Re-challenging FODMAPs: the low FODMAP diet phase two

bs_bs_banner doi:10.1111/jgh.13687 REVIEW ARTICLE Re-challenging FODMAPs: the low FODMAP diet phase two Caroline Tuck and Jacqueline Barrett * Department of Gastroenterology, Monash University, Melbourne, Victoria, Australia Key words diet therapy, FODMAPs, functional bowel disorders, irritable bowel syndrome. Accepted for publication 14 November 2016. Correspondence Caroline Tuck, Department of Gastroenterology Central Clinical School, Monash University, Level 6, The Alfred Centre 99 Commercial Road, Prahran, Melbourne, Vic 3004, Australia. Email: caroline.tuck@monash.edu Disclosures: C Tuck was supported by an Australian Postgraduate Award Scholarship. The authors have no conflicts of interest to declare. Abstract The low fermentable, oligosaccharides, disaccharides, monosaccharides, and polyols (FODMAP) diet has good evidence for use in the treatment of patients with irritable bowel syndrome. Importantly, patients are encouraged not to remain on a strict low FODMAP diet long-term, and many patients maintain symptom improvement with a relaxed, moderate FODMAP restriction. The re-challenge phase is crucial to assist patients in identifying specific dietary triggers, reduce the level of dietary restriction required, and increase prebiotic intake. Limited evidence is available to guide best practice, but, in practice, beneficial outcomes can be seen through strategic food reintroductions. Here, we set out some practical recommendations based on clinical experience. Dietitians should tailor the challenge process to the individual patient and their needs. Food challenges should aim to improve dietary variety and nutritional adequacy while considering specific food preferences and usual dietary habits. Identifying FODMAP subgroups that are well tolerated is helpful, allowing the reintroduction of some moderate to high FODMAP foods back into the diet without symptom induction. FODMAP subtypes that are less well tolerated may also be reintroduced, but dosage and frequency of consumption need to be individualized. Additional challenges that face dietitians include consideration of patients with multiple dietary restrictions such as in vegetarians or patients with diabetes who are simultaneously following a low FODMAP diet. Ensuring nutritional adequacy is essential. The outcome of the re-challenge process aims to find a balance between good symptom control and expansion of the diet. Introduction Symptoms of functional bowel disorders (FBD) including irritable bowel syndrome (IBS) can be treated with a diet low in fermentable carbohydrates, named FODMAPs (fermentable, oligosaccharides, disaccharides, monosaccharides, and polyols). The low FODMAP diet is now included as first-line therapy and has been shown to provide symptom improvement in approximately 68 76% of individuals. 1 Symptom improvement generally occurs following 3 4 weeks on the restrictive phase of the diet, 2 although the length of time required and degree of symptom improvement can vary between patients. Following the restrictive phase, patients are encouraged to reintroduce high FODMAP foods to assess their tolerance to the individual FODMAP subgroups. The aim of this re-challenge phase is to find a balance between good symptom control and expansion of the diet. Patients requiring the diet long-term then follow a modified FODMAP diet based on their dietary tolerance found while challenging. 2 Although this rechallenge phase is conducted worldwide, and anecdotally has success in relaxing the approach and maintaining symptomatic improvement, limited data exist to define the re-challenge process. What is clear is that working with a dietitian experienced in the area is crucial for the success of the diet and the re-challenge process. Reasons for re-challenging foods with higher FODMAP content. There are a number of reasons for the importance of the re-challenge process. High FODMAP foods, specifically those containing fructans and galacto-oligosaccharides (GOS), are known to be prebiotic, and 3 4 weeks of a low FODMAP diet has been shown to lead to marked alterations in the colonic microbiota. 3,4 However, the clinical significance of these changes is not known. 2 Reintroduction of some prebiotic high FODMAP foods, even if in small quantity, may attenuate potential long-term impact of dietary alteration on the microbiota. However, this has not been investigated. Although the low FODMAP diet does not restrict entire food groups, reintroduction of high FODMAP foods will assist in improving food variety and nutritional adequacy. There is risk of nutritional inadequacy with implementation of any exclusion diet or dietary restriction. 5 Indeed, recent data demonstrate that more than half of patients following a low FODMAP diet did not meet their recommended intakes of calcium and iron, although values were not dissimilar to the healthy population on a habitual diet. Interestingly, this study did not see any change in the proportion of those meeting fiber recommendations from baseline to follow-up. 6 Further 11

Re-challenging FODMAPs C Tuck and J Barrett data including comprehensive analysis of micronutrient intake are needed to fully understand what effect the low FODMAP diet and re-challenge phase has on nutritional adequacy. Patients often report difficulty with complying with the low FODMAP diet when eating away from the home through, for example, fear of inadvertently consuming high FODMAP foods, possibly affecting social inclusion and quality of life (QOL). Expansion of the diet through re-challenge would increase flexibility of food choices and thereby hope to reduce any potential negative effects on QOL. One study assessing IBS-specific QOL found 19 patients with diarrheapredominant IBS had improved QOL during a 6-week trial of the low FODMAP diet. However, this study showed no improvement of QOL in those with constipation predominant or alternating IBS subtypes. 7 The improved QOL in the diarrhea-predominant patients may have been related to enhanced symptom control. It is encouraging that the dietary restrictions themselves did not result in a reduction in QOL in any of the IBS subtypes. However, more data are needed to understand the balance of improved symptom control versus the potential negative impact on QOL due to the dietary restrictions imposed. Importantly, once a patient has completed the re-challenges, their improved understanding of their own food tolerance can assist them to establish their own modified FODMAP diet to be used in the long-term. Evidence for the re-challenge phase. Owing to the relatively recent emergence of the low FODMAP diet, most studies to date have focused on confirming the efficacy of the restrictive phase. Preliminary data regarding symptom control and total dietary intake are now emerging for the reintroduction phase and the use of the diet in the long-term. One study has specifically assessed long-term dietary intake and level of FODMAP reintroduction in patients with IBS. Follow-up questionnaires provided to 100 patients at 6 18 months following initial education showed that 62% had satisfactory relief on the low FODMAP diet. Of those, 71% continued to have satisfactory relief at 1 year postreintroduction, and 68% continued to avoid high FODMAP foods at least 50% of the time. 8 Another study providing a follow-up questionnaire at 6 months post-treatment found that those who had remained on a strict or attenuated diet at 6 months had a significantly greater symptomatic improvement at 6 weeks compared with those who had abandoned the diet, although information on the level of reintroduction was not assessed. 9 Those who had abandoned the diet were likely to have been unresponsive within the initial 6-week strict elimination phase. 9 It is key that those who do not respond to the low FODMAP diet should not be encouraged to continue on the dietary restrictions. Further, longterm data on the re-challenge phase are needed regarding how challenges are carried out, amount of high FODMAP foods patients are able to reintroduce back into the diet, and the effects this has on nutritional adequacy, microbiota composition, and QOL. Undertaking the re-challenge process. Despite limited evidence, re-challenge protocols have been established based on clinical experience. The re-challenge phase is usually commenced following 2 6 weeks on the restrictive phase of the low FODMAP diet. The length of time on the restrictive phase can be adapted depending on the time required for an adequate symptom response to occur as well as constraints related to, for example, clinic waiting times. The degree of symptom improvement provided by the restrictive phase is variable between patients and should be discussed with the patient prior to commencing the re-challenge process in order to establish level of baseline symptom control. Figure 1 provides a flowchart of steps of the re-challenge phase. The dietitian plays a key role in assisting the patient to complete the challenge process in a strategic way to ensure patients are able to identify specific dietary triggers for their symptoms. The rechallenge phase can finally provide patients with some certainty around their dietary intolerances, of which patients have often struggled for many years. Patients are encouraged to remain on the strict low FODMAP diet while completing the challenges. One challenge is completed at a time, often over a 3-day period. Owing to differing physiological effects of FODMAPs in the gastrointestinal tract, 10 it is important that each FODMAP subgroup be challenged individually as tolerance to each may vary. Table 1 provides example challenge foods and doses for each FODMAP subgroup. The suggested foods only contain significant amounts of one FODMAP subgroup; for example, milk is high in lactose and does not contain any other FODMAP subgroup. Small doses are listed in Table 1 and can be used as a guide, but the dosage used in practice should be adapted to the patient. As outlined in Table 1, some challenges may be better tolerated if consumed every second day rather than in consecutive days; hence, the food can be challenged second daily first and, if well tolerated, challenged again across consecutive days. Patients are encouraged to monitor and record their symptom types and severity throughout the challenges. If a particular challenge causes a significant increase in symptoms, it is recommended the patient stops challenging this particular food. If symptoms continue to be controlled, then patients can increase the dosage of the challenge food toward their preferred serving size. Between challenges, patients are encouraged to have a 2- to 3-day washout to ensure no additive and/or crossover effects occur. Once tolerance to each subgroup is established, patients are encouraged to assess their tolerance to larger doses, increased frequency, and combinations of high FODMAP foods. At this point in the re-challenge process, challenges should be adapted to suit the specific dietary needs of the patient and to assist the patient to return toward their pre-morbid diet. As an example, a patient may choose to challenge with honey to determine their tolerance to excess fructose (Table 1). Honey is chosen as it is a food that contains excess fructose but is not high in other FODMAP subgroups. One teaspoon of honey is consumed per day, for 3 days. If symptoms worsen, the patient should be encouraged to stop the challenge. Alternatively, if good symptom control persists, on the third day, they may increase the dosage to two teaspoons and monitor their response for a further 1 2 days or as long as the dietitian and patient feel is required to adequately assess symptom response. Following the excess fructose challenge, the patient should be advised to undertake a 2- to 3-day break remaining on the low FODMAP diet, prior to commencing the next challenge in order to ensure no additive or crossover effect occurs. If they have had good symptom control during the 12

C Tuck and J Barrett Re-challenging FODMAPs Figure 1 Flowchart of the re-challenge process. honey challenge, future challenges to evaluate FODMAP combinations and higher total FODMAP doses could include trialing honey on wheat bread (or other alternatives depending on the patient s preferences and tolerance). Table 1 Examples of re-challenge foods for each FODMAP subgroup FODMAP Suggested food Quantity Frequency Excess fructose Honey 1 tsp Daily for 3 days Mango ½ mango Lactose Milk ½ cup Daily for 3 days Yoghurt 200 g Sorbitol Avocado ⅓ ½ avocado Daily for 3 days Apricot 1 small Mannitol Mushroom ½ cup Daily for 3 days Cauliflower ½ cup Fructose + sorbitol Apple ½ apple Daily for 3 days Pear ½ pear Fructan (wheat) Wholemeal bread Pasta 1 slice Second daily for 3 days 1 cup Fructan (onion/garlic) Onion 1 ring Second daily for Garlic ¼ ½ clove 3 days GOS (galactooligosaccharides) Lentils ½ cup Daily or second Chickpeas 2 tbs daily for 3 days The order and nature of the challenges completed should be adapted to suit the patients needs. Foods that were previously consumed more frequently may be those that the patient would prefer to challenge earlier. Foods that the patient suspects to be a trigger may be best to be challenged later. The quantity of foods trialed and the specific food chosen to represent each FODMAP subgroup should be adapted to the patients preferences and usual dietary intake. For example, challenging their intake of yoghurt with one cup provides irrelevant information if the most yoghurt they would ever consume is two tablespoons in one sitting. The dietitian has a key role in helping the patient understand and interpret the response to each challenge. Those challenges in which no symptoms occur are likely foods that the patient can reintroduce back into their diet freely. Foods that cause a mild response may be reintroduced at times when the patient is able, such as when the patient is at home, or smaller doses at a lower frequency could be trialed. Those foods that cause more severe symptoms should be avoided in the long-term for optimal symptom control. However, symptoms of FBD can vary over time within the individual, and foods that are not tolerated should be re-challenged at another time, with the long-term aim of increasing intake of prebiotics, including preferred foods and optimizing dietary adequacy. An alternative to completing the re-challenge phase in this way is to utilize the Monash University, Low FODMAP diet smartphone application. 11 Information within the app is provided using a traffic light rating of green, amber, and red serves representing low, moderate, and high FODMAP content, respectively. 11 14 Green and amber foods represent foods containing low and moderate quantities of FODMAPs and are designated as 13

Re-challenging FODMAPs C Tuck and J Barrett suitable during the restrictive phase of the diet. To assist with reintroductions, patients may gradually increase intake of amber serves and assess tolerance. Subsequently, they may increase intake of red serves as tolerated to gradually increase total FODMAP intake. This particular approach is more suitable for patients who may struggle to complete more structured challenges for reasons such as time constraints or unpredictable and unplanned meal patterns. Re-challenging in special populations. Care should be taken when working with patients who have additional dietary requirements such as vegetarians, patients with diabetes, or those with additional food intolerances. The dietitian can assist these patients to preferentially reintroduce foods of highest nutritional concern. For example, protein sources can be limited during the restrictive phase for patients following a vegetarian diet owing to the high FODMAP content of legumes. Therefore, the dietitian may encourage vegetarians to challenge legumes early in the challenge process and may suggest more strategic legume challenges (e.g. assessing tolerance to multiple different types of legumes) in an effort to increase the likelihood of meeting protein requirements. Patients with diabetes may need to consider carbohydrate sources to assist in blood glucose control, and therefore, the choice of challenge foods in particular for the fructan challenge should be chosen carefully. Finally, anxiety is common in patients with FBD, and hence, the patients level of anxiety toward completing food challenges is important to consider. Those patients who report more anxiety or reluctance to challenge may benefit from a modified re-challenge approach. This may include challenging with smaller serving sizes or at reduced frequency. These patients may prefer to use the alternative method of challenging by gradually increasing FODMAP intake using the traffic light rating system in the smartphone application as discussed previously. It is important to note, the stress surrounding the FODMAP challenge process may in itself induce symptoms in anxious patients due to the interaction of the brain gut axis. 15 The dietitian should adapt the challenge process accordingly with the aim of reducing these effects and utilize his or her important counseling skills. The dose effect. Data are available from sugar solution studies to show the effect of different FODMAP doses on gastrointestinal symptoms. One study comparing symptom response found that symptoms were more frequent at higher dose of fructose, with 71% experiencing symptoms at 50 g fructose dose compared with 48% at a 25 g dose. 16 Another study comparing symptoms with fructose, fructan, and combined solutions also found that the presence of symptoms occurred more frequently with increasing dose. 17 The data are more limited for the additive effect when FODMAPs are ingested in combination, which commonly occurs in foods such as an apple that contains both excess fructose and sorbitol. The fructan/fructose combined solution in the aforementioned study showed increased symptoms compared with fructose alone but not fructan alone. 17 Despite data from sugar solutions studies, limited data are available on how varied doses of individual FODMAPs or FODMAPs in combination in every day foods and fluids may affect symptoms owing to the difficulty in conducting well-controlled studies using whole food, because of the complexities of the food matrix. Hence, a strategic and individualized re-challenge phase that includes varying doses of individual FODMAPs and combinations of FODMAPs specific for each patient is vital to assist the patient in assessing their own tolerance thresholds. Long-term concepts. Once the re-challenges are completed, the patient is encouraged to then follow their own individual modified version of the low FODMAP diet in the longer term, ensuring that their diet is only as restrictive as their symptoms require. Strategies to assist the patient in the long-term should be discussed; for example, limiting intake of higher FODMAP foods prior to eating out may assist the patient to better tolerate meals eaten away from the home. Advice regarding the prebiotic effect of higher FODMAP foods may help to motivate the patient to reintroduce well-tolerated foods. Patients should also be advised that a certain degree of symptoms is normal (for example, some flatulence or bloating after a large meal are common); that the patient may find symptoms worsen in times of heightened stress; and that functional gastrointestinal symptoms may change over time, hence food tolerance may not remain stagnant. Limitations of the current literature. Despite the challenges faced with implementing dietary studies, some data are now emerging regarding the long-term use of the low FODMAP diet and the implementation of the re-challenge phase. However, significant gaps exist in the current literature including the level of FODMAP reintroduction tolerated by patients, whether tolerance to FODMAPs changes over time, and if reintroduction leads to changes in the microbiota and nutritional adequacy. Further data on the degree of dietary FODMAP restriction required for individual patients would be beneficial to help tailor the diet more specifically to the individual patients needs. This may only be possible with the identification of biomarkers or clinical features that could predict an individual s sensitivity to specific FODMAP subgroups. Conclusions While evidence is limited regarding the re-challenge phase, it is an integral part in the dietary management of patients who undergo the low FODMAP diet. A suggested re-challenge protocol based on clinical experience has been set out here. Re-challenging high FODMAP foods is critical to reduce the burden of dietary restrictions and to avoid potential negative effects on the microbiota, nutritional adequacy, and QOL. The principle aim of the re-challenge phase is to identify specific dietary triggers and reintroduce foods that are well tolerated. The dietitian has a key role in supporting patients in correctly identifying dietary triggers and to ensure long-term nutritional adequacy. Further data to provide best practice guidelines for re-challenging FODMAPs are required. References 1 Tuck CJ, Muir JG, Barrett JS, Gibson PR. Fermentable oligosaccharides, disaccharides, monosaccharides and polyols: role in irritable bowel syndrome. Expert Rev. Gastroenterol. Hepatol. 2014; 8: 819 34. 14

C Tuck and J Barrett Re-challenging FODMAPs 2 Lomer M. Review article: the aetiology, diagnosis, mechanisms and clinical evidence for food intolerance. Aliment. Pharmacol. Ther. 2015; 41: 262 75. 3 Staudacher HM, Lomer MCE, Anderson JL et al. Fermentable carbohydrate restriction reduces luminal bifidobacteria and gastrointestinal symptoms in patients with irritable bowel syndrome. J. Nutr. 2012; 142: 1510 8. 4 Halmos EP, Christophersen CT, Bird AR, Shepherd SJ, GIbson PR, Muir JG. The low FODMAP diet alters the composition of the colonic microbiota compared to a typical Australian intake in patients with irritable bowel syndrome: a randomised controlled cross-over trial. J. Gastroenterol. Hepatol. 2013; 28 (Suppl. 2): 122. 5 Gibson PR, Varney J, Malakar S, Muir JG. Food components and irritable bowel syndrome. Gastroenterology 2015; 148: 1158 74.e4 6 Staudacher H, Ross F, Briscoe Z, Irving P, Whelan K, Lomer M. PTU- 183 Advice from a dietitian regarding the low fodmap diet broadly maintains nutrient intake and does not alter fibre intake. Gut 2015; 64 (Suppl 1): A143 A1A4. 7 Pedersen N, Andersen NN, Végh Z et al. Ehealth: Low FODMAP diet vs Lactobacillus rhamnosus GG in irritable bowel syndrome. World J. Gastroenterol. WJG. 2014; 20: 16215. 8 Martin L, van Vuuren C, Seamark L et al. OC-104 Long term effectiveness of short chain fermentable carbohydrate (FODMAP) restriction in patients with irritable bowel syndrome. Gut 2015; 64 (Suppl 1): A51 AA2. 9 Peters S, Yao C, Shepherd S et al. Su1369 Gut-directed hypnotherapy and a low FODMAP diet are similarly efficacious in patients with irritable bowel syndrome: a randomised controlled non-inferiority trial. Gastroenterology 2015; 148: S-487 S-S-8. 10 Murray K, Wilkinson-Smith V, Hoad C et al. Differential effects of FODMAPs (fermentable oligo-, di-, mono-saccharides and polyols) on small and large intestinal contents in healthy subjects shown by MRI. Am. J. Gastroenterol. 2013; 109: 110 19. 11 Monash University. The Monash University Low FODMAP App. http://wwwmedmonashedu/cecs/gastro/fodmap/. 12 Muir JG, Shepherd SJ, Rosella O, Rose R, Barrett JS, Gibson PR. Fructan and free fructose content of common Australian vegetables and fruit. J. Agric. Food Chem. 2007; 55: 6619. 13 Muir JG, Rose R, Rosella O et al. Measurement of short-chain carbohydrates in common Australian vegetables and fruits by highperformance liquid chromatography (HPLC). J. Agric. Food Chem. 2009; 57: 554. 14 Biesiekierski JR, Rosella O, Rose R et al. Quantification of fructans, galacto-oligosacharides and other short-chain carbohydrates in processed grains and cereals. J. Hum. Nutr. Diet. 2011; 24: 154 76. 15 Mayer EA, Tillisch K. The brain gut axis in abdominal pain syndromes. Annu. Rev. Med. 2011; 62: 381 96. 16 Goebel-Stengel M, Stengel A, Schmidtmann M, van der Voort I, Kobelt P, Mönnikes H. Unclear abdominal discomfort: pivotal role of carbohydrate malabsorption. J Neurogastroenterol Motil. 2014; 20: 228. 17 Shepherd SJ, Parker FC, Muir JG, Gibson PR. Dietary triggers of abdominal symptoms in patients with irritable bowel syndrome: randomized placebo-controlled evidence. Clin. Gastroenterol. Hepatol. 2008; 6: 765 71. 15