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Influence of Dietary Restriction on Irritable Bowel Syndrome

Kamal, Afrin, MD1; Pimentel, Mark, MD, FRCP(C)2

American Journal of Gastroenterology: February 2019 - Volume 114 - Issue 2 - p 212–220
doi: 10.1038/s41395-018-0241-2
REVIEW ARTICLES

Up to two-thirds of patients with IBS attribute their gastrointestinal symptoms to food. The therapeutic focus of IBS has been to alleviate gastrointestinal symptoms, approached by pharmaceutical and non-pharmaceutical treatments. Although the most traditional approach has involved the use of medications such as bulking agents, anticholinergics, antispasmodics, and antidiarrheals, unfortunately these are only modestly effective and patients are left with a small menu of successful pharmacologic agents. These treatments, however, are not always enough to alleviate symptoms. Alternative approaches have therefore been tried, including dietary manipulation. This article aims to review dietary restrictions as a non-pharmaceutical management approach for IBS, covering literature on various dietary triggers and the impact of dietary manipulation on gastrointestinal symptoms.

1Department of Gastroenterology and Hepatology, Digestive Diseases and Surgical Institute, Cleveland Clinic, Cleveland, OH, USA;

2Department of Gastroenterology and Hepatology, Digestive Diseases Center, Cedars-Sinai, Los Angeles, CA, USA.

Correspondence: Mark Pimentel, MD, FRCP(C). E-mail: Mark.Pimentel@cshs.org.

Received February 27, 2018

Accepted July 18, 2018

Irritable bowel syndrome (IBS) is a chronic gastrointestinal (GI) disorder that classically presents with symptoms of abdominal pain, bloating, and altered bowel habits of diarrhea or constipation. IBS affects ∼11% of the population globally (1), with an increased prevalence in young individuals and females (2). Currently the diagnosis of IBS relies on the fourth version of the criteria set by the Rome Foundation, encompassing symptoms of recurrent abdominal pain and changes in stool frequency and form, in the setting of absent alarm features or structural abnormalities (3–5). Based on predominant bowel habits, IBS is further classified into one of four subtypes: constipation-predominant (IBS-C), diarrhea-predominant (IBS-D), predominant irregular (mixed diarrhea/constipation) bowel habits (IBS-M), and unspecified (IBS-U) (6). What causes these symptoms, however, is unknown. Proposed pathophysiologies for IBS include heightened pain sensitivity or visceral hypersensitivity, abnormal gut motility, low-grade intestinal inflammation, post-infectious enteritis, and abnormalities in the gut–brain axis (7–9).

The therapeutic focus of IBS has been to alleviate gastrointestinal symptoms, approached by two methods: pharmaceutical and non-pharmaceutical treatments. The most traditional approach to treating IBS has involved the use of medications such as bulking agents, anticholinergics, antispasmodics, and antidiarrheals in efforts to specifically target gastrointestinal symptoms. However, these are only modestly effective and patients fortunately now have a small menu of successful pharmacological treatments meeting new and more objective benchmarks for US Food and Drug Administration (FDA) approval (10). For IBS-C these include lubiprostone (11) and linaclotide (12) and for IBS-D, rifaximin (13, 14) and eluxadolinea (15). For severe cases of IBS-D in women who have failed other therapies, alosetron (16, 17) may also be used.

Unfortunately, pharmaceutical treatments alone are not always enough to provide adequate symptom relief (18). In such cases, alternative approaches are tried. Examples of these include cognitive-behavioral therapy, hypnotherapy, exercise, and more commonly dietary manipulation (7). The use of dietary control in IBS management reflects the 84% of patients who attribute their symptoms to dietary intake. Therefore, a rising trend has been to restrict specific foods in an effort to minimize post-prandial symptoms (19). This article aims to review dietary restrictions as a non-pharmaceutical management approach for IBS, covering literature on various dietary triggers and the impact of dietary manipulation on gastrointestinal symptoms.

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GLUTEN RESTRICTION

Up to two-thirds of patients with IBS attribute their gastrointestinal symptoms to food (20). Many food components have been proposed as contributing toward IBS symptoms, gluten being one. Symptoms of long-standing abdominal pain and altered bowel habits, although characteristic of IBS, are not specific for the disorder. A similar symptom pattern can be seen in celiac disease and non-celiac gluten sensitivity (NCGS), two disorders characterized by their intolerance to gluten, or grains that encompass wheat, barley, rye, or triticale. Celiac disease describes a chronic immune-mediated enteropathy instigated by the exposure to dietary gluten in predisposed individuals carrying the genotype HLA-DQ2 or HLA-DQ8. In these individuals, exposure to gluten can cause symptoms of abdominal pain, bloating, diarrhea, and constipation (21). Whereas celiac disease is the result of dietary gluten exposure in genetically susceptible hosts, in contrast, NCGS refers to individuals with signs, symptoms, or extra-intestinal manifestations related to gluten intake or wheat proteins in the absence of known immune-mediated injury or genetic biomarkers. Due to this lack of specificity, NCGS is suspected when individuals present with diarrhea, bloating, flatulence, and/or abdominal discomfort as well as extra-intestinal symptoms, with subsequent symptom improvement after gluten cessation in the setting of a negative work up for celiac disease (21–24). Considering both celiac disease and NCGS present with gastrointestinal symptoms paralleling IBS, and ∼5% of patients with IBS have confirmed celiac disease (24), the question arises - is there a role for gluten-free diet as a means for IBS management?

Biesiekierski et al. measured this association in a double-blind, randomized, placebo-controlled trial. After excluding individuals with celiac disease, authors designated IBS patients to receive either placebo or gluten in the form of two bread slices and one muffin daily for up to 6 weeks. Of the 19 patients in the gluten arm, 13 (68%) reported uncontrolled symptoms, in comparison to 6 of 15 (40%) in the placebo arm (p=0.001). Patients exposed to gluten complained of worsening pain, bloating, satisfaction with stool consistency, and tiredness within 1 week of gluten exposure (25). Further comparison of a 4-week trial of gluten-free diet (GFD) to a gluten-containing diet (GCD) was performed by Vazquez-Roque et al. Patients meeting the Rome II criteria for IBS-D and with genotype analyses for HLA-DQ2 and HLA-DQ8 underwent a 14-day baseline and 28-day study period. Patients recorded daily bowel patterns including ease of passage, completeness of evacuation, and date and timing of each bowel movement; while authors measured gastric, small bowel, and colonic transit by scintigraphy, and small bowel and colonic mucosal morphology and permeability using hematoxylin and eosin (H&E) stained sections from biopsy specimens. Following the 4-week diet intervention, authors identified an increase in stool frequency among subjects with positive HLA-DQ2/DQ8 who were exposed to gluten. Subjects on a GCD experienced more frequent bowel movements (p=0.04) and higher small bowel permeability, particularly among HLA-DQ2/ DQ8 positive subjects (26).

Despite the above-described study, there is controversy as to the potential of gluten-free diets in managing IBS symptoms. This stems from a double-blind, cross-over trial which tested gluten in combination with a reduced intake of fermentable oligo-, di-, mono-saccharides, and polyols, referred to as a low FODMAP diet. IBS subjects were randomly assigned to a reduced FODMAP diet plus high-gluten (16 g gluten/day), low gluten (2 g gluten/day and 14 g whey protein/day) or control (16 g whey protein/day) for two weeks, followed by a two-week washout period. Subsequently, twenty-two subjects crossed over and were given either gluten (16 g/day), whey (16 g/day), or control for 3 days. At study conclusion, all participants improved with a reduced FODMAP diet, and experienced significant worsening of symptoms with the introduction of gluten or whey protein. Gluten-specific symptoms, however, were reproduced only in 8% (27). This study suggested the carbohydrate component of fructans, wheat, and galacto-oligosaccharides may be responsible for IBS symptoms, and not specifically gluten (7). Fructans being a possible cause of symptoms was seen in a randomized, double-blind, placebo-controlled, cross-over study aiming to assess effects of gluten and fructan on gastrointestinal symptoms in patients with self-reported non-celiac sensitivity by Skodje et al. Following exclusion of celiac disease by negative duodenal biopsies on gluten-free diet or lack of HLA-DQ2 and HLA-DQ8 genetic markers, individuals were challenged with a seven-day diet rich in gluten (5.7 g), fructans (2.1 g), or placebo, followed by a washout period, and crossed over into another diet group. The study was complete when subjects had been challenged with all three diets. The authors measured gastrointestinal symptoms using the Gastrointestinal Symptom Rating Scale, IBS-version (GSRS-IBS) and among the 59 patients challenged, results demonstrated a significantly higher symptom score after fructan intake (p=0.049) than after gluten (28).

Furthermore, when reviewing the structure of a gluten-free diet, a common factor to note is the removal of foods composed of wheat, barley, rye, and triticale. Therefore, foods that are allowed due to their natural gluten-free properties include beans, eggs, fresh meats, fish, and poultry, in addition to fruits, vegetables, and most dairy products (29). What one will notice is the limited carbohydrates allowed, as unfortunately wheat is a common grain used in the production of breads, pastas, and baked goods (30). Due to this limitation in carbohydrates, the effects of a very low-carbohydrate diet (VLCD) emerged as a possible explanation for IBS symptom improvements, rather than the removal of gluten from the diet. VLCD has received significant attention as means of weight loss and consists of <20–50 g/day of carbohydrates paired with a high fat or high protein diet (31), more commonly referred as a ketogenic diet (32). This has proven effective in weight loss therapy and reducing cardiovascular risk factors (33). Austin et al. prospectively assessed this diet in IBS management, evaluating relief of stool frequency and abdominal pain in 13 out of 17 enrolled patients meeting Rome II criteria for IBS-D. After initially placing subjects on a standard diet (55% calories from carbohydrates, 30% from fat, and 15% from protein) for 2 weeks, followed by a VLCD limited to 20 grams per day (51% calories from fat, 45% from protein, and 4% from carbohydrates), authors noted 10 (77%) patients described adequate relief in stool frequency and abdominal pain after all four weeks (34). Looking further into carbohydrate intake, specifically absorption capacity, Goldstein et al. measured differences in absorption of lactose (18 g), fructose (25 g), and mixture of fructose (25 g) plus sorbitol (5 g) between 94 patients meeting Rome criteria for IBS and 145 patients defined as functional. Following administration of carbohydrate solutions weekly, hydrogen and methane breath tests were performed. All individuals were subsequently maintained on a 1-month restricted diet lacking all tested sugars. Authors revealed only 7% of IBS patients absorbed all three sugars normally compared to non-IBS patients, with a frequency of lactose malabsorption at 16% vs. 12%, respectively. Following dietary restriction, 56% of IBS patients experienced marked symptom improvement (p<0.01) (35). These study indicated that when carbohydrates are limited, whether due to the limitation of wheat or sugars, patients with IBS demonstrate improvement in symptoms. Together, these studies suggest that although gluten can be thought of as contributing to IBS-like symptoms, when considering carbohydrates, we may be looking entirely in the wrong direction?

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LACTOSE RESTRICTION

Lactose is an importance source of calories from all mammalian milk, with the exception of sea lions (36). To appropriately absorb lactose, humans require the enzyme lactase-phlorizin hydrolase (LPH), located in the brush-borders of the small intestine. This enzyme, more simply referred to as lactase, functions by hydrolyzing the disaccharide lactose into the monosaccharides glucose and galactose, facilitating intestinal absorption. When this enzyme becomes deficient, however, the end result is lactose malabsorption (37).

Humans experience a rise in lactase activity starting at week eight of gestation and increasing until week 34, with its expression peaking at birth. In up to two-thirds of the world’s population, however, this activity decreases following first months of life (36). This decline in activity occurs by down-regulating lactase expression, referred to as primary lactase deficiency. Conversely secondary lactase deficiency, or acquired hypolactasia, refers to the decrease in lactase activity after injury to the small bowel mucosal brush border. This can be seen following a gastrointestinal viral or non-viral infection, after abdominal surgery, or secondary to a diagnosis of inflammatory bowel disease (IBD). Contrary to individuals with primary deficiency, those with secondary lactase deficiency can experience a drop in enzyme activity at any age and have the potential to restore this activity following elimination of the underlying disorder (38).

When lactase is deficient, the milk sugar fails to be absorbed by the proximal small bowel and continues into the distal small bowel and colon. Unabsorbed lactose is subsequently fermented by colonic bacteria producing short chain fatty acids (SCFA) and gas, mainly hydrogen (H2), carbon dioxide (CO2), and methane (CH4). The non-digested contents additionally lead to an increase in osmotic load and therefore a rise in intestinal water content. Together, these changes contribute to symptoms of lactose intolerance including diarrhea, bloating, and abdominal pain (37).

It is easy to recognize that the symptoms of lactose intolerance are similar symptoms to those of IBS, and researchers have explored whether a relationship between the two disorders exists. In a Norwegian population of IBS patients, Farup et al. measured variations in symptoms after intake of milk and lactose, in addition to the presence of lactose malabsorption, as compared to healthy volunteers. In the 187 patients [IBS (n=82) and healthy volunteers (n=105)], the authors noted that despite a high prevalence of symptoms following milk (p<0.001) and lactose (p<0.01) among IBS patients, the presence of true lactose malabsorption was low (4.1%) (39). When considering whether self-reported lactose intolerance (SLI) predicted findings on lactose hydrogen breath test, Zheng et al. took a group of patients with lower digestive tract symptoms and assessed the presence of IBS by Rome III, the presence of SLI by questionnaires and the presence of lactose malabsorption by breath test. The authors revealed that although SLI was found to be higher among those with IBS than other participants (p<0.001), the rise in hydrogen confirming lactose malabsorption was found to be the same in both groups (61% vs. 54% respectively, p=0.14) (40). In essence, IBS patients may more commonly report lactose intolerance-like symptoms, however these symptoms are not predictive of true lactose malabsorption.

In efforts to assess whether IBS symptoms change following a lactose restriction diet, Parker et al. followed 33 patients with known IBS and lactose intolerance diagnosed by hydrogen breath test (LHBT) in a double-blind, placebo-controlled challenge. Subjects followed a lactose-restricted diet for three weeks, and those who improved were subsequently placed on diets containing 5 g, 10 g, or 15 g of lactose or placebo. Applying symptom scores following dietary changes, authors noted only moderate symptom improvement (39%) in patients on a low-lactose diet (41). Similarly Vernia et al. designed a prospective trial measuring lactose malabsorption prevalence in 230 Italian patients with suspected IBS, in addition to clinical effects of long-term lactose-free diets. Applying hydrogen breath tests, 157 patients (68.2%) were identified with lactose malabsorption. Of the 110 patients compliant with diet restrictions, 48 (43.6%) reported symptom cessation, 43 (39%) noted reduced symptoms, and 17 (15.5%) described unchanged symptoms (42). Prospectively, in a 5-year follow up study quantifying effects of lactose-restriction in patients with IBS and lactose malabsorption, the latter confirmed by hydrogen breath testing and blood-glucose measurements, Böhmer et al. demonstrated that at 6 weeks, patients reported marked improvement in symptoms (p<0.001). Subsequently at 5 years, the majority continued to report symptom improvement (88%). Unique to this study was the author’s ability to express cost and change in number of outpatient visits as a result of diet restriction. In 16 patients, a mean of 2.4 visits/year/person (range 1–7 visits) was seen before diet initiation, significantly decreasing at 5 years to a mean of 0.6 visits/year/person (range 0–6 visits). Hence, the authors not only demonstrated short and long-term GI symptom improvement after following a lactose-restricted diet, but an additional decline in cost and time spent on outpatient visits (43).

Although some studies have demonstrated improvement in GI symptoms with lactose-restriction in IBS, authors have questioned the accuracy of lactose malabsorption diagnosis following breath testing. To review, a rise in H2 occurs following colonic fermentation of unabsorbed lactose. This is excreted into expired air, and is detectable on breath testing (44). Therefore hydrogen breath tests have become a common means to detect lactase deficiency, measured after ingesting 25 g of lactose mixed with or following one cup of water and observing a rise of ≥20 parts per million (ppm) from baseline hydrogen (45).

The difficulty occurs when subjects with IBS have underlying small intestinal bacterial overgrowth (SIBO), which is present in >50% of these patients (44). When the milk sugar is incompletely digested, it reaches the distal small bowel as lactose residue. In patients with bacterial overgrowth, the lactose is fermented before it has time to be broken down and absorbed, resulting in a false increase in hydrogen on a lactose breath test (45). This concept that the presence of bacterial overgrowth can lead to early fermentation and elevation of exhaled hydrogen was proposed by Pimentel et al. when observing diarrhea-predominant IBS subjects after a lactulose breath test and lactose tolerance test. Nineteen subjects underwent an initial lactulose breath test, and within 7 days, patients returned for a fasting lactose breath test and blood glucose measurement. The authors demonstrated a significant relationship between hydrogen production on lactulose and lactose breath testing (r=0.56, p=0.01), suggesting that lactose breath testing in the IBS population may be reflective of bacterial overgrowth, rather than a reflector of true lactose malabsorption (46). This lead to the consensus that using breath testing to rule out lactose malabsorption necessitated the need to first rule out SIBO (45).

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LOW FRUCTOSE, LACTOSE, FRUCTO- AND GALACTO-OLIGOSACCHARIDES AND POLYOLS (FODMAP)

In efforts to define an improved diet therapy for IBS, a global restriction of fructose, lactose, fructo-, and galacto-oligosaccharides (fructans galactans), and polyols (sorbitol, mannitol, xylitol, and malitol), termed fermentable oligo-, di-, monosaccharides, and polyols or “FODMAP” was designed. The logic behind restricting FODMAPs was two-fold. First, short-chain carbohydrates were found to be poorly absorbed in the small intestine, particularly under conditions of low or absent brush border enzymes (e.g., lactase) and the presence of low-capacity epithelial transporters. When poorly absorbed, FODMAPs create an osmotic load and consequently draw fluid into the small intestine, leading to symptoms of abdominal distention and an increased colonic delivery of fluid (7). This physiologic change was demonstrated in a randomized, cross-over, single-blinded intervention study of 12 ileostomates consuming two diets differing in FODMAP content. By measuring the 14 h ileal effluents on day 4 of each diet, authors demonstrated an increased mean effluent weight, water content, and dry weight on a high versus low FOD-MAP diet. These results suggest that FODMAPs augment colonic delivery of water and fermentable substrates (47).

The second logic behind restricting FODMAPs is the feature of rapid fermentation of the short-chain carbohydrates by colonic microbiota, resulting in increased gas production (H2, CO2, and CH4) and colonic distention. In the setting of underlying gut dysmotility and visceral sensation, symptoms can manifest as pain, cramping, and bloating (48, 49). This hypothesis was tested by comparing patterns of breath hydrogen and methane with symptoms in response to differing diets of FODMAP content. In a single-blind, crossover intervention study involving 15 individuals with IBS and 15 controls, subjects maintained food and symptom diaries after consuming either a low (9 g/day) or high (50 g/day) FODMAP diet. Those with IBS consuming high FODMAP diets produced higher levels of breath hydrogen than healthy volunteers, suggesting FODMAPs induce increased intestinal fermentation and hydrogen production in IBS (49).

Subtypes within FODMAP exist based on carbohydrate length, as seen in Table 1. Oligosaccharides are the longest chain and composed of fructans and galacto-oligosaccharides (GOS). These are naturally found in wheat, rye products, legumes, nuts, artichokes, onions, and garlic. As humans we lack enzymes to break down fructans and GOS (hydrolase), illustrated in Table 1, the higher the intake, the greater the increase in fermentation and gas production. This leads to bloating, abdominal pain, and excessive flatus.

Table 1

Table 1

Disaccharides such as lactose, as mentioned previously, require lactase activity for absorption. By assessing lactose absorptive capacity through hydrogen breath testing, individuals can tailor dietary lactose intake. Monosaccharides include fructose, the smallest chain subtype, found naturally in apples, pears, mango, watermelon, honey, and a few vegetables including sugar snap peas. Commercially, fructose is found in sweeteners and corn syrup. Due to its size, fructose leads to a high osmotic effect, leading to increased small bowel water content. The larger fructose load parallels the increased risk of diarrhea and altered intestinal motility. Lastly, polyols comprise mannitol and sorbitol, naturally found in apples, pears, cauliflower, mushroom, and snow peas. Similar to fructose, this group exhibits slow absorption and high osmotic effects along the small bowel length (50).

Studies exploring the effect of dietary FODMAP restriction in IBS have generally been positive and support overall improvements GI symptoms. Previous studies suggested restricting lactose alone, or fructose with or without sorbitol, as a dietary approach in managing IBS. The latter worked well in patients with fructose malabsorption. However as mentioned above, fructans are poorly absorbed in humans due to lack of hydrolase. Prior to the concept of FODMAP, dietary fructan restriction was not standard. Based on the hypothesis that dietary FODMAP restriction optimized symptom control in IBS, in particular fructans, fructose, and foods with free fructose exceeding free glucose, Shepherd et al. measured daily dietary symptoms after graded introduction of fructose, fructans, alone or in combination, or glucose taken in drinks, followed by a 10-day washout period. The authors revealed that symptom triggers in the IBS population included not only fructose, but also fructans. This was the first evidence suggesting dietary FODMAP reduction specifically of fructose and fructans, could lead to symptom improvement (51).

To compare the effects of a reduced FODMAP diet to traditional dietary advice in IBS such as avoiding larger meals, reduced fat intake, and reduced excessive fiber and gas-producing foods, Böhn et al. performed a multi-center, randomized trial comparing symptoms. The results demonstrated that IBS symptoms severity reduced significantly in both dietary groups (p < 0.0001), however no significant difference was found between the two diets (52). In contrast, Eswaran et al. compared a low FODMAP diet to a diet based upon the modified National Institute for Health and Care Excellence (mNICE) guidelines in individuals with IBS-D in a randomized, controlled trial. After 4-weeks of either diet, individuals reported relief of IBS-D symptoms including change in abdominal pain and stool consistency based on the Bristol Stool Form. The authors demonstrated that individuals following a low FODMAP diet reported greater improvements in abdominal pain, stool consistency, frequency, and urgency compared to those following the mNICE diet (53). Furthermore, parallel to the hypothesis that symptoms associated with IBS relate to intraluminal gas production, Ong et al. sought to measure a similar pattern relating breath hydrogen and methane to changes in FODMAP content. In this randomized, single-blinded, crossover intervention study, the authors compared two FODMAP diets: either low (9 g/day) or high (50 g/day), between healthy volunteers and subjects with IBS. Not only was higher breath hydrogen production seen in the high FODMAP group, but increased gastrointestinal symptoms and lethargy were also significantly induced among IBS patients (49).

The degree of malabsorption with FODMAPs differs with each individual, therefore is not considered a “one-size-fits-all” approach. The recommendation of a restricted FODMAP diet is short-term, initiating a full elimination for 2–6 weeks with aid of a licensed dietician. Understanding individuals’ tolerance level to FODMAPs differ, with tailored dietary counseling foods containing FODMAPs are gradually re-introduced, arriving at an individualized and less restricted “low FODMAP” diet (50). When a low FODMAP diet does not work, or demonstrates no clinical efficacy, it is recommended to transition towards other therapeutic interventions (54).

Long term implications are to be considered when applying FODMAPs. The fermentable carbohydrates in FODMAPs provide substrates for healthy bacteria. Studies have compared low FODMAP to the traditional IBS diet, revealing a reduction in proportion and concentration of Bifidobacteria while other studies have demonstrated a decrease in total bacteria (55,56). Additionally, fermentation by natural colonic microbiota generates products including short-chain fatty acids, which provide nutrients to the colonic mucosa (butyrate) and are used as substrates for lipogenesis and gluconeogenesis (acetate, propionate). The change in micronutrient intake with a low FODMAP diet was recently measured by Farida et al. in a single-center, randomized-controlled study of individuals with IBS-D on a low FODMAP diet compared to mNICE guidelines, or standard dietary recommendations. Among 78 patients, 41 were randomized to follow a low FODMAP diet whereas 37 patients followed the mNICE diet. At 4-weeks, a statistically significant decrease in retinol (p=0.03), thiamin (p=0.009), riboflavin (p=0.045), and calcium (p=0.009) were observed in the low FODMAP group, compared to a significant decrease in polyunsaturated fatty acids (p=0.04) seen in the standard diet group (57). Therefore, while low FODMAPs may improve symptoms of abdominal bloating, gas, and diarrhea/constipation in IBS, avoidance of long-term use may need to be considered (58).

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“SPICY FOODS” RESTRICTION

In addition to gluten, lactose, and short-chain carbohydrates, spicy foods have received attention in IBS. Foods are categorized as “spicy” when they create a hot sensation, produced by capsaicin. The degree of heat is measured by Scoville heat units (SHU) and any pepper marked as ≥1 SHU is regarded as spicy (59). The term “spicy foods” encompasses many ingredients, the most common of which are onion, black and white pepper, chili pepper, garlic, and ginger (60–62). In efforts to make food tastier and more colorful, spices are an integral part of cooking around the world. In fact, chili peppers are considered the most popular spice in Chinese culture (63). Interestingly, it is estimated 5–10% of the adult Asian population is affected by IBS (60), and the impact of spicy foods in contributing to IBS has been questioned (63).

The Asian diet is characterized by high consumption of carbohydrates and fiber, but is less balanced in fat and meat protein. A common flavor in this diet is chili, averaging 2.5–8 g/person daily, a huge increase when compared to European and American counterparts at 0.005–0.5 g/person. The downstream effects of chili are a direct consequence of capsaicin, the active ingredient in chili peppers. Through modulation of gastrointestinal sensation via the effects of transient receptor potential vanilloid-1 (TRPV1) expression on sensory nerve fibers, capsaicin is the reason humans feel a burning, painful sensation in their digestive system after chili ingestion (61). This effect is thought to be enhanced in IBS due to an increased number of colonic TRPV1 receptors, as seen in rectosigmoid biopsies from patients with IBS (64).

The correlation with the generation of IBS symptoms, however, is the subject of mixed reviews. The effects of chili-containing diet on postprandial gastrointestinal symptoms was measured in IBS-D subjects by Gonlachanvit et al., who randomized subjects to either a standard meal, standard meal mixed with 2 g chili, or standard meal with 2 g chili in capsules. By measuring postprandial symptoms every 15 min by a 2-hour visual analogue scale, the authors demonstrated a significant degree of abdominal pain and burning in IBS-D subjects compared to healthy controls (p<0.05) (65).

Although we know short-term capsaicin exposure can aggravate abdominal pain and bloating via TRPV1 expression, chronic intake has been proposed to actually decrease visceral hypersensitivity by TRPV1 desensitization. A preliminary study tested this theory in 42 patients diagnosed with IBS using the Rome II criteria – 17 received 4 pills/day for six weeks containing 150 mg of red pepper powder, while 25 patients unknowingly received placebo pills. Abdominal pain and bloating intensity were scored following the 5-point Likert scale. Interestingly, intra-group comparisons revealed groups receiving red pepper improved their abdominal pain and bloating, with lower mean values (66).

Even though chronic ingestion of red pepper resulted in improved GI symptoms, the question lingers whether the broad category of spicy foods may contribute to symptoms, particularly for foods beyond chilies and therefore not solely limited to capsaicin effects. To answer this question, Esmailzadeh et al. explored the association between IBS and spicy foods in an Iranian population, whose prevalence of IBS is estimated at 1.1–25% of the population, and whose diet included large amounts of turmeric, saffron, and ginger. In a sample of adults working in 50 various healthcare centers across the province of Isfahan, 8691 subjects returned completed questionnaires on dietary habits and symptoms in addition to a modified Persian version of the Rome III questionnaire. Authors assessed dietary habits by measuring meal frequencies, regularity of meals, drinks before meals, and regularity of spicy foods (chili pepper, curry, ginger, cinnamon, and turmeric) during the study week. The authors determined that study subjects consuming spicy foods ≥10 times/week were not only more likely to be young and women, but also had an increased prevalence of IBS. After adjusting for age and gender, a significant association between consumption of spicy foods ≥10 times/week and IBS remained (p<0.001) (60).

As we know consumption of spicy foods is highest among Eastern countries. In the United States, the intake of spicy ingredients has doubled since 1980 - the result of a rising appeal of spicy and hot flavors (59). Despite this, Europeans and Americans still consume spicy foods to a lesser extent than their Eastern counterparts.

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Curcumin Supplement

Herbal remedies are a traditional means of treating a variety of conditions. Recently curcumin, the main active ingredient in turmeric, has demonstrated effectiveness in the management of chronic inflammatory conditions including rheumatoid arthritis, ulcerative colitis (UC), as well as IBS. Turmeric is a curry spice used throughout Asia and in certain regions consumption is as high as 2500 mg/day. Native to the Eastern World, the spice was introduced to Europe in the 13th century by Marco Palo and only recently received attention for its anti-inflammatory properties (67).

First isolated in 1815, curcumin has been noted to affect several inflammatory pathways including down-regulating the activity of COX-2, inhibiting production of tumor necrosis factor (TNF) alpha, and down-regulating mitogen-activating and Janus kinases, in addition to affecting anti-neoplastic cell cycle arrest and induction of apoptotic signals. Today curcumin has been approved by the United States Food and Drug Administration (FDA) as a “Generally Recognized as Safe” (GRAS) supplement, recognizing it as a safe food additive (67).

Curcumin is used in traditional Chinese, Indian, and Western herbal remedies for the management of gastrointestinal symptoms, particularly abdominal pain and bloating (67). More recently, curcumin has been shown to improve bowel symptoms in patients with UC by inhibiting pro-inflammatory cytokines and their signaling pathways, resulting in improvements in Clinical Activity Index (CAI) and endoscopic scores, and reduction in flares (68). This therapeutic potential of curcumin, however, goes beyond inflammatory bowel disease and may extend to functional bowel diseases. As a compound with a vanilloid ring moiety similar to that of capsaicin, curcumin has been shown to competitively inhibit activation of TRPV1 expression on sensory nerve fibers, and therefore modify the body’s response to various stimulants. In contrast to capsaicin, which aggravated abdominal pain and bloating via TRPV1 expression, curcumin had been found to reverse gut hypersensitivity (69).

In a pilot study, Bundy et al. randomized 207 volunteers meeting the Rome II criteria for IBS and assessed the effects of turmeric consumption after 8 weeks. Patients who took one or two tablets of turmeric daily reported reductions in abdominal pain and discomfort of 22 and 25%, respectively. Findings, however, fell short of statistical significance (p=0.071) (70). Portincasa et al. randomized 121 patients with mild to moderate IBS based on the Irritable Bowel Syndrome Symptom Severity Score (IBS-SSS) to receive 30 days of either a combination of curcumin and fennel essential oil (CU-FEO) or placebo. Anethole, the active ingredient in fennel oil seeds, acts as an intestinal smooth muscle relaxant. Patients receiving CU-FEO experienced a significant drop in symptom severity from baseline scores (p<0.001), including abdominal pain (p<0.001), higher complete symptom-free rates at day 30 (p=0.005), and a greater IBS-quality of life score (p=0.003). The use of curcumin led to no serious adverse effects (68). Therefore, curcumin has shown promising effects in mediating IBS symptoms.

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DIETARY FIBER

It has been suggested that IBS is directly related to a lack of dietary fiber, non-digestible carbohydrates intrinsic to plants. Dietary fiber can be separated into soluble fibers (pectins, gums, and mucilages) and insoluble fibers (cellulose, hemicelluloses, and lignins), or characterized based on carbohydrate length (shortchain and long-chain) and fermentability (71). Soluble fibers can form a viscous gel that delays gastric emptying and impedes small intestinal absorption, and is ultimately fermented by bacteria in the large intestine. Fermentation results in production of gas and short-chain fatty acids which increase stool mass, and changes in oro-anal transit time (71). In contrast, insoluble fibers are poorly fermented, influence the viscosity of intestinal contents less, and retain water. These processes increase the volume and bulk of stool, in addition to increasing colon transit time (72).

The proposed mechanisms by which dietary fiber benefits those with IBS are: (1) increased stool bulk through fermentation of byproducts (as with soluble fiber) or accelerated colonic transit by mechanical stimulation (as with insoluble fiber); (2) influences on the microbiota - the production of short-chain fatty acids and the decrease in colonic pH support the growth of bacteria such as lactobacilli and bifidobacteria; and (3) influences on the neuroendocrine system (NES) of the gastrointestinal tract through the release of hormones including serotonin, which impacts visceral sensitivity, and peptide YY (PYY) which increases colonic absorption of water and electrolytes (71). These effects of dietary fiber were first noted by Manning et al., who compared 26 IBS patients receiving either a high or low wheat-fiber diet. After 6 weeks, those receiving the high-fiber diet reported more significant improvements in IBS symptoms (73). In a meta-analysis, 14 randomized controlled trials on dietary fiber in IBS were reviewed. By comparing fiber to placebo, control treatment, or standard management in a total of 906 patients, the authors noted a significant overall benefit in IBS (RR=0.86; 95% CI 0.80–0.94, number needed to treat (NNT)=10; 95% CI 6–33) and when stratifying for type of fiber, authors revealed a more prominent response with soluble fiber versus bran, an insoluble fiber (RR=0.83; 95% CI 0.73–0.94 and RR=0.90; 95% CI 0.79–1.03, respectively) (74).

As IBS patients do not all have the same presentation, but are categorized into subtypes based on the predominant symptom of diarrhea or constipation, Cann et al. assessed which category of fiber is more beneficial. In a double-blind, crossover trial, patients with IBS received either a course of wheat bran or placebo. The use of bran resulted in a significant improvement in constipation, with increases in whole gut transit time (p<0.05) and daily stool weight (p<0.01). Abdominal pain, however, was increased with the use of bran and demonstrated limited efficacy in patients with diarrhea (75). Similarly, in a double-blind placebo-controlled trial of ispaghula husk (a soluble fiber commonly referred to as psyllium) versus placebo in 80 IBS patients, Prior et al. assessed changes in bowel habits, whole gut transit time, and abdominal pain. The study revealed patients felt better overall after receiving ispaghula husk (p<0.02), with particular benefits for relief of constipation (p=0.026) and increased whole gut transit time (p=0.001). In contrast, no improvements in abdominal pain or distention were seen between the two treatment groups (76). Therefore, authors concluded the use of soluble fiber (psyllium/ispaghula husk) and not insoluble fiber (bran) should be considered as a dietary option in management of IBS symptoms, particularly for those with constipation-predominant IBS, but not for the management of abdominal symptoms (5 , 77).

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CONCLUSIONS

Up to two-thirds of IBS patients attribute their abdominal symptoms and changes in bowel habits to their dietary intake, and as a result there is a rising trend towards restricting specific foods in an effort to minimize post-prandial symptoms. A review of the literature on various dietary manipulations, however, yields mixed results (Table 2). This is particularly notable for literature on patients with gluten intolerance, whether due to celiac disease or NCGS. For example, Biesiekierski et al. demonstrated positive symptom correlation with gluten exposure in the form of bread slices and muffins in IBS individuals compared to controls, reporting worsening abdominal pain, bloating, satisfaction with stool consistency, and tiredness within 1 week of gluten exposure. However, following a cross-over trial in which a similar subject population to reduced FODMAP and gluten, the same authors concluded that the carbohydrate components of wheat, fructans, and galacto-oligosaccharides had more pronounced effects on IBS symptoms than gluten itself. Further, questions arise as to whether gluten restricted diets are functioning similarly to a very low carbohydrate diet, and whether symptom response could in fact be a reflection of reduced carbohydrate intake.

Table 2

Table 2

Despite positive evidence supporting lactose restriction in IBS, questions arise as to the validity of applying hydrogen breath testing in the diagnosis of lactose intolerance. Are patients truly lactose intolerant producing hydrogen due to underlying small intestinal bacterial overgrowth? Trials of this diet in IBS using the low FODMAP have produced mixed results. When compared to mNICE guidelines in IBS-D, a low FODMAP diet was found to be favorable in reducing abdominal pain, improving stool consistency, frequency, and urgency. Interestingly, low FODMAP diet was not superior to traditional dietary advice, such as reducing excessive fiber, fat intake, and avoiding larger meals. Despite these findings, the low FODMAP diet has gained popularity in IBS treatment, leading to concerns for potential long-term ramifications.

Our review also identified mixed results in the literature on spicy foods, as trials have revealed worsening abdominal pain after isolated capsaicin exposure, even in an Iranian diet containing large amounts of turmeric, saffron, and ginger, whereas another trial found improved symptoms following chronic red pepper exposure.

The latter result suggested that chronic intake of capsaicin could in fact decrease visceral hypersensitivity. Further, turmeric has demonstrated promising effects in improving IBS symptoms, with significant improvements reported when paired with fennel essential oils. Lastly, although dietary fiber appears to play a beneficial role in IBS, the use of soluble fibers (psyllium, ispaghula husk) in constipation-predominant IBS has shown the most promising results. Fiber did not significantly improve abdominal symptoms.

Overall, we have found mixed results regarding various dietary triggers and the impacts of dietary manipulations on GI symptoms. Although there are data to support dietary restrictions in the management of IBS, further and better controlled trials will be required to provide definitive recommendations.

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CONFLICTS OF INTEREST

Guarantor of the article: Mark Pimentel.

Specific author contributions: AK drafted and revised the manuscript. MP reviewed and revised the manuscript. Both AK and MP have approved the final draft submitted.

Financial support: None.

Potential competing interests: Cedars-Sinai has licensing agreements with Valeant Pharmaceuticals International Inc., Commonwealth Laboratories Inc., and Synthetic Biologics Inc. Mark Pimentel is a consultant for Valeant Pharmaceuticals, Commonwealth Laboratories Inc., Synthetic Biologics Inc., Micropharma Inc., and Naia Pharmaceuticals and is on the advisory boards for Valeant Pharmaceuticals and Commonwealth Laboratories. The remaining authors declare that they have no conflicts of interest.

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REFERENCES

1. Canavan C, West J, Card T. The epidemiology of irritable bowel syndrome. Clin Epidemiol. 2014;6:71–80. https://doi.org/10.2147/CLEP.S40245
2. Lovell RM, Ford AC. Global prevalence of and risk factors for irritable bowel syndrome: a meta-analysis. Clin Gastroenterol Hepatol. 2012;10:712–21.e4. https://doi.org/10.1016/j.cgh.2012.02.029
3. Chang L. Updates to the rome criteria for irritable bowel syndrome. Gastroenterol Hepatol. 2017;13:304–6.
4. What’s New for Rome IV – Rome Foundation. https://theromefoundation.org/rome-iv/whats-new-for-rome-iv/. Accessed on 23 November 2017.
5. Lacy BE, Mearin F, Chang L, et al Bowel Disorders. Gastroenterology. 2016;150:1393–07.e5. https://doi.org/10.1053/j.gastro.2016.02.031
6. Kibune Nagasako C, Garcia Montes C, Silva Lorena SL, Mesquita MA. Irritable bowel syndrome subtypes: Clinical and psychological features, body mass index and comorbidities. Rev Esp Enferm Dig. 2016;108:59–64. https://doi.org/10.17235/reed.2015.3979/2015
7. Nanayakkara WS, Skidmore PM, O’Brien L, Wilkinson TJ, Gearry RB. Efficacy of the low FODMAP diet for treating irritable bowel syndrome: the evidence to date. Clin Exp Gastroenterol. 2016;9:131–42. https://doi.org/10.2147/CEG.S86798
8. Villani A-C, Lemire M, Thabane M, et al Genetic risk factors for postinfectious irritable bowel syndrome following a waterborne outbreak of gastroenteritis. Gastroenterology. 2010;138:1502–13. https://doi.org/10.1053/j.gastro.2009.12.049
9. Klem F, Wadhwa A, Prokop LJ, et al Prevalence, risk factors, and outcomes of irritable bowel syndrome after infectious enteritis: a systematic review and meta-analysis. Gastroenterology. 2017;152:1042–54.e1. https://doi.org/10.1053/j.gastro.2016.12.039
10. Occhipinti K, Smith JW. Irritable bowel syndrome: a review and update. Clin Colon Rectal Surg. 2012;25:46–52. https://doi.org/10.1055/s-0032-1301759
11. Drossman DA, Chey WD, Johanson JF, et al Clinical trial: lubiprostone in patients with constipation-associated irritable bowel syndrome–results of two randomized, placebo-controlled studies. Aliment Pharmacol Ther. 2009;29:329–41. https://doi.org/10.1111/j.1365-2036.2008.03881.x
12. Chey WD, Lembo AJ, Lavins BJ, et al Linaclotide for irritable bowel syndrome with constipation: a 26-week, randomized, double-blind, placebo-controlled trial to evaluate efficacy and safety. Am J Gastroenterol. 2012;107:1702–12. https://doi.org/10.1038/ajg.2012.254
13. Pimentel M, Lembo A, Chey WD, et al Rifaximin therapy for patients with irritable bowel syndrome without constipation. N Engl J Med. 2011;364:22–32. https://doi.org/10.1056/NEJMoa1004409
14. Lembo A, Pimentel M, Rao SS, et al Repeat treatment with rifaximin is safe and effective in patients with diarrhea-predominant irritable bowel syndrome. Gastroenterology. 2016;151:1113–21. https://doi.org/10.1053/j.gastro.2016.08.003
15. Lembo AJ, Lacy BE, Zuckerman MJ, et al Eluxadoline for irritable bowel syndrome with diarrhea. N Engl J Med. 2016;374:242–53. https://doi.org/10.1056/NEJMoa1505180
16. Lewis JH. Alosetron for severe diarrhea-predominant irritable bowel syndrome: safety and efficacy in perspective. Expert Rev Gastroenterol Hepatol. 2010;4:13–29. https://doi.org/10.1586/egh.09.72
17. Andresen V, Hollerbach S. Reassessing the benefits and risks of alosetron: what is its place in the treatment of irritable bowel syndrome? Drug Saf. 2004;27:283–92.
18. Gilkin RJ. The spectrum of irritable bowel syndrome: a clinical review. Clin Ther. 2005;27:1696–709. https://doi.org/10.1016/j.clinthera.2005.11.012
19. Böhn L, Störsrud S, Törnblom H, Bengtsson U, Simrén M. Self-reported food-related gastrointestinal symptoms in IBS are common and associated with more severe symptoms and reduced quality of life. Am J Gastroenterol. 2013;108:634–41. https://doi.org/10.1038/ajg.2013.105
20. El-Salhy M, Gundersen D. Diet in irritable bowel syndrome. Nutr J. 2015;14:36 https://doi.org/10.1186/s12937-015-0022-3
21. Leonard MM, Sapone A, Catassi C, Fasano A. Celiac disease and non-celiac gluten sensitivity: a review. JAMA. 2017;318:647–56. https://doi.org/10.1001/jama.2017.9730
22. Makharia A, Catassi C, Makharia GK. The overlap between irritable bowel syndrome and non-celiac gluten sensitivity: a clinical dilemma. Nutrients. 2015;7:10417–26. https://doi.org/10.3390/nu7125541
23. Catassi C, Alaedini A, Bojarski C, et al The overlapping area of non-celiac gluten sensitivity (NCGS) and wheat-sensitive irritable bowel syndrome (IBS): an update. Nutrients. 2017;9:pii: E1268. https://doi.org/10.3390/ nu9111268
24. Giorgio RD, Volta U, Gibson PR. Sensitivity to wheat, gluten and FODMAPs in IBS: facts or fiction? Gut. 2016;65:169–78. https://doi.org/10.1136/gutjnl-2015-309757
25. Biesiekierski JR, Newnham ED, Irving PM, et al Gluten causes gastrointestinal symptoms in subjects without celiac disease: a double-blind randomized placebo-controlled trial. Am J Gastroenterol. 2011;106:508–14. https://doi.org/10.1038/ajg.2010.487. quiz515
26. Vazquez–Roque MI, Camilleri M, Smyrk T, et al A controlled trial of gluten-free diet in patients with irritable bowel syndrome-diarrhea: effects on bowel frequency and intestinal function. Gastroenterology . 2013;144:903–11.e3. https://doi.org/10.1053/j.gastro.2013.01.049
27. Biesiekierski JR, Peters SL, Newnham ED, Rosella O, Muir JG, Gibson PR. No effects of gluten in patients with self-reported non-celiac gluten sensitivity after dietary reduction of fermentable, poorly absorbed, short-chain carbohydrates. Gastroenterology. 2013;145:320–28.e3. https://doi.org/10.1053/j.gastro.2013.04.051
28. Skodje GI, Sarna VK, Minelle IH, et al Fructan, rather than gluten, induces symptoms in patients with self-reported non-celiac gluten sensitivity. Gastroenterology. 2017. https://doi.org/10.1053/j.gastro.2017.10.040
29. Gluten-free diet: What’s allowed, what’s not. Mayo Clinic. http://www.mayoclinic.org/healthy-lifestyle/nutrition-and-healthy-eating/in-depth/gluten-free-diet/art-20048530. Accessed on 14 November 2017.
30. Saturni L, Ferretti G, Bacchetti T. The gluten-free diet: safety and nutritional quality. Nutrients. 2010;2:16–34. https://doi.org/10.3390/ nu20100016
31. Frigolet M-E, Barragán V-ER, González MT. Low-carbohydrate diets: a matter of love or hate. Ann Nutr Metab. 2011;58:320–34. https://doi.org/10.3390/ijerph110202092
32. Paoli A. Ketogenic diet for obesity: friend or foe? Int J Environ Res Public Health. 2014;11:2092–107. https://doi.org/10.3390/ijerph110202092
33. Bueno NB, de Melo ISV, de Oliveira SL, da Rocha Ataide T. Very-low-carbohydrate ketogenic diet v. low-fat diet for long-term weight loss: a meta-analysis of randomised controlled trials. Br J Nutr. 2013;110: 1178–87. https://doi.org/10.1017/S0007114513000548
34. Austin GL, Dalton CB, Hu Y, et al A very low-carbohydrate diet improves symptoms and quality of life in diarrhea-predominant irritable bowel syndrome. Clin Gastroenterol Hepatol. 2009;7:706–08.e1. https://doi.org/10.1016/j.cgh.2009.02.023
35. Goldstein R, Braverman D, Stankiewicz H. Carbohydrate malabsorption and the effect of dietary restriction on symptoms of irritable bowel syndrome and functional bowel complaints. Isr Med Assoc J. 2000;2:583–7.
36. Deng Y, Misselwitz B, Dai N, Fox M. Lactose intolerance in adults: biological mechanism and dietary management. Nutrients. 2015;7:8020–35. https://doi.org/10.3390/nu7095380
37. Misselwitz B, Pohl D, Frühauf H, Fried M, Vavricka SR, Fox M. Lactose malabsorption and intolerance: pathogenesis, diagnosis and treatment. United Eur. Gastroenterol J. 2013;1:151–9. https://doi.org/10.1177/2050640613484463
38. Bhatnagar S, Aggarwal R. Lactose intolerance. BMJ. 2007;334:1331–2. https://doi.org/10.1136/bmj.39252.524375.80
39. Farup PG, Monsbakken KW, Vandvik PO. Lactose malabsorption in a population with irritable bowel syndrome: prevalence and symptoms. A case‐control study. Scand J Gastroenterol. 2004;39:645–9. https://doi.org/10.1080/00365520410005405
40. Zheng X, Chu H, Cong Y, et al Self-reported lactose intolerance in clinic patients with functional gastrointestinal symptoms: prevalence, risk factors, and impact on food choices. Neurogastroenterol Motil. 2015;27:1138–46. https://doi.org/10.1111/nmo.12602
41. Parker TJ, Woolner JT, Prevost AT, Tuffnell Q, Shorthouse M, Hunter JO. Irritable bowel syndrome: is the search for lactose intolerance justified? Eur J Gastroenterol Hepatol. 2001;13:219–25.
42. Vernia P, Ricciardi MR, Frandina C, Bilotta T, Frieri G. Lactose malabsorption and irritable bowel syndrome. Effect of a long-term lactose-free diet. Ital J Gastroenterol. 1995;27:117–21.
43. Böhmer CJ, Tuynman HA. The effect of a lactose-restricted diet in patients with a positive lactose tolerance test, earlier diagnosed as irritable bowel syndrome: a 5-year follow-up study. Eur J Gastroenterol Hepatol. 2001;13:941–4.
44. Levitt M, Wilt T, Shaukat A. Clinical implications of lactose malabsorption versus lactose intolerance. J Clin Gastroenterol. 2013;47:471–80. https://doi.org/10.1097/MCG.0b013e3182889f0f
45. Rezaie A, Buresi M, Lembo A, et al Hydrogen and methane-based breath testing in gastrointestinal disorders: The North American consensus. Am J Gastroenterol. 2017;112:775–84. https://doi.org/10.1038/ajg.2017.46
46. Pimentel M, Kong Y, Park S. Breath testing to evaluate lactose intolerance in irritable bowel syndrome correlates with lactulose testing and may not reflect true lactose malabsorption. Am J Gastroenterol. 2003;98:2700–4. https://doi.org/10.1111/j.1572-0241.2003.08670.x
47. Barrett JS, Gearry RB, Muir JG, et al Dietary poorly absorbed, short-chain carbohydrates increase delivery of water and fermentable substrates to the proximal colon. Aliment Pharmacol Ther. 2010;31:874–82. https://doi.org/10.1111/j.1365-2036.2010.04237.x
48. Eswaran S. (2017) Low FODMAP in 2017: Lessons learned from clinical trials and mechanistic studies. Neurogastroenterol Motil Off J Eur Gastrointest Motil Soc. 2017;29(4). https://doi.org/10.1111/nmo.13055
49. Ong DK, Mitchell SB, Barrett JS, et al Manipulation of dietary short chain carbohydrates alters the pattern of gas production and genesis of symptoms in irritable bowel syndrome. J Gastroenterol Hepatol. 2010;25:1366–73. https://doi.org/10.1111/j.1440-1746.2010.06370.x
50. Barrett JS. How to institute the low-FODMAP diet. J Gastroenterol Hepatol. 2017;32(Suppl 1):8–10. https://doi.org/10.1111/jgh.13686
51. 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. https://doi.org/10.1016/j.cgh.2008.02.058
52. Böhn L, Störsrud S, Liljebo T, et al Diet low in FODMAPs reduces symptoms of irritable bowel syndrome as well as traditional dietary advice: a randomized controlled trial. Gastroenterology. 2015;149:1399–07.e2. https://doi.org/10.1053/j.gastro.2015.07.054
53. Eswaran SL, Chey WD, Han-Markey T, Ball S, Jackson K. A randomized controlled trial comparing the low FODMAP diet vs. modified NICE guidelines in US adults with IBS-D. Am J Gastroenterol. 2016;111: 1824–32. https://doi.org/10.1038/ajg.2016.434
54. Halmos EP. When the low FODMAP diet does not work. J Gastroenterol Hepatol. 32(S1):69–72. https://doi.org/10.1111/jgh.13701
55. Hustoft TN, Hausken T, Ystad SO, et al Effects of varying dietary content of fermentable short-chain carbohydrates on symptoms, fecal microenvironment, and cytokine profiles in patients with irritable bowel syndrome. Neurogastroenterol Motil. 2017;29. https://doi.org/10.1111/nmo.12969
56. Halmos EP, Christophersen CT, Bird AR, Shepherd SJ, Gibson PR, Muir JG. Diets that differ in their FODMAP content alter the colonic luminal microenvironment. Gut. 2015;64:93–100. https://doi.org/10.1136/ gutjnl-2014-307264
57. Farida J, Shah E, Ball S, et al Micronutrient intake changes with the low FODMAP and mNICE Diets. In: World Congress of Gastroenterology; 2017.
58. Eswaran S. Low FODMAP in 2017: Lessons learned from clinical trials and mechanistic studies. Neurogastroenterol Motil. 2017;29. https://doi.org/10.1111/nmo.13055
59. Lillywhite JM, Simonsen JE, Uchanski ME. Spicy pepper consumption and preferences in the United States. HortTechnology. 2013;23: 868–76.
60. Esmaillzadeh A, Keshteli AH, Hajishafiee M, Feizi A, Feinle-Bisset C, Adibi P. Consumption of spicy foods and the prevalence of irritable bowel syndrome. World J Gastroenterol Wjg. 2013;19:6465–71. https://doi.org/10.3748/wjg.v19.i38.6465
61. Gonlachanvit S. Are rice and spicy diet good for functional gastrointestinal disorders? J Neurogastroenterol Motil. 2010;16:131–8. https://doi.org/10.5056/jnm.2010.16.2.131
62. Gutierrez R, Simon SA. Why do people living in hot climates like their food spicy? Temp Multidiscip Biomed J. 2015;3:48–49. https://doi.org/10.1080/23328940.2015.1119616
63. Lv J, Qi L, Yu C, et al Consumption of spicy foods and total and cause specific mortality: population based cohort study. BMJ. 2015;351:h3942 https://doi.org/10.1136/bmj.h3942
64. Akbar A, Yiangou Y, Facer P, Walters JRF, Anand P, Ghosh S. Increased capsaicin receptor TRPV1-expressing sensory fibres in irritable bowel syndrome and their correlation with abdominal pain. Gut. 2008;57: 923–9. https://doi.org/10.1136/gut.2007.138982
65. Gonlachanvit S, Mahayosnond A, Kullavanijaya P. Effects of chili on postprandial gastrointestinal symptoms in diarrhoea predominant irritable bowel syndrome: evidence for capsaicin-sensitive visceral nociception hypersensitivity, Neurogastroenterol Motil J Eur Gastrointest Motil Soc. 2009;21:–, https://doi.org/10.1111/j.1365-2982.2008.01167.x
66. Bortolotti M, Porta S. Effect of red pepper on symptoms of irritable bowel syndrome: preliminary study. Dig Dis Sci. 2011;56:3288–95. https://doi.org/10.1007/s10620-011-1740-9
67. Fadus MC, Lau C, Bikhchandani J, Lynch HT. Curcumin: an age-old anti-inflammatory and anti-neoplastic agent. J Tradit Complement Med. 2017;7:339–46. https://doi.org/10.1016/j.jtcme.2016.08.002
68. Portincasa P, Bonfrate L, Scribano MLL, et al Curcumin and fennel essential oil improve symptoms and quality of life in patients with irritable bowel syndrome. J Gastrointest Liver Dis. 2016;25:151–7.
69. Dulbecco P, Savarino V. Therapeutic potential of curcumin in digestive diseases. World J Gastroenterol Wjg. 2013;19:9256–70. https://doi.org/10.3748/wjg.v19.i48.9256
70. Bundy R, Walker AF, Middleton RW, Booth J. Turmeric extract may improve irritable bowel syndrome symptomology in otherwise healthy adults: a pilot study. J Altern Complement Med. 2004;10:1015–8.https://doi.org/10.1089/acm.2004.10.1015
71. El-Salhy M, Ystad SO, Mazzawi T, Gundersen D. Dietary fiber in irritable bowel syndrome (Review). Int J Mol Med. 2017;40:607–13. https://doi.org/10.3892/ijmm.2017.3072
72. Zuckerman MJ. The role of fiber in the treatment of irritable bowel syndrome: therapeutic recommendations. J Clin Gastroenterol. 2006;40:104–8.
73. Manning AP, Harvey RF, Heaton KW, Uglow P. Wheat fibre and irritable bowel syndrome: a controlled trial. Lancet. 1977;310:417–8. https://doi.org/10.1016/S0140-6736(77)90605-5
74. Moayyedi P, Quigley EMM, Lacy BE, et al The effect of fiber supplementation on irritable bowel syndrome: a systematic review and meta-analysis. Am J Gastroenterol. 2014;109:1367–74. https://doi.org/ 10.1038/ajg.2014.195
75. Cann PA, Read NW, Holdsworth CD. What is the benefit of coarse wheat bran in patients with irritable bowel syndrome? Gut. 1984;25:168–73.
76. Prior A, Whorwell PJ. Double blind study of ispaghula in irritable bowel syndrome. Gut. 1987;28:1510–3.
77. Lacy BE, Weiser K, De Lee R. The treatment of irritable bowel syndrome. Therap Adv Gastroenterol. 2009;2:221–38. https://doi.org/10.1177/1756283X09104794
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