to assess diet quality as that found in a national survey of the UK general popu- and diversity that have been widely associated with health lation,44 which contrasts with findings reporting lower fiber outcomes.38,41,45 Although the Healthy Diet Score is based on intake in IBS vs controls.9 UK dietary guidelines, it has not been validated against health In line with the nutrient intake findings, habitual diet quality outcomes in cohort studies. The other dietary indices used was relatively poor. This supports recent evidence suggesting were not based on UK dietary guidelines. that diet quality is lower in IBS than healthy controls using a It is also acknowledged that participants were from a tertiary Dutch diet quality score.9 The mean score for the Healthy Diet setting and had noneconstipation-predominant symptoms. Indicator was low in this cohort compared with cutoffs used in a Therefore, the findings may not be generalizable to all patients large cohort of 3,045 men in which Healthy Diet Indicator score with IBS. Volunteer bias could have led to over- and/or un- was inversely correlated with all-cause mortality.38 The results derestimation of true dietary intake. It is known that motiva- for diet diversity here were equivocal. Of all participants, 72% tion and behaviors in research volunteers may be different achieved the cutoff (in this case the maximum) score for the from those who do not volunteer, with potential consequences Dietary Diversity Score, which is much higher than that re- for external validity.48 Reassuringly, the demographic charac- ported in a healthy population from a large cohort study of more teristics of this patient population are representative of other than 10,000 (35%) individuals.45 However, when diet diversity large IBS cohort studies. Nutrient intake findings are based on was measured using the Diet Quality Index-Revised Dietary food and fluid intake excluding supplements, which provides Diversity Score, a poorer diversity was found, with only 52% the most conservative estimate of nutrient intake, and may achieving the cutoff score. This discrepancy may be due to the marginally underestimate true intakes in a population where a Diet Quality Index-Revised Dietary Diversity Score requiring small proportion use vitamin and/or mineral supplements. intake of a greater number of individual foods to contribute to While statistical adjustment for multiple comparisons were component scores. considered and would have provided an even more conser- After implementation of the low FODMAP diet, there were vative assessment, it may have masked clinically relevant no significant differences in the intake of energy or macro- findings. The findings are also limited by the small numbers in nutrients compared with the control diets, but there was a the habitual control group. Finally, although significant effort lower intake of starch compared with the habitual control was made to ensure the nutrient database was complete, diet. Previous studies have reported lower carbohy- especially for specialized food products (eg, wheat-free), this drate27,46,47 and energy intake46,47 in individuals following a was sometimes limited to information available on food low FODMAP diet compared with pre-intervention habitual packaging, which may have underestimated nutrient intake. diet. However, according to the current findings, energy and macronutrient intakes after a low FODMAP diet were not different from either sham control or habitual control diet. CONCLUSIONS The nutritional short- or long-term significance of a lower This study demonstrates that many individuals with IBS fail starch intake of 20 g/day found here is debatable, particularly to meet the DRV for a number of nutrients and overall diet as overall mean intake remained relatively high. quality is low. Furthermore, a 4-week low FODMAP diet, There were indications that the low FODMAP diet might, in when delivered by a specialist dietitian, does not significantly fact, improve overall dietary intake. For example, intake of impact overall nutrient intake or measures of diet diversity, vitamin B-12 was higher than the habitual control diet, which but leads to a lower diet quality compared with control diets. could represent a greater intake of eggs or fish.Furthermore,diet Overall diet quality should be assessed and considered diversity was not affected by the dietary restriction. Previous throughout the dietetic consultation process, with specific findings suggest a low FODMAP diet leads to a lower intake of emphasis on inclusion of suitable fruit, vegetables, whole- calcium compared with habitual diet,27 but these data failed to grain, and milk products. Finally, it is acknowledged that support these findings, and although a smaller proportion of these findings are likely to be representative of a “best case participants achieved the calcium DRV compared with habitual scenario,” in which patients are provided expert counseling control diet, this did not reach statistical significance. from a specialist dietitian. The nutritional impact of the low An important finding here is that a low FODMAP diet led to FODMAP diet in individuals that do not seek specialist lower diet quality scores at 4 weeks compared with a counseling requires investigation. habitual control diet when measured by the Healthy Diet Indicator and the Healthy Diet Score index. This suggests that, References even when counseling is provided by a specialist dietitian, 1. Lacy BE, Mearin F, Chang L, et al. Bowel disorders. Gastroenterology. the overall ability for individuals to meet the dietary 2016;150(6):1393-1407.

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2. Lovell RM, Ford AC. Global prevalence of and risk factors for irritable Dietary Patterns Methods Project. Am J Clin Nutr. 2015;101(3): bowel syndrome: A meta-analysis. Clin Gastroenterol Hepatol. 587-597. 2012;10(7):712-721 e4. 25. Sotos-Prieto M, Bhupathiraju SN, Mattei J, et al. Association of 3. Gralnek IM, Hays RD, Kilbourne A, Naliboff B, Mayer EA. The impact changes in diet quality with total and cause-specific mortality. N Engl of irritable bowel syndrome on health-related quality of life. J Med. 2017;377(2):143-153. Gastroenterology. 2000;119(3):654-660. 26. Staudacher HM, Lomer MCE, Farquharson FM, et al. Diet low in 4. Monsbakken KW, Vandvik PO, et al. Perceived food intolerance in FODMAPs reduces symptoms in patients with irritable bowel syn- subjects with irritable bowel syndrome—etiology, prevalence and drome and probiotic restores Bifidobacterium species: A randomized consequences. Eur J Clin Nutr. 2006;60(5):667-672. controlled trial. 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AUTHOR INFORMATION H. M. Staudacher is an Alfred Deakin Postdoctoral Research Fellow, Food and Mood Centre, IMPACT Strategic Research Centre, School of Medicine, Deakin University, Melbourne, Australia; at the time of the study, she was a clinical doctoral research fellow, Department of Nutritional Sciences, King’s College London, London, UK. F. S. E. Ralph is a dietitian, Department of Nutrition and Dietetics, Berkshire Healthcare NHS Foundation Trust, Reading, London, UK; at the time of the study, she was a dietetics student, Department of Nutritional Sciences, King’s College London, London, UK. P. M. Irving is a lecturer, Department of Nutritional Sciences, King’s College London, and a consultant gastroenterologist, Department of Gastroenterology, Guys and St Thomas’ NHS Foundation Trust, London, UK. K. Whelan is a professor of dietetics, Department of Nutritional Sciences, King’s College London, London, UK. M. C. E. Lomer is a reader in dietetics, Department of Nutritional Sciences, King’s College London, and a senior consultant dietitian, Departments of Gastroenterology and Nutrition and Dietetics, Guys and St Thomas’ NHS Foundation Trust, London, UK. Address correspondence to: Miranda C. E. Lomer, PhD, RD, Department of Nutritional Sciences, King’s College London, 150 Stamford St, 4.104 Franklin-Wilkins Building, London SE1 9NH, UK. E-mail: [email protected] STATEMENT OF POTENTIAL CONFLICT OF INTEREST M. C. E. Lomer and K. Whelan are co-inventors of a mobile application relating to the low FODMAP diet. No potential conflict of interest was reported by the remaining authors. FUNDING/SUPPORT This study/project is funded by the National Institute for Health Research (NIHR) [CDRF-2012-03-060]. The views expressed are those of the author(s) and not necessarily those of the NIHR or the Department of Health and Social Care. ACKNOWLEDGEMENTS The authors thank professor Peter Gibson, MD, FRACP, and Jane Muir, PhD (Monash University, Melbourne, Australia) for providing analysis of total and individual FODMAP intake data. AUTHOR CONTRIBUTIONS All authors conceived the study and developed the research plan; H. M. Staudacher and F. S. E. Ralph conducted the data collection; H. M. Staudacher, F. S. E. Ralph, M. C. E. Lomer, and K. Whelan developed the analysis plan; F. S. E. Ralph and H. M. Staudacher analyzed the data; H. M. Staudacher and F. S. E. Ralph wrote the paper; M. C. E. Lomer, K. Whelan, and P. M. Irving had primary responsibility for final content. All authors provided critical comment on the intellectual content of the manuscript and approved the final version for submission.

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