Hostname: page-component-7c8c6479df-fqc5m Total loading time: 0 Render date: 2024-03-27T11:48:22.672Z Has data issue: false hasContentIssue false

Dietary and nutritional considerations for inflammatory bowel disease

Published online by Cambridge University Press:  30 March 2011

Miranda C. E. Lomer*
Affiliation:
Department of Gastroenterology, Guy's and St Thomas' NHS Foundation Trust, London, UK Department of Nutrition and Dietetics, Guy's and St Thomas' NHS Foundation Trust, London, UK Diabetes and Nutritional Sciences Division, King's College London, London, UK
*
Corresponding author: Dr Miranda C. E. Lomer, fax +44 20 7848 4171, email miranda.lomer@kcl.ac.uk
Rights & Permissions [Opens in a new window]

Abstract

Nutritional assessment and dietary advice are fundamental to inflammatory bowel disease (IBD) patient management and all patients should have access to a dietitian. Newly diagnosed patients often think that their pre-illness diet has contributed to the development of their IBD. However, epidemiological evidence to support diet as a risk factor is lacking. How the diet contributes to the gastrointestinal microbiota is interesting, although the role is not yet clearly defined. Nutritional problems in IBD are common. Malnutrition occurs in up to 85% of patients and weight loss affects up to 80% of patients with Crohn's disease and 18–62% of patients with ulcerative colitis. Nutritional deficiencies are prevalent, particularly in relation to anaemia and osteoporosis. Intestinal strictures can be problematic in Crohn's disease and limiting fibrous foods that may cause a mechanical obstruction in the gastrointestinal tract is helpful. Patients often explore dietary exclusion to alleviate symptoms but such changes may be self-directed or inappropriately advised and can lead to further nutritional deficiencies. Some patients experience concurrent functional symptoms (e.g. abdominal bloating, abdominal pain, flatulence and diarrhoea) that can significantly affect quality of life. Recently, a group of poorly absorbed carbohydrates that occur naturally in the diet called fermentable oligo-, di-, mono-saccharides and polyols have been associated with functional symptoms by intestinal bacterial fermentation leading to rapid gas production, and an osmotic effect increasing fluid delivery to the colon. Emerging evidence indicates that a diet low in fermentable oligo-, di-, mono-saccharides and polyols can alleviate functional symptoms in IBD.

Type
Conference on ‘Malnutrition matters’
Copyright
Copyright © The Author 2011

Abbreviations:
CD

Crohn's disease

FODMAP

fermentable oligo-

di-

mono-saccharides and polyols

IBD

inflammatory bowel disease

LOFFLEX

low-fat fibre-limited exclusion

UC

ulcerative colitis

Inflammatory bowel disease (IBD) is characterised by chronic intestinal inflammation with a relapsing and remitting nature. IBD comprises Crohn's disease (CD) and ulcerative colitis (UC). CD may occur anywhere within the gastrointestinal tract, most frequently affecting the ileum, and it is characterised by skip lesions with confluent deep linear ulcers, apthoid ulcers, cobblestoning, granuloma, deep fissures, fistulae, strictures, fat wrapping, and is often rectal sparing(Reference Van Assche, Dignass and Panes1). Clinical features include diarrhoea, abdominal pain, weight loss, malaise, anorexia or fever(Reference Van Assche, Dignass and Panes1). UC is confined to continuous mucosal inflammation usually affecting the rectum and a variable extent of the colon without granuloma(Reference Stange, Travis and Vermeire2). Depending on the extent and severity of disease, symptoms include bloody diarrhoea, rectal bleeding and urgency(Reference Stange, Travis and Vermeire2).

The aetiology of IBD is not fully understood but evidence indicates an immune dysfunction that is influenced by a genetic predisposition, the enteric microflora and environmental triggers(Reference Xavier and Podolsky3, Reference Scaldaferri and Fiocchi4). Age, ethnicity and geographical location influence the rates of IBD with a modern Western lifestyle being positively associated(Reference Chapman-Kiddell, Davies and Gillen5, Reference Jayanthi, Probert and Pinder6). Smoking has a significant role and childhood infections and diet have also been implicated(Reference Molodecky and Kaplan7).

It is important to consider diet in terms of the aetiology of IBD but, due to the nature of the disease, diet and nutrition are also important to health during the disease process in nutritional assessment, addressing nutritional deficiencies, as a potential treatment and also in the management of ongoing symptoms. All of the above require good access to dietetic services although there are inconsistencies in the quality of care that patients receive throughout the health service. This review will focus on all of these dietary and nutritional considerations for patients with IBD.

Does diet cause inflammatory bowel disease?

The gastrointestinal tract and enteric microbiota are in careful equilibrium with respect to immune tolerance but in IBD there is an immune dysfunction(Reference Sartor8). The modern Western diet is often implicated as an environmental factor involved in the aetiology of IBD(Reference Chapman-Kiddell, Davies and Gillen5). Rates of IBD increased dramatically over the latter part of the 20th Century and particularly in developed countries(Reference Karlinger, Gyorke and Mako9). Interestingly, increases in IBD rates have also been observed in countries where the diet is becoming more westernised (e.g. Japan and India) and in ethnic groups who move to a developed country and adopt a westernised diet(Reference Chapman-Kiddell, Davies and Gillen5, Reference Jayanthi, Probert and Pinder6).

There are many challenges when studying diet as an aetiological factor in IBD. Case–control and cohort studies are often biased in their method of recruitment and selection of subjects, dietary assessment methods used and carrying out multiple comparisons(Reference Molodecky, Panaccione and Ghosh10).

Numerous studies have reported a high intake of refined carbohydrate, particularly sugar, being associated with the onset of IBD(Reference Porro and Panza11Reference Tragnone, Valpiani and Miglio15). Recall bias in assessing dietary intake retrospectively is a major limiting factor in these studies, particularly as dietary changes often occur soon after symptoms develop which, in some, may be years before a diagnosis of IBD is confirmed(Reference Molodecky, Panaccione and Ghosh10). Furthermore, these studies cannot demonstrate a causal mechanism in the development of IBD. A higher sugar intake is more likely to occur as a consequence of IBD due to altering the diet to alleviate symptoms. This may coincide with a corresponding decrease in the intake of dietary fibre(Reference Thornton, Emmett and Heaton14).

The immunomodulatory effects of PUFA are of great interest in the aetiology of IBD(Reference Reif, Klein and Lubin12, Reference Gassull16). The n-3 PUFA, e.g. EPA and DHA, have anti-inflammatory properties, whereas the n-6 PUFA (e.g. arachidonic acid) have pro-inflammatory properties. Fish oil supplementation, rich in EPA and DHA, has been associated with a decrease in the production of inflammatory mediators, interferon-γ and PGE2, in CD(Reference Belluzzi, Brignola and Campieri17, Reference Trebble, Stroud and Wootton18). A high proportion of n-6 to n-3 PUFA in the diet has been reported in a Japanese study as possibly contributing to the development of CD(Reference Shoda, Matsueda and Yamato19) and the use of margarine, which is typically high in n-6 PUFA, has been associated with the development of UC(20). The most compelling evidence to suggest that fat has a role in the aetiology of UC began with a European prospective cohort study that indicated a possible increased risk with a high intake of PUFA(Reference Hart, Luben and Olsen21). This was followed up with a nested case–control study from a cohort of 203 193 subjects where an increase in the intake of linoleic acid, an n-6 PUFA, was associated with the onset of UC(Reference Tjonneland, Overvad and Bergmann22). Participants who developed UC (n 126) were age and gender matched to four controls (n 504) and dietary data were compared. Despite the high quality of the study design, the number of incident cases of UC is small and an association still needs to be verified for consistency with further studies.

There is a potential role for dietary protein to be linked to the aetiology of IBD(Reference Jowett, Seal and Pearce23). When undigested sulphur-containing proteins reach the colon, they are available for metabolism by the colonic microflora. The resulting end products may be toxic to the colon, for example, hydrogen sulphide. When hydrogen sulphide is exposed to nitric oxide, which is produced by anaerobic bacteria present in the colon, the barrier function of the colonic mucosa may be lost leading to immune dysregulation in UC. High intakes of animal protein have been reported in a prospective cohort study of 67 581 French women with 77 incident cases of IBD(Reference Jantchou, Morois and Clavel-Chapelon24); however, another European prospective cohort study did not report similar findings(Reference Hart, Luben and Olsen21).

Other dietary factors have also been considered. A deficit in micronutrients may have a contributing role as studies of the pre-illness diet have reported a low consumption of fruit and vegetables(Reference Thornton, Emmett and Heaton14) and an increase in fast food(Reference Persson, Ahlbom and Hellers25). Another hypothesis involved dietary microparticles that are resistant to degradation in the gastrointestinal tract but can bind luminal biomolecules and act as adjuncts potentially stimulating an inflammatory cascade(Reference Lomer, Thompson and Powell26). However, removal of such microparticles from the diet did not facilitate disease remission in CD(Reference Lomer, Grainger and Ede27).

There is little conclusive epidemiological evidence to link diet in the causation of IBD. Perhaps the role of different types of fat warrants further investigation due to their immunological effects. More long-term epidemiological dietary studies are needed to identify what dietary habits and exposures may contribute. In addition, a better understanding of the gastrointestinal microbiota may provide some clues between diet and the aetiology of IBD.

Nutritional considerations during the disease process

The disease process of IBD leads to many nutritional challenges (Table 1) that can occur soon after diagnosis and during periods of remission as well as during relapses. Appetite and energy expenditure changes, possibly due to circulating inflammatory cytokines and malabsorption, affect nutritional status(Reference Bannerman, Davidson and Conway28, Reference Gassull and Cabre29). Appropriate dietary advice soon after diagnosis is an essential component of IBD care(30, Reference Lomer31). However, access to dietetic services is often limited(Reference Gourgey, Whelan and Lomer3234) and patients often seek advice from alternative and potentially less evidence-based sources(Reference Prince, Moose and Whelan35) that can lead to patients following restricted diets that may detrimentally affect their nutritional intake(Reference Lomer, Kodjabashia and Hutchinson36, Reference Vagianos, Bector and McConnell37). Recent UK IBD service standards recommend that all patients with IBD should have access to a dietitian(30) and for a local population of 250 000 an IBD service should have a minimum of 0·5 whole time equivalent of a dietitian dedicated to gastroenterology(30).

Malnutrition is present in up to 85% of patients with IBD and weight loss occurs in up to 80% of patients with CD and 18–62% of patients with UC(Reference Gassull and Cabre29, Reference Geerling, Stockbrugger and Brummer38). Patients with IBD should routinely have their BMI measured. Although a one-off measurement may not be particularly helpful as an indicator of lean body mass or nutritional status, particularly if it is in the healthy range or even indicates overweight or obesity(Reference Vagianos, Bector and McConnell37), if BMI is routinely measured, it helps generate a longer-term assessment of nutritional status. In addition, assessment of muscle function and micronutrient status are useful as these are often poor(Reference Vagianos, Bector and McConnell37, Reference Valentini, Schaper and Buning39). A recent study suggested that BMI and albumin levels are easy measurements to record for nutritional assessment but more detailed IBD-specific nutritional assessment criteria have not yet been developed(Reference Mijac, Jankovic and Jorga40).

Extra intestinal gastrointestinal losses, malabsorption, small-intestinal bacterial overgrowth, ileal resection and high-output stoma or fistulae can lead to Mg and/or Zn deficiency. This is particularly relevant for patients with CD where Mg and Zn deficiency have been reported in 14–33 and 3–5%, respectively(Reference Geerling, Badart-Smook and Stockbrugger41, Reference O'Sullivan and O'Morain42).

Osteoporosis

Patients with IBD have up to a 40% increased risk of fractures compared to the general population(Reference Bernstein, Blanchard and Leslie43, Reference van Staa, Cooper and Brusse44). Osteoporosis is common in IBD occurring in 3–58% and 4–50% of patients with UC and CD, respectively(Reference Tilg, Moschen and Kaser45). Increasing age, weight loss over 10%, BMI <20, malabsorption, poor Ca and vitamin D status, corticosteroid use and inflammation all contribute to the cause of osteoporosis(Reference Lewis and Scott46). Important considerations include reducing the use of corticosteroids and assessing dietary intake of Ca and vitamin D, supplementing as appropriate, particularly as some patients restrict their intake due to avoiding dairy foods. The daily recommendation for Ca intake in IBD is 1000 mg(Reference Lewis and Scott46). When corticosteroids are used for at least 12 weeks, patients should be given Ca and vitamin D supplementation(Reference Dignass, Assche and Lindsay47) although there are arguments to supplement all patients receiving corticosteroids(Reference Lewis and Scott46, Reference Compston48).

Anaemia

Anaemia occurs in up to 67% and 74% of patients with UC and CD, respectively(Reference Vagianos, Bector and McConnell37, Reference Valentini, Schaper and Buning39, Reference Kulnigg and Gasche49). The causes are multi-factorial with Fe deficiency and anaemia of chronic disease being the most common. Poor dietary Fe intakes(Reference Lomer, Kodjabashia and Hutchinson36) through avoidance of Fe-rich foods due to food aversions or intolerances may contribute to ongoing Fe deficiency but they are unlikely to be the only contributing factor to the anaemia in IBD(Reference Gasche, Lomer and Cavill50).

In IBD, inflammation, Fe deficiency and anaemia of chronic disease often co-exist, making assessment of Fe status complex. Guidelines for diagnostic criteria and management have been developed and involve different cut-off levels for measuring Fe stores in the presence and absence of anaemia and inflammation(Reference Gasche, Berstad and Befrits51, Reference Stein, Hartmann and Dignass52). Patients with IBD often develop gastrointestinal side effects to oral Fe and so these may not be helpful. Intravenous Fe may be warranted where supplementation is considered(Reference Gasche, Berstad and Befrits51, Reference Stein, Hartmann and Dignass52).

Anaemia in IBD may also be caused by folate and/or vitamin B12 deficiency resulting from a multitude of causes including increased nutritional requirements, reduced dietary intake, malabsorption or even medication used to treat IBD, particularly sulphasalazine(Reference Yakut, Ustun and Kabacam53). Folate and vitamin B12 deficiency has been reported in up to 54% and 48% of patients with CD and 36% and 5% of patients with UC(Reference O'Sullivan and O'Morain42). Regular monitoring and oral supplementation (folate) or intravenous injection (vitamin B12) may be required.

Diet in active disease

In the 1970s, total bowel rest and intravenous glucose was considered appropriate for patients with active disease but they soon developed protein-energy malnutrition. Parenteral nutrition overcame this issue(Reference Driscoll and Rosenberg54, Reference Ostro, Greenberg and Jeejeebhoy55); however, it is invasive and carries more risks of serious complications and leads to gut atrophy arising from complete bowel rest. More recently, the enteral route has been considered more suitable if it is working and accessible. In children and adolescents, enteral nutrition is used a primary treatment for active CD(Reference Griffiths, Ohlsson and Sherman56, Reference Zachos, Tondeur and Griffiths57). Not only does it induce disease remission but it also improves nutritional status and helps with growth and development. In adults with CD, the evidence for using enteral nutrition to induce disease remission is not so strong and it is less effective than corticosteroids(Reference Griffiths, Ohlsson and Sherman56, Reference Zachos, Tondeur and Griffiths57). In adults, enteral nutrition can be useful as an adjunctive treatment to other therapeutic measurements and particularly where the benefits of nutritional support are warranted(Reference Dignass, Assche and Lindsay47).

Early enteral diets were based on an elemental formula but are often unpalatable due to the synthetic taste from free amino acids providing the source of nitrogen. More palatable peptide and whole protein formulas have been developed and are as efficacious as the elemental formula diets(Reference Zachos, Tondeur and Griffiths57). The nutritional composition of enteral nutrition is an important consideration, particularly because of the immunomodulatory effects of fats. However, various studies have assessed different types of fats in enteral nutrition and to date no studies have identified what type of fat is most helpful(Reference Bamba, Shimoyama and Sasaki58Reference Leiper, Woolner and Mullan61).

Enteral nutrition is usually prescribed from 10 d to 8 weeks. By 10 d there should be a clinical response and patients may even go into disease remission(Reference Giaffer, North and Holdsworth62) but longer studies indicate that mucosal healing does not occur until later on and 8 weeks or more may be required(Reference Fell, Paintin and Arnaud-Battandier63, Reference Yamamoto, Nakahigashi and Umegae64).

Enteral nutrition does not provide a primary therapeutic option in UC but can be used for nutritional support(Reference Gonzalez-Huix, Fernandez-Banares and Esteve-Comas65).

Maintenance of disease remission

In CD, the use of exclusion diets can be useful following a period of enteral nutrition(Reference Riordan, Hunter and Cowan66, Reference Woolner, Parker and Kirby67). One of the most successful exclusion diets is the low-fat fibre-limited exclusion (LOFFLEX) diet and it not only helps maintain disease remission(Reference Woolner, Parker and Kirby67) but it helps to identify potentially problematic foods that are poorly tolerated. There is an initial 2–4-week period where LOFFLEX foods are introduced to provide a nutritionally complete diet as quickly as possible, whereas the enteral diet is reduced and usually discontinued. A slow reintroduction programme then follows introducing a new food every 2–4 d to determine tolerance(Reference Woolner, Parker and Kirby67).

Supplementary enteral nutrition providing 35–50% of energy requirements using either an elemental or polymeric formula has been shown to help in the maintenance of disease remission if provided for up to 12 months(Reference Akobeng and Thomas68).

In UC, patients often consider specific foods induce symptoms and self-restrict their diet(Reference Ballegaard, Bjergstrom and Brondum69). There is no evidence to support enteral nutrition in the maintenance of disease remission in UC.

Stricturing disease

Patients with stricturing disease should be advised to alter the dietary content of fibrous foods to prevent and alleviate obstructive symptoms(Reference Meier and Gassull70). The degree of dietary strictness will be dependent on the nature (inflammatory and/or fibrotic) and extent (tightness and length) of the stricture. Typically high-fibre foods (whole grains, skins and pips in fruit and vegetables, nuts and seeds) and foods that are difficult to mechanically break down (e.g. gristle, skin on meat or fish) are avoided(Reference Lomer, Whayman, Duncan and O'Connor71). In some cases, patients may only be able to manage fluids without developing symptoms while others will manage a much wider variety of foods(Reference Raouf, Hildrey and Daniel72).

Probiotics and prebiotics

There is much interest in the role of the gastrointestinal microbiota and inflammation in IBD. Evidence for the pro-inflammatory and immune-regulatory effects is mounting(Reference Hedin, Whelan and Lindsay73). The potential therapeutic effects of probiotics and prebiotics have thus been investigated.

In patients with pouchitis, a multi-strain probiotic (VSL No. 3) appears to maintain remission(Reference Mimura, Rizzello and Helwig74, Reference Gionchetti, Rizzello and Venturi75) and following pouch surgery help to prevent pouchitis(Reference Gionchetti, Rizzello and Helwig76). For maintenance of UC, a single-strain probiotic Escherichia coli Nissle 1917 is as effective as aminosalicylates(Reference Kruis, Schutz and Fric77Reference Rembacken, Snelling and Hawkey79). Prebiotics have often been assessed in combination with probiotics and therefore it is difficult to determine their isolated effects(Reference Hedin, Whelan and Lindsay73). There is insufficient evidence for the use of probiotics or prebiotics to induce or maintain disease remission in CD(Reference Hedin, Whelan and Lindsay73, Reference Butterworth, Thomas and Akobeng80, Reference Mallon, McKay and Kirk81).

Functional symptoms in inflammatory bowel disease

It is well recognised that patients with IBD experience functional symptoms (e.g. abdominal bloating, abdominal pain, diarrhoea and flatulence) with estimates in the order of 33% and 57% of patients with UC and CD, respectively(Reference Simren, Axelsson and Gillberg82). It can be difficult to distinguish between whether symptoms are functional in nature or due to the ongoing inflammatory process. Functional symptoms can have a huge impact on patients’ quality of life(Reference Simren, Axelsson and Gillberg82). Recent evidence supports a role for fermentable oligo-, di-, mono-saccharides and polyols (FODMAP) to contribute to the ongoing functional symptoms in susceptible individuals(Reference Shepherd, Parker and Muir83). FODMAP are poorly digested short-chain carbohydrates that increase fluid and gas production within the gastrointestinal tract. This process occurs in everyone and, in health, the gas and fluid are excreted without the onset of symptoms. However, in susceptible individuals the gas and fluid increases may lead to abdominal bloating, pain, flatulence, diarrhoea and urgency.

FODMAP have been shown to increase fluid output. In a single-blinded randomised crossover intervention study of a high FODMAP v. a low-FODMAP diet in ten IBD patients with an ileostomy, the low-FODMAP diet led to a significant decrease in daytime fluid output of 19% with P=0·01(Reference Barrett, Gearry and Muir84). In addition, 32% of the FODMAP were recovered in the effluent in the high-FODMAP diet.

In another single-blinded randomised crossover intervention study in healthy volunteers and patients with irritable bowel syndrome assessing gas production, breath hydrogen was significantly higher following a high-FODMAP diet compared to a low-FODMAP diet(Reference Ong, Mitchell and Barrett85). Interestingly, the patients with irritable bowel syndrome also reported an increase in symptoms after following the high-FODMAP diet but not the low-FODMAP diet(Reference Ong, Mitchell and Barrett85).

A retrospective review of patients with IBD treated with a low-FODMAP diet indicates that overall functional symptoms and individual symptoms of abdominal pain, diarrhoea, bloating and wind were significantly better than before starting the diet(Reference Gearry, Irving and Barrett86). Although this is early work and a randomised controlled trial is warranted, FODMAP appear to induce functional gastrointestinal symptoms in susceptible individuals.

A low-FODMAP diet is complex, avoids a wide range of foods(Reference Barrett and Gibson87) and requires longer patient appointments and detailed written information to support the dietary advice(Reference Gibson and Shepherd88). The diet originated in Australia and needs careful adaptation for use outside of Australia to include consideration of locally available fruit, vegetables and grains and local legislation on food labelling where high-FODMAP ingredients may be present in pre-packed foods.

Summary

There still remains no conclusive evidence that diet has a direct effect on the development of IBD. Advances in prospective cohort studies using high-quality dietary assessment methods will help to identify whether diet really does play a role. Nutritional assessment is central to identifying and treating nutritional problems during the disease process and the role of the dietitian cannot be under-estimated. Enteral nutrition continues to be a consideration for the management of active CD, more as an adjunctive treatment rather than a primary therapy. The introduction of a diet low in FODMAP shows some promising early data to improve functional symptoms in IBD. Further prospective work is needed to identify which patients may benefit from this approach.

Acknowledgement

The author declares no conflicts of interest. No funding was received.

References

1.Van Assche, G, Dignass, A, Panes, J et al. (2010) The second European evidence-based consensus on the diagnosis and management of Crohn's disease: Definitions and diagnosis. J Crohns Colitis 4, 7–27.CrossRefGoogle Scholar
2.Stange, EF, Travis, SP, Vermeire, S et al. (2008) European evidence-based consensus on the diagnosis and management of ulcerative colitis: Definitions and diagnosis. J Crohns Colitis 2, 123.Google Scholar
3.Xavier, RJ & Podolsky, DK (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448, 427434.Google Scholar
4.Scaldaferri, F & Fiocchi, C (2007) Inflammatory bowel disease: Progress and current concepts of etiopathogenesis. J Dig Dis 8, 171178.CrossRefGoogle ScholarPubMed
5.Chapman-Kiddell, CA, Davies, PS, Gillen, L et al. . (2010) Role of diet in the development of inflammatory bowel disease. Inflamm Bowel Dis 16, 137151.CrossRefGoogle ScholarPubMed
6.Jayanthi, V, Probert, CS, Pinder, D et al. . (1992) Epidemiology of Crohn's disease in Indian migrants and the indigenous population in Leicestershire. Q J Med 82, 125138.Google ScholarPubMed
7.Molodecky, NA & Kaplan, GG (2010) Environmental risk factors for inflammatory bowel disease. Gastroenterol Hepatol 16, 339346.Google Scholar
8.Sartor, RB (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134, 577594.CrossRefGoogle ScholarPubMed
9.Karlinger, K, Gyorke, T, Mako, E et al. . (2000) The epidemiology and the pathogenesis of inflammatory bowel disease. Eur J Radiol 35, 154167.CrossRefGoogle ScholarPubMed
10.Molodecky, NA, Panaccione, R, Ghosh, S et al. . (2010) Challenges associated with identifying the environmental determinants of the inflammatory bowel diseases. Inflamm Bowel Dis Epublication ahead of print.Google ScholarPubMed
11.Porro, GB & Panza, E (1985) Smoking, sugar, and inflammatory bowel disease. Br Med J 291, 971972.Google Scholar
12.Reif, S, Klein, I, Lubin, F et al. . (1997) Pre-illness dietary factors in inflammatory bowel disease. Gut 40, 754760.Google Scholar
13.Sakamoto, N, Kono, S, Wakai, K et al. (2005) Dietary risk factors for inflammatory bowel disease: A multicenter case-control study in Japan. Inflamm Bowel Dis 11, 154163.Google Scholar
14.Thornton, JR, Emmett, PM & Heaton, KW (1979) Diet and Crohn's disease: Characteristics of the pre-illness diet. Br Med J 2, 762764.Google Scholar
15.Tragnone, A, Valpiani, D, Miglio, F et al. (1995) Dietary habits as risk factors for inflammatory bowel disease. Eur J Gastroenterol Hepatol 7, 4751.Google ScholarPubMed
16.Gassull, MA (2001) Dietary fat intake and inflammatory bowel disease. Curr Gastroenterol Rep 3, 358361.Google Scholar
17.Belluzzi, A, Brignola, C, Campieri, M et al. . (1996) Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med 334, 15571560.Google Scholar
18.Trebble, TM, Stroud, MA, Wootton, SA et al. (2005) High-dose fish oil and antioxidants in Crohn's disease and the response of bone turnover: A randomised controlled trial. Br J Nutr 94, 253261.CrossRefGoogle ScholarPubMed
19.Shoda, R, Matsueda, K, Yamato, S et al. . (1996) Epidemiologic analysis of Crohn disease in Japan: Increased dietary intake of n-6 polyunsaturated fatty acids and animal protein relates to the increased incidence of Crohn disease in Japan. Am J Clin Nutr 63, 741745.CrossRefGoogle Scholar
20.Epidemiological Group of the Research Committee of IBD in Japan (1994) Dietary and other risk factors of ulcerative colitis. A case-control study in Japan. Epidemiology group of the research committee of inflammatory Bowel disease in Japan. J Clin Gastroenterol 19, 166171.Google Scholar
21.Hart, AR, Luben, R, Olsen, A et al. (2008) Diet in the aetiology of ulcerative colitis: A European prospective cohort study. Digestion 77, 5764.Google Scholar
22.Tjonneland, A, Overvad, K, Bergmann, MM et al. (2009) Linoleic acid, a dietary n-6 polyunsaturated fatty acid, and the aetiology of ulcerative colitis: A nested case-control study within a European prospective cohort study. Gut 58, 16061611.Google ScholarPubMed
23.Jowett, SL, Seal, CJ, Pearce, MS et al. (2004) Influence of dietary factors on the clinical course of ulcerative colitis: A prospective cohort study. Gut 53, 14791484.CrossRefGoogle ScholarPubMed
24.Jantchou, P, Morois, S, Clavel-Chapelon, F et al. . (2010) Animal protein intake and risk of inflammatory bowel disease: The E3N prospective study. Am J Gastroenterol 105, 21952201.Google Scholar
25.Persson, PG, Ahlbom, A & Hellers, G (1992) Diet and inflammatory bowel disease: A case-control study. Epidemiology 3, 4752.CrossRefGoogle ScholarPubMed
26.Lomer, MC, Thompson, RP & Powell, JJ (2002) Fine and ultrafine particles of the diet: Influence on the mucosal immune response and association with Crohn's disease. Proc Nutr Soc 61, 123130.CrossRefGoogle ScholarPubMed
27.Lomer, MC, Grainger, SL, Ede, R et al. (2005) Lack of efficacy of a reduced microparticle diet in a multi-centred trial of patients with active Crohn's disease. Eur J Gastroenterol Hepatol 17, 377384.CrossRefGoogle Scholar
28.Bannerman, E, Davidson, I, Conway, C et al. . (2001) Altered subjective appetite parameters in Crohn's disease patients. Clin Nutr 20, 399405.CrossRefGoogle ScholarPubMed
29.Gassull, MA & Cabre, E (2001) Nutrition in inflammatory bowel disease. Curr Opin Clin Nutr Metab Care 4, 561569.Google Scholar
30.IBD Standards Working Group Quality Care: Service standards for the healthcare of people who have inflammatory bowel disease (IBD) 2009. http://www.ibdstandards.org.uk/uploaded_files/IBDstandards.pdf (accessed 6 May 2009).Google Scholar
31.Lomer, MCE (2009) National UK audits in inflammatory bowel disease (IBD) highlight a deficit of dietitians in gastroenterology: A priority for improvement supported by national IBD standards. J Hum Nutr Diet 22, 287289.Google Scholar
32.Gourgey, R, Whelan, K & Lomer, MCE (2009) Dietetic assessment and management of enteral nutrition in patients with Crohn's disease: Current practice in the United Kingdom. J Hum Nutr Diet (In the Press).Google Scholar
33.UK IBD Audit Steering Group IBD audit (2006) National results for the organisation and process of IBD care in the UK 2007. http://www.rcplondon.ac.uk/clinical-standards/ceeu/Current-work/Documents/ceeu_uk_ibd_audit_2006.pdf (accessed 6 May 2009).Google Scholar
34.UK IBD Audit Steering Group IBD audit (2008) National results for the organisation and process of IBD care in the UK (2009). http://www.rcplondon.ac.uk/clinical-standards/ceeu/Current-work/Documents/UK-IBD-Audit-2nd-Round-Full-National-Report-Appendices.pdf (accessed 6 May 2009).Google Scholar
35.Prince, A, Moose, A, Whelan, K et al. . (2010) Patients with Crohn's disease and ulcerative colitis have similar food and nutrition problems and share views on research priorities in inflammatory bowel disease. J Hum Nutr Diet 23, 460461.Google Scholar
36.Lomer, MC, Kodjabashia, K, Hutchinson, C et al. . (2004) Intake of dietary iron is low in patients with Crohn's disease: A case-control study. Br J Nutr 91, 141148.Google Scholar
37.Vagianos, K, Bector, S, McConnell, J et al. . (2007) Nutrition assessment of patients with inflammatory bowel disease. J Parenter Enteral Nutr 31, 311319.CrossRefGoogle ScholarPubMed
38.Geerling, BJ, Stockbrugger, RW & Brummer, RJ (1999) Nutrition and inflammatory bowel disease: An update. Scand J Gastroenterol Suppl 230, 95–105.Google Scholar
39.Valentini, L, Schaper, L, Buning, C et al. (2008) Malnutrition and impaired muscle strength in patients with Crohn's disease and ulcerative colitis in remission. Nutrition 24, 694702.Google Scholar
40.Mijac, DD, Jankovic, GL, Jorga, J et al. . (2010) Nutritional status in patients with active inflammatory bowel disease: Prevalence of malnutrition and methods for routine nutritional assessment. Eur J Intern Med 21, 315319.Google Scholar
41.Geerling, BJ, Badart-Smook, A, Stockbrugger, RW et al. . (1998) Comprehensive nutritional status in patients with long-standing Crohn disease currently in remission. Am J Clin Nutr 67, 919926.CrossRefGoogle ScholarPubMed
42.O'Sullivan, M & O'Morain, C (2006) Nutrition in inflammatory bowel disease. Best Pract Res Clin Gastroenterol 20, 561573.Google Scholar
43.Bernstein, CN, Blanchard, JF, Leslie, W et al. . (2000) The incidence of fracture among patients with inflammatory bowel disease. A population-based cohort study. Ann Intern Med 133, 795799.CrossRefGoogle ScholarPubMed
44.van Staa, TP, Cooper, C, Brusse, LS et al. . (2003) Inflammatory bowel disease and the risk of fracture. Gastroenterology 125, 15911597.CrossRefGoogle ScholarPubMed
45.Tilg, H, Moschen, AR, Kaser, A et al. . (2008) Gut, inflammation and osteoporosis: Basic and clinical concepts. Gut 57, 684694.Google Scholar
46.Lewis, NR & Scott, BB (2007) Guidelines for osteoporosis in inflammatory bowel disease and coeliac disease 2007. http://www.bsg.org.uk/clinical-guidelines/ibd/guidelines-for-osteoporosis-in-inflammatory-bowel-disease-and-coeliac-disease.html (accessed 5 February 2011).Google Scholar
47.Dignass, A, Assche, GV, Lindsay, JO et al. (2010) The second European evidence-based consensus on the diagnosis and management of Crohn's disease: Current management. J Crohns Colitis 4, 2862.Google Scholar
48.Compston, J (2003) Osteoporosis in inflammatory bowel disease. Gut 52, 6364.Google Scholar
49.Kulnigg, S & Gasche, C (2006) Systematic review: Managing anaemia in Crohn's disease. Aliment Pharmacol Ther 24, 15071523.CrossRefGoogle ScholarPubMed
50.Gasche, C, Lomer, MC, Cavill, I et al. . (2004) Iron, anaemia, and inflammatory bowel diseases. Gut 53, 11901197.Google Scholar
51.Gasche, C, Berstad, A, Befrits, R et al. (2007) Guidelines on the diagnosis and management of iron deficiency and anemia in inflammatory bowel diseases. Inflamm Bowel Dis 13, 15451553.Google Scholar
52.Stein, J, Hartmann, F & Dignass, AU (2010) Diagnosis and management of iron deficiency anemia in patients with IBD. Nat Rev Gastroenterol Hepatol 7, 599610.Google Scholar
53.Yakut, M, Ustun, Y, Kabacam, G et al. . (2010) Serum vitamin B12 and folate status in patients with inflammatory bowel diseases. Eur J Intern Med 21, 320323.Google Scholar
54.Driscoll, RH Jr & Rosenberg, IH (1978) Total parenteral nutrition in inflammatory bowel disease. Med Clin North Am 62, 185201.CrossRefGoogle ScholarPubMed
55.Ostro, MJ, Greenberg, GR & Jeejeebhoy, KN (1985) Total parenteral nutrition and complete bowel rest in the management of Crohn's disease. J Parenter Enteral Nutr 9, 280287.Google Scholar
56.Griffiths, AM, Ohlsson, A, Sherman, PM et al. . (1995) Metaanalysis of enteral nutrition as a primary-treatment of active Crohns-disease. Gastroenterology 108, 10561067.Google Scholar
57.Zachos, M, Tondeur, M & Griffiths, AM (2007) Enteral nutritional therapy for induction of remission in Crohn's disease. Cochrane Database Syst Rev 3, CD000542.Google Scholar
58.Bamba, T, Shimoyama, T, Sasaki, M et al. (2003) Dietary fat attenuates the benefits of an elemental diet in active Crohn's disease: A randomized, controlled trial. Eur J Gastroenterol Hepatol 15, 151157.CrossRefGoogle ScholarPubMed
59.Gassull, MA, Fernandez-Banares, F, Cabre, E et al. (2002) Fat composition may be a clue to explain the primary therapeutic effect of enteral nutrition in Crohn's disease: Results of a double blind randomised multicentre European trial. Gut 51, 164168.Google Scholar
60.Gorard, DA (2003) Enteral nutrition in Crohn's disease: Fat in the formula. Eur J Gastroenterol Hepatol 15, 115118.CrossRefGoogle ScholarPubMed
61.Leiper, K, Woolner, J, Mullan, MM et al. (2001) A randomised controlled trial of high versus low long chain triglyceride whole protein feed in active Crohn's disease. Gut 49, 790794.CrossRefGoogle ScholarPubMed
62.Giaffer, MH, North, G & Holdsworth, CD (1990) Controlled trial of polymeric versus elemental diet in treatment of active Crohn's disease. Lancet 335, 816819.CrossRefGoogle ScholarPubMed
63.Fell, JM, Paintin, M, Arnaud-Battandier, F et al. (2000) Mucosal healing and a fall in mucosal pro-inflammatory cytokine mRNA induced by a specific oral polymeric diet in paediatric Crohn's disease. Aliment Pharmacol Ther 14, 281289.CrossRefGoogle Scholar
64.Yamamoto, T, Nakahigashi, M, Umegae, S et al. . (2007) Impact of long-term enteral nutrition on clinical and endoscopic recurrence after resection for Crohn's disease: A prospective, non-randomized, parallel, controlled study. Aliment Pharmacol Ther 25, 6772.Google Scholar
65.Gonzalez-Huix, F, Fernandez-Banares, F, Esteve-Comas, M et al. (1993) Enteral versus parenteral nutrition as adjunct therapy in acute ulcerative colitis. Am J Gastroenterol 88, 227232.Google ScholarPubMed
66.Riordan, AM, Hunter, JO, Cowan, RE et al. (1993) Treatment of active Crohn's disease by exclusion diet: East Anglian multicentre controlled trial. Lancet 342, 11311134.Google Scholar
67.Woolner, JT, Parker, TJ, Kirby, GA et al. . (1998) The development and evaluation of a diet for maintaining remission in Crohn's disease. J Hum Nutr Diet 11, 111.Google Scholar
68.Akobeng, AK & Thomas, AG (2007) Enteral nutrition for maintaenance of remission in Crohn's disease. Cochrane Database Syst Rev 3, CD005984.Google Scholar
69.Ballegaard, M, Bjergstrom, A, Brondum, S et al. . (1997) Self-reported food intolerance in chronic inflammatory bowel disease. Scand J Gastroenterol 32, 569571.Google Scholar
70.Meier, R & Gassull, M (2004) Consensus recommendations on the effects and benefits of fibre in clinical practice. Clin Nutr Suppl 1, 7380.CrossRefGoogle Scholar
71.Lomer, MCE (2011) Dietary considerations in IBD. In Inflammatory Bowel Disease Nursing, pp. 139159 [Whayman, K, Duncan, J and O'Connor, M.]. Quay Books: London.Google Scholar
72.Raouf, AH, Hildrey, V, Daniel, J et al. (1991) Enteral feeding as sole treatment for Crohns-disease – controlled trial of whole protein upsilon-amino acid based feed and a case-study of dietary challenge. Gut 32, 702707.CrossRefGoogle Scholar
73.Hedin, C, Whelan, K & Lindsay, JO (2007) Evidence for the use of probiotics and prebiotics in inflammatory bowel disease: A review of clinical trials. Proc Nutr Soc 66, 307315.Google Scholar
74.Mimura, T, Rizzello, F, Helwig, U et al. (2004) Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut 53, 108114.CrossRefGoogle ScholarPubMed
75.Gionchetti, P, Rizzello, F, Venturi, A et al. (2000) Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: A double-blind, placebo-controlled trial. Gastroenterology 119, 305309.Google Scholar
76.Gionchetti, P, Rizzello, F, Helwig, U et al. (2003) Prophylaxis of pouchitis onset with probiotic therapy: A double-blind, placebo-controlled trial. Gastroenterology 124, 12021209.Google Scholar
77.Kruis, W, Schutz, E, Fric, P et al. . (1997) Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 11, 853858.CrossRefGoogle ScholarPubMed
78.Kruis, W, Fric, P, Pokrotnieks, J et al. (2004) Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53, 16171623.CrossRefGoogle ScholarPubMed
79.Rembacken, BJ, Snelling, AM, Hawkey, PM et al. . (1999) Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: A randomised trial. Lancet 354, 635639.CrossRefGoogle ScholarPubMed
80.Butterworth, AD, Thomas, AG & Akobeng, AK (2008) Probiotics for induction of remission in Crohn's disease. Cochrane Database Syst Rev 3, CD006634.Google Scholar
81.Mallon, P, McKay, D, Kirk, S et al. . (2007) Probiotics for induction of remission in ulcerative colitis. Cochrane Database Syst Rev 4, CD005573.Google Scholar
82.Simren, M, Axelsson, J, Gillberg, R et al. . (2002) Quality of life in inflammatory bowel disease in remission: The impact of IBS-like symptoms and associated psychological factors. Am J Gastroenterol 97, 389396.Google Scholar
83.Shepherd, SJ, Parker, FC, Muir, JG et al. . (2008) Dietary triggers of abdominal symptoms in patients with irritable bowel syndrome: Randomized placebo-controlled evidence. Clin Gastroenterol Hepatol 6, 765771.CrossRefGoogle ScholarPubMed
84.Barrett, JS, Gearry, RB, Muir, JG et al. (2010) Dietary poorly absorbed, short-chain carbohydrates increase delivery of water and fermentable substrates to the proximal colon. Aliment Pharmacol Ther 31, 874882.Google Scholar
85.Ong, DK, Mitchell, SB, Barrett, JS et al. (2010) Manipulation of dietary short chain carbohydrates alters the pattern of gas production and genesis of symptoms in irritable bowel syndrome. J Gastroenterol Hepatol 25, 13661373.Google Scholar
86.Gearry, RB, Irving, PM, Barrett, JS et al. . (2009) Reduction of dietary poorly absorbed short-chain carbohydrates (FODMAPs) improves abdominal symptoms in patients with inflammatory bowel disease. J Crohns Colitis 3, 8–14.Google Scholar
87.Barrett, JS & Gibson, PR (2007) Clinical ramifications of malabsorption of fructose and other short chain carbohydrates. Pract Gastroenterol 53, 5165.Google Scholar
88.Gibson, PR & Shepherd, SJ (2010) Evidence-based dietary management of functional gastrointestinal symptoms: The FODMAP approach. J Gastroenterol Hepatol 25, 252258.CrossRefGoogle ScholarPubMed
89.Krok, KL & Lichtenstein, GR (2003) Nutrition in Crohn disease. Curr Opin Gastroenterol 19, 148153.CrossRefGoogle ScholarPubMed
Figure 0

Table 1. Nutritional challenges in inflammatory bowel disease(29,39,42,71,89)