Share this article on:

Is nutrition an aetiological factor for inflammatory bowel disease?

Cashman, Kevin Da,b; Shanahan, Fb

European Journal of Gastroenterology & Hepatology: June 2003 - Volume 15 - Issue 6 - pp 607-613
Review in depth

Inflammatory bowel disease (IBD) is a chronic inflammatory process, the aetiology of which is complex and probably multi-factorial. Nutrition has been proposed to be an important aetiological factor for IBD. The present review critically examines the relationship between components of the diet (such as sugar, fat, fibre, fruit and vegetables, and protein) and IBD, including ulcerative colitis and Crohn's disease. In addition, it investigates the possible role of infant feeding practices in the development of IBD.

aDepartment of Food & Nutritional Sciences, and bDepartment of Medicine, University College, Cork, Ireland.

Correspondence to Prof. Kevin D. Cashman, Department of Food and Nutritional Sciences, University College, Cork, Ireland. Tel: +353 21 490 1317; fax: +353 21 427 0244; e-mail: k.cashman@ucc.ie

Back to Top | Article Outline

Introduction

Crohn's disease (CD) and ulcerative colitis (UC), collectively referred to as inflammatory bowel disease (IBD), are chronic aggressive disorders, which affect approximately 35–55 per 100 000 people in Western Europe [1]. CD and UC are important diseases, increasing in frequency, disabling for many patients, and generating a significant burden in the health care system [2]. The disease normally starts in childhood or youth with a peak between 20 and 30 years of age. Although there are many similarities concerning pathomechanisms and clinical course, the disorders have very distinct features. UC is characterized by inflammation with superficial ulcerations limited to the mucosa of the colon [1]. It normally starts in the rectum and continuously spreads throughout the large intestine. CD, however, is characterized by a discontinuous pattern, potentially affecting the whole gastrointestinal tract [3]. In contrast to UC, the inflammation is transmural with large ulcerations and occasional granuloma [1].

Although the aetiology of IBD is unclear, the pathogenesis of these disorders is better understood, and it is increasingly clear that these diseases represent the outcome of three essential interactive co-factors: genetic susceptibility, environment and host immune response [2] (Fig. 1). The environmental factors could represent both the local microenvironment (enteric microflora), but also, the nutritional environment. The importance of environmental factors is evidenced by the increasing incidences of CD in recent decades and changing incidence of IBD in migrant populations [4], whereas the genetic influence appears to be stable [3]. This article will review much of the research that has evaluated the role of dietary factors in the aetiology of IBD.

Back to Top | Article Outline

Infant feeding practices

There has been considerable interest in a possible role of infant feeding practices in the development of IBD. In particular, there have been 13 reported case–control studies conducted since 1961 (identified through MEDLINE). These studies have been in European, North American and Japanese populations [5–17]. Some studied both UC and CD, others either CD or UC. Three of the nine studies on UC [5,7,16] and three of the nine studies on CD [6,7,11] found that cases were less likely to have breast fed subjects than controls. Furthermore, even in infants that are breast fed, the duration of feeding may be an important consideration. For example, Bergstrand and Hellers [6] reported that, in a case–control study, the mean length of the breast-feeding period was significantly (P < 0.01) shorter among CD patients (4.59 months) compared to controls (5.76 months) (Fig. 2).

Various hypotheses have been offered to explain how breast feeding may confer some degree of protection against IBD: (1) breast feeding may protect infants from gastrointestinal infections in infancy [18–20], presumably due to the many immunoglobulins and antimicrobial peptides present in milk as well as the lessened risk of microbial contamination of human milk compared to infant formula; and (2) breast feeding may stimulate the early development and maturation of the infant gastrointestinal mucosa [21], especially its normal immunological competence [22,23]. This stimulatory effect may be due to the growth factors in human breast milk which act as gastrointestinal tract trophic factors [24]. Alternatively, it may be that breast feeding protects against CD through other means, such as delaying the infant's encounter with cow's milk and its constituents, potential aetiological agents (see below).

On recently reviewing the evidence for a protective effect of breast feeding, Davis [25] suggested that, while there is not enough evidence to conclude that breast feeding is an important determinant for the development of IBD, there is enough to warrant further research. Therefore, there is a need for inclusion of data on infant feeding practices in future aetiological studies.

Back to Top | Article Outline

Cow's milk

The concept of ‘milk allergy’ was introduced in the early part of the 20th century (even as early as 1925 [26]) when it was believed that foods and eating habits were involved in the pathogenesis of IBD [27–31]. However, the concept of ‘milk allergy’ as initially proposed was not based on objective immunological testing and gradually gave way to theories involving malabsorption of, and ‘intolerance’ to, lactose in the 1960s and, more recently, intolerance to the long-chain triacylglycerols and other components of dairy products (see review by Mishkin [32]).

Allergy to milk proteins still remains a possible cause of dairy sensitivity or milk intolerance in a small percentage of IBD patients. Glassman et al. [33] reported that the frequency of symptoms compatible with cow's milk protein sensitivity during infancy was greater (P < 0.03) in UC (20.9%) compared with a control population (2.8%) or children with CD (8.5%). In addition, patients with a history of cow's milk allergy, who subsequently developed UC, did so at an earlier age (6.7 years) compared to those without a history of cow's milk sensitivity (10.6 years, P < 0.02) [33]. This increased prevalence of cow's milk sensitivity during infancy among children and adolescents with IBD may suggest that antigenic stimuli at an early age play a role in development of colitis at a later age.

There are conflicting data regarding the serum levels of specific antibodies to cow's milk proteins in reported cases of UC and CD [8,11,12,34–40]. This discrepancy, in part, may be due to different techniques used for measuring the antibodies [41]. Mishkin [32] has suggested that the only recognized value of the studies showing elevated levels of serum antibodies to cow's milk proteins is that they provide evidence that the lack of breast feeding and increased prevalence of cow's milk sensitivity may be risk factors for the later development of IBD.

Use of enzyme linked immunosorbent assay (ELISA) techniques has recognized specific antibody (IgM) isotypes to major milk proteins in both UC and CD, and in CD (but not UC) the antibodies were correlated with disease activity in adults [39]. Lerner and colleagues [42] used ELISA technology to measure serum antibodies to five cow's milk proteins (namely, α-casein, bovine serum albumin (BSA), β-lactoglobulin A and B and α-lactalbumin) in adolescent patients with IBD (56 with CD and 24 with UC) and 20 age matched controls. They found that, in comparison to controls, patients with CD had higher IgG antibodies (against BSA and β-lactoglobulin A and B) and IgA (against α-casein), whereas patients with UC had higher IgA (against α-casein) than controls [42].

There has been considerable attention recently on Mycobacterium avium subspecies paratuberculosis (Map) as a major candidate infectious aetiological agent [43,44]. While studies are in progress to investigate the possibility that Map exists in milk from infected cows and survives pasteurization [45], even assuming Map is an aetiological agent, it would seem unlikely that this route of exposure would have a major bearing on the incidence of CD.

Back to Top | Article Outline

Sugar and refined carbohydrate

In 1976, Martini and Brandes [46] and Miller et al. [47] were the first to report that CD patients consumed an excess amount of sugar and products containing highly refined carbohydrates. Since then, there have been numerous studies which have confirmed the observation of increased sugar consumption (for example, in coffee, tea, and on cereals, and an increased consumption of sweets, pastries and sweetened beverages) in CD patients [47–63]. In fact, some researchers have suggested that the most consistent, distinct dietary association with IBD is the relationship between increased consumption of refined carbohydrates (or added sugar) and CD [55,64]. These results can, of course, be interpreted as a consequence of the disease rather than as a factor in the pathogenesis. This issue of whether the increased sugar intake is a cause or a consequence of the disease has been a matter of some debate [52,65,66]. However, the pattern of increased sugar intake has also been noted in new onset CD, suggesting that this dietary pattern may be related to the development of the disease rather than representing a response to the disease [65]. Two studies have calculated the relative risk of developing CD with a high sugar intake as 3.4 [67] and 4.6 [52], respectively.

The observation of increased sugar intake has also been shown in some [55,58,65,67–70], but not all [71] studies of UC patients. For example, a recent study showed that, compared with healthy controls, the dietary intakes of total carbohydrates and mono- plus disaccharides were significantly increased in patients with recently diagnosed CD (within 6 months of diagnosis) but not in patients with long-standing (>10 years) CD, currently in remission [71] (Table 1).

The findings of a recent large epidemiological study suggest that high consumption of sugar loaded foods (e.g. chocolate, chewing gum and cola drinks) was a risk factor for development of CD or UC, whereas a high intake of citrus fruit reduced disease risk [72]. However, the authors suggested that, while these nutritional factors may be true risk factors for IBD, they may also be just an expression of a ‘modern lifestyle’ also involving other risk factors for the development of IBD [72].

Interestingly, epidemiological studies have failed to find correlations between the rising incidence of IBD and marked change in sugar consumption over the last 50 years (see review by Riordan et al. [73]). Stokes [74] has argued that, because CD is extremely rare in countries such as Saudi Arabia and Morocco despite a large indigenous intake of sugar [75], the consumption of sugar is either a consequence of the disease or that factors in addition to sugar are necessary for its development.

Since the possible role of sugar in the pathogenesis of IBD was postulated, several clinical trials have investigated the therapeutic use of a diet low in refined carbohydrates in CD patients. Several small trials suggested a benefit (see reviews by Husain and Korzenik [65], and Geerling et al. [64]), but larger studies failed to confirm the benefits of such a diet. For example, in a large multi-centre trial, 162 patients were randomized to continue their regular diet (typically high in refined carbohydrates (sugar) and low in unrefined carbohydrates (fibre)) and a further 190 patients were counselled to adhere to a diet high in fibre and low in refined carbohydrate [76]. However, no significant benefits in disease activity were demonstrated. Husain and Korzenik [65] have suggested that, although the conclusions of this study may be accurate, the study design actually tested the use of dietary counselling for patients rather than the effect of a specific diet. However, the dietary compliance of patients was good in both groups as assessed by dietary recall assessment [76]. In another large study [77], remission rates at 1 year in CD patients were identical in the low carbohydrate group compared with the placebo group. However, Husain and Korzenik [65] have suggested that the study may have been confounded by the fact that only less than 15% of the low carbohydrate group were able to adhere to the recommended diet of less than 84 g of carbohydrates. Therefore, further investigation of this dietary hypothesis may be warranted before it is discarded.

It is clear that clarification of whether high sugar consumption has an aetiological role in IBD has been hampered, in part, by the methodological limitations of many of the studies carried out to date and there is a need for future well-designed studies before this hypothesis can be accepted or rejected.

Back to Top | Article Outline

Dietary fibre, and fruit and vegetables

In one study, bran showed an inverse relationship to the occurrence of CD [60]. However, in several other studies the association between cereal intake and CD has not been confirmed [46,49,54–56,63]. On the other hand, the consumption of dietary fibre, especially the consumption of fibre from fruit, was also found to be negatively associated with the risk of IBD [60,61,67]. Decreased consumption of fruit, fruit juice or vegetables has been reported among CD [51,54,63,68] and UC patients [68]. It is not clear, however, whether the fibre content of the fruit and vegetables is the seemingly protective factor or whether it is one or more of the micronutrient components of these foods. For example, Reif et al. [61] reported that, in addition to a negative association between fruit and vegetable consumption and IBD risk, there was also a reduced risk associated with increased consumption of water, potassium (in CD patients only), magnesium and vitamin C. Furthermore, the finding that fibre and/or fruit and vegetable intake is lower in IBD patients may represent a response to the disease rather than an aetiological factor. For example, patients may choose or be advised to follow a low fibre diet and consequently avoid fruit and vegetables.

Back to Top | Article Outline

Dietary fat

It has been suggested that chemically processed hydrogenated fats, such as margarine, may be important in the aetiology of CD [78]. This hypothesis was based on the association between the onset of margarine consumption and the first reports of granulomatous ileitis, and on similarities in their geographical distribution [64]. In support of this hypothesis, a Japanese study found that the use of margarine showed a significant positive association with risk of UC [13]. A close correlation has also been found between the incidence of CD and the national consumption of margarine [79]. Further evidence for this hypothesis comes from Germany, where a retrospective analysis of diet before the onset of the disease has been performed [80]. However, another epidemiological study has questioned this relationship as well as an effect of margarine consumption on the incidence of IBD [81].

Chuah et al. [82] showed no significant differences in the consumption of dietary oil between Asian IBD patients and controls. However, Geerling et al. [64] recently drew attention to the fact that CD patients in the study by Chuah et al. [82] recycled their cooking oil significantly more often than did controls. Some studies have reported an increased relative risk of CD and UC associated with consumption of ‘fast foods’ (typically high in fat) [58,72], which may have been prepared in chemically modified fat.

In addition to studies which have investigated a relationship between overall fat intake and IBD risk, a number of studies have investigated fat intake (in both qualitative and quantitative terms) as a risk factor for IBD. A recent case–control study of recently diagnosed UC patients found that high intakes of monounsaturated fat (odds ratio (OR), 33.9) and polyunsaturated fat (OR, 5.1) (adjusted for energy intake) were associated with an increased risk to develop UC [83] (Table 2). However, the authors suggest that further investigation is required to establish whether these are true dietary risk factors in the development of UC or rather a reflection of a certain dietary lifestyle [83]. Tragnone et al. [84] studied the dietary habits of 104 patients with IBD just prior to the onset of disease and compared this with the habits of a matched control population in Italy. They reported a lack of difference in fat consumption (qualitative and quantitative) between IBD patients and controls [84]. However, their reported mean daily nutrient consumption was not corrected for energy intake, and this methodological limitation could have biased the results [64]. Reif et al. [61] reported that increased fat consumption (covering animal fat, vegetable fat, saturated as well as unsaturated fat, and cholesterol) in the pre-illness period was found among IBD patients, especially those suffering from UC. Shoda et al. [85] reported that, in their epidemiological study from Japan, increasing incidence of CD (between 1966 and 1985) in their racially homogeneous population was shown to parallel increasing daily intake of animal protein, total fat and animal fat, especially n-6 polyunsaturated fatty acids (PUFAs) relative to n-3 PUFAs. This pattern may influence the disease process by affecting arachidonic acid metabolism, which increases the proinflammatory leukotriene B4 [65]. Although this study is limited by the fact that it was a retrospective correlational-type study, it does provide some explanation as to why the incidence of CD might have increased in what is a genetically stable and homogeneous population. The conclusion regarding the risk imparted by a low n-3 fatty acid intake is supported by the findings of a placebo controlled study using enteric coated, fish oil capsules designed for ileal release, demonstrating a substantial reduction in clinical relapse rate among patients with CD in clinical but not biochemical remission at baseline [86]. However, another double-blind, controlled study showed no benefit to patients with CD from fish oils [77].

Back to Top | Article Outline

Dietary protein

Gee et al. [87] reported an increased mean intake of protein among IBD patients (CD, UC and ulcerative proctitis) compared with control subjects (with other gastrointestinal disorders). On the other hand, Reif et al. [61] failed to find an association between total protein intake and risk of IBD. Tragnone et al. [84] reported that patients with UC, but not CD, tended to have higher intakes of total protein than control individuals, whereas animal protein was related to an increased incidence of CD in a Japanese study [85].

Back to Top | Article Outline

Total caloric intake

In three studies total energy intake was increased in CD patients compared to controls [87–89]. However, this finding may represent a response to the disease rather than an aetiological factor and, thus, the cause-and-effect relationship would need to be clarified.

Back to Top | Article Outline

Conclusion

Although many foods and food components have been suggested to play a role in the cause of IBD, the results from the numerous studies have been equivocal and there are not yet definitive data to support diet as a cause of either CD or UC. However, while it is possible that the dietary factors studied so far are not true risk factors for CD or UC, an alternative possibility is that real differences in dietary intake between patients and controls do exist but remain undetected. Most studies reviewed were subject to methodological limitations [64,73], which could have biased the results. For example, most studies have investigated post-illness diet. This is important as dietary habits, food choice and acceptability may have changed since onset of the illness. It is known that retrospectively recalled information dating from several years before the onset of illness has limited accuracy [90]. In addition, abdominal pain or diarrhoea can affect appetite, but most studies did not report data on disease activity. Further limitations include the lack of representativeness of the control groups (most being hospital controls suffering from some disease or disorder) and lack of information about the magnitude of the increase in disease risk (i.e. generation of relative risk or odds ratio) (for more detailed discussion on these methodological limitations see reviews by Persson et al. [58], Riordan et al. [73] and Geerling et al. [64]).

Finally, despite the lack of conclusive evidence regarding the role of specific dietary components in the pathogenesis of CD or UC, there is emerging evidence that nutritional therapy (including omega-3 fatty acids and other bioactive lipids, and possibly, glutamine) is effective in the treatment of CD (see reviews by Geerling et al. [64] and Stein et al. [91]). Therefore, there is a continuing need to investigate both the aetiological and therapeutic role of nutrition in IBD.

Back to Top | Article Outline

References

1.Schultz M, Rath HC. The possible role of probiotic therapy in inflammatory bowel disease. In: Tannock GW, editor. Probiotics and Prebiotics – Where Are We Going? Norfolk: Caister Academic Press; 2002. pp. 175–237.
2.Shanahan F. Inflammatory bowel disease: immunodiagnostics, immunotherapeutics, and ecotherapeutics. Gastroenterology 2001; 120: 622–635.
3.Young RJ, Vanderhoof JA. Nutrition in pediatric inflammatory bowel disease. Nutrition 2000; 16:78–80.
4.Calkins BM, Mendeloff AI. Epidemiology of inflammatory bowel disease. Epidemiol Rev 1986; 8:60–91.
5.Acheson ED, Truelove SC. Early weaning in the aetiology of ulcerative colitis: a study of feeding in infancy in cases and controls. Br Med J 1961; ii:929–933.
6.Bergstrand O, Hellers G. Breast-feeding during infancy in patients who later develop Crohn's disease. Scand J Gastroenterol 1983; 18: 903–906.
7.Corrao G, Tragnone A, Caprilli R, Trallori G, Papi C, Andreoli A, et al. Risk of inflammatory bowel disease attributable to smoking, oral contraception and breastfeeding in Italy: a nationwide case–control study. Int J Epidemiol 1998; 27:397–404.
8.Dudek B, Spiro HM, Thayer WR. A study of ulcerative colitis and circulating antibodies to milk proteins. Gastroenterology 1965; 49: 544–547.
9.Gilat T, Haccohen D, Lilos P, Langman MJ. Childhood factors in ulcerative colitis and Crohn's disease: an international study. Scand J Gastroenterol 1987; 22:1009–1024.
10.Gruber M, Marshall JR, Zielezney M, Lance P. A case–control study to examine the influence of maternal perinatal behaviours on the incidence of Crohn's disease. Gastroenterol Nurs 1996; 19:53–59.
11.Koletzko S, Sherman P, Corey M, Griffiths A, Smith C. Role of infant feeding practices in the development of Crohn's disease in childhood. Br Med J 1989; 298:1617–1618.
12.Koletzko S, Griffiths A, Corey M, Smith C, Sherman P. Infant feeding practices and ulcerative colitis in childhood. Br Med J 1991; 302: 1580–1581.
13.Kurata JH, Epidemiology Group of the Research Committee of Inflammatory Bowel Disease in Japan. Dietary and other risk factors of ulcerative colitis: a case–control study in Japan. J Clin Gastroenterol 1994; 19:166–171.
14.Rigas A, Rigas B, Glassman M, et al. Breast-feeding and maternal smoking in the etiology of Crohn's disease and ulcerative colitis in childhood. Ann Epidemiol 1993; 3:387–392.
15.Thompson NP, Pounder RE, Wakefield AJ. Perinatal and childhood risk factors for inflammatory bowel disease: a case–control study. Eur J Gastroenterol Hepatol 1995; 7:385–390.
16.Whorwell PJ, Holdstock G, Whorwell GM, et al. Bottle feeding, early gastroenteritis, and inflammatory bowel disease. Br Med J 1979; i:382.
17.Thompson NP, Montgomery SM, Wadsworth ME, Pounder RE, Wakefield AJ. Early determinants of inflammatory bowel disease: use of two national longitudinal birth cohorts. Eur J Gastroenterol Hepatol 2000; 12:25–30.
18.Beaudry M, Dufour R, Marcoux S. Relation between infant feeding and infections during the first six months of life. J Pediatr 1995; 126: 191–197.
19.Duffy LC, Byers TE, Reipenhoff-Talty M, La Scolea LJ, Zielezny M, Ogra PL. The effects of infant feeding on rotavirus-induced gastroenteritis: a prospective study. Am J Public Health 1986; 76:259–263.
20.Howie PW, Forsyth JS, Ogston SA, Clark A, Florey CD. Protective effect of breast feeding against infection. Br Med J 1990; 300:11–16.
21.Bernt KM, Walker WA. Human milk as a carrier of biochemical messages. Acta Paediatr Suppl 1999; 88 (suppl):27–41.
22.Pittard WB. Breast milk immunology. A frontier in infant nutrition. Am J Dis Child 1979; 133:83–87.
23.Pittard WB 3rd, Bill K. Immunoregulation by breast milk cells. Cell Immunol 1979; 42:437–441.
24.Carver JD, Barness LA. Trophic factors for the gastrointestinal tract. Clin Perinatol 1996; 23:265–285.
25.Davis MK. Breastfeeding and chronic disease in childhood and adolescence. Pediatr Clin North Am 2001; 48:125–141.
26.Andresen AFR. Gastrointestinal manifestations of food allergy. Med J Res 1925; 122:171–175.
27.Andresen AFR. Ulcerative colitis – an allergic phenomenon. Am J Dig Dis 1942; 9:91–98.
28.Mackie TT. The medical management of chronic ulcerative colitis. JAMA 1938; 3:2071–2076.
29.Rowe AH. Chronic ulcerative colitis – allergy in its etiology. Ann Intern Med 1942; 17:83–100.
30.Truelove SC. Ulcerative colitis provoked by milk. Br Med J 1961; i: 154–160.
31.Binder HJ, Gryboski JD, Thayer WR Jr, Spiro HM. Intolerance to milk in ulcerative colitis. A preliminary report. Am J Dig Dis 1966; 11:858–864.
32.Mishkin S. Dairy sensitivity, lactose malabsorption, and elimination diets in inflammatory bowel disease. Am J Clin Nutr 1997; 65:564–567.
33.Glassman MS, Newman LJ, Berezin S, Stockbrugger RW, Brummer RJ, Gryboski JD. Cow's milk protein sensitivity during infancy in patients with inflammatory bowel disease. Am J Gastroenterol 1990; 85: 838–840.
34.Lerner A, Rossi TM, Park B, Albini B, Lebenthal E. Serum antibodies to cow's milk proteins in pediatric inflammatory bowel disease: Crohn's disease versus ulcerative colitis. Acta Paediatr Scand 1989; 78: 384–389.
35.Taylor KB, Truelove SC. Circulating antibodies to milk proteins in ulcerative colitis. Br Med J 1961; ii:924–929.
36.Taylor KB, Truelove SC, Wright R. Serologic reactions to gluten and cow's milk proteins in gastrointestinal disease. Gastroenterology 1964; 46:99–108.
37.Jewell DP, Truelove SC. Circulation antibodies to cow's milk proteins in ulcerative colitis. Gut 1972; 13:796–801.
38.Martinez-Resa P, Alvarez-Moreno C, Hermida F, Chordi A. Identification by immunoelectrophoresis of bovine milk proteins. J Dairy Sci 1969; 52:1–7.
39.Knoflach P, Park BH, Cunningham R, Weiser MM, Albini B. Serum antibodies to cow's milk proteins in ulcerative colitis and Crohn's disease. Gastroenterology 1987; 92:479–485.
40.Falchuk KR, Isselbacher KJ. Circulating antibodies to bovine albumin in ulcerative colitis and Crohn's disease. Characterisation of the antibody response. Gastroenterology 1976; 70:5–8.
41.McCaffery TD Jr, Kraft SC, Rothberg RM. The influence of different techniques in characterizing human antibodies to cow's milk proteins. Clin Exp Immunol 1972; 11:225–234.
42.Lerner A, Rossi TM, Park B, Albini B, Lebenthal E. Serum antibodies to cow's milk proteins in pediatric inflammatory bowel disease: Crohn's disease vs. ulcerative colitis. Acta Paediatr Scand 1989; 78:81–86.
43.Hermon-Taylor, Bull TJ, Sheridan JM, Cheng J, Stellakis ML, Sumar N. Causation of Crohn's disease by Mycobacterium avium subspecies paratuberculosis. Can J Gastroenterol 2000; 14:521–539.
44.Hermon-Taylor J, Bull T. Crohn's disease caused by Mycobacterium avium subspecies paratuberculosis: a public health tragedy whose resolution is long overdue J Med Microbiol 2002; 51:3–6.
45.Harris JE, Lammerding AM. Crohn's disease and Mycobacterium avium subspecies paratuberculosis: current issues. J Food Prot 2001; 64: 2103–2110.
46.Martini GA, Brandes JW. Increased consumption of refined carbohydrates in patients with Crohn's disease. Klinische Wochenschrift 1976; 54:367–371.
47.Miller B, Fervers F, Rohbeck R, Strohmeyer G. Sugar consumption in patients with Crohn's disease. Verhandlungen der Deutsche Gesellschaft fur Innere Medizin 1976; 82:922–924.
48.Brauer PM, Gee MI, Grace M, Thomson ABR. Diet of women with Crohn's and other gastrointestinal diseases. J Am Dietetic Assoc 1983; 82:659–664.
49.Graham WB, Torrance B, Taylor TV. Breakfast and dietary aspects of Crohn's disease [Letter]. Br Med J 1978; ii:768.
50.Jarnerot G, Jarnmark I, Nilsson K. Consumption of refined sugar by patients with Crohn's disease, ulcerative colitis or irritable bowel syndrome. Scand J Gastroenterol 1983; 18:999–1002.
51.Kasper H, Sommer H. Dietary fibre and nutrient intake in Crohn's disease. Am J Clin Nutr 1979; 32:1898–1901.
52.Katschinski B, Logan RFA, Edmond M, Langman MJS. Smoking and sugar intake are separate but interactive risk factors in Crohn's disease. Gut 1988; 29:1202–1206.
53.Matsui T, Iida M, Fujishima M, Imai K, Yao T. Increased sugar consumption in Japanese patients with Crohn's disease. Gastroenterol Japonica 1990; 25:271.
54.Mayberry JF, Rhodes J, Newcombe RG. Breakfast and dietary aspects of Crohn's disease. Br Med J 1978; ii:1401.
55.Mayberry JF, Rhodes J, Newcombe RG. Increased sugar consumption in Crohn's disease. Digestion 1980; 20:323–326.
56.Mayberry JF, Rhodes J, Allan R, Newcombe RG, Regan GM, Chamberlain LM, Wragg KG. Diet in Crohn's disease. Two studies of current and previous habits in newly diagnosed patients. Dig Dis Sci 1981; 26: 444–448.
57.Penny WJ, Mayberry JF, Aggett PJ, Gilbert JO, Newcombe RG, Rhodes J. Relationship between trace elements, sugar consumption, and taste in Crohn's disease. Gut 1983; 24:288–292.
58.Persson PG, Ahlbom A, Hellers G. Diet and inflammatory bowel disease: a case control study. Epidemiology 1992; 3:47–52.
59.Porro GB, Panza E. Smoking, sugar and inflammatory bowel disease. Br Med J 1985; 291:971–972.
60.Rawcliffe PM, Truelove SC. Breakfast and Crohn's disease. Br Med J 1978; ii:539–540.
61.Reif S, Klein I, Lubin F, Farbstein M, Hallak A, Gilat T. Pre-illness dietary factors in inflammatory bowel disease. Gut 1997; 40:754–760.
62.Silkoff K, Hallak A, Yegena L, Rozen P, Mayberry JF, Rhodes J, Newcombe RG. Consumption of refined carbohydrates by patients with Crohn's disease in Tel-Aviv-Yafo. Postgraduate Med J 1980; 56: 842–846.
63.Thornton BR, Emmett PM, Heaton KW. Diet and Crohn's disease: characteristics of the pre-illness diet. Br Med J 1979; ii:762–764.
64.Geerling BJ, Stockbrugger RW, Brummer RJ. Nutrition and inflammatory bowel disease: an update. Scand J Gastroenterol 1999; 230:95–105.
65.Husain A, Korzenik JR. Nutritional issues and therapy in inflammatory bowel disease. Semin Gastrointestinal Dis 1998; 9:21–30.
66.Philipsen-Geerling BJ, Brummer RJM. Nutrition in Crohn's disease. Curr Opin Clin Nutr Metab Care 2000; 3:305–309.
67.Panza E, Franceschi S, La Vecchia C. Dietary factors in the aetiology of inflammatory bowel disease. Ital J Gastroenterol 1987; 19:205–209.
68.Panza E, Porro GB. Smoking, sugar, and inflammatory bowel disease. Br Med J 1985; 291:971–972.
69.Thornton BR, Emmett PM, Heaton KW. Diet and ulcerative colitis. Br Med J 1980; ii:293–294.
70.Thornton BR, Emmett PM, Heaton KW. Smoking, sugar and inflammatory bowel disease. Br Med J 1985; 290:1786–1787.
71.Geerling BJ, vHouwelingen AC, Badart-Smook A, Stockbrügger RW, Brummer RJ. Fat intake and fatty acid profile in plasma phospholipids and adipose tissue in patients with Crohn's disease, compared with controls. Am J Gastroenterol 1999; 94:410–417.
72.Russel MGVM, Engels LG, Muris JW, Limonard CB, Volovics A, Brummer RJ, Stockbrügger RW. ‘Modern life’ in the epidemiology of inflammatory bowel disease: a case–control study with special emphasis on nutritional factors. Eur J Gastroenterol Hepatol 1998; 10:243–249.
73.Riordan AM, Ruxton CHS, Hunter JO. A review of associations between Crohn's disease and consumption of sugars. Eur J Clin Nutr 1998; 52:229–238.
74.Stokes MA. Crohn's disease and nutrition. Br J Surg 1992; 79: 391–394.
75.Kirsner JB, Shorter RG. Recent developments in non-specific inflammatory bowel disease. N Engl J Med 1982; 306:837–848.
76.Ritchie JK, Wadsworth J, Lennard-Jones JE, Rogers E. Controlled multicentre therapeutic trial of an unrefined carbohydrate, fibre rich diet in Crohn's disease. Br Med J 1987; 295:517–520.
77.Lorenz-Meyer H, Bauer P, Nicolay C, Schulz B, Purrmann J, Fleig WE, et al. Omega-3 fatty acids and low carbohydrates diet for maintenance of remission in Crohn's disease. Scand J Gastroenterol 1996; 31: 778–785.
78.Guthy E. Morbus Crohn und Nahrungsfette. Hupothese zur Aetiologie der Enteritis regionalis. Deutsche Medizinische Wochenschrift 1982; 107:71–73.
79.Nordenvall B, Brostrom O, Hellers G. Entzündliche Darmkrankheiten und Nahrungsfette. Deutsche Medizinische Wochenschrift 1982; 107: 1900–1901.
80.Guthy E. Ätiologie des Morbus Crohn: was spricht für Fette als mögliche Ursache? Deutsche Medizinische Wochenschrift 1983; 108: 1729–1733.
81.Sonnenberg A. Geographic and temporal variations of sugar and margarine consumption in relation to Crohn's disease. Digestion 1988; 41:161–171.
82.Chuah SY, Jayanthi V, Lee CN, McDonald B, Probert CSJ, Mayberry JF. Dietary fats and inflammatory bowel disease in Asians. Ital J Gastroenterol 1992; 24:386–388.
83.Geerling BJ, Dagnelie PC, Badart-Smook A, Russel MG, Stockbrugger RW, Brummer RJ. Diet as a risk factor for the development of ulcerative colitis. Am J Gastroenterol 2000; 95:1008–1013.
84.Tragnone A, Valpiani D, Miglio F, Elmi G, Bazzocchi G, Pipitone E, Lanfranchi GA. Dietary habits as risk factors for inflammatory bowel disease. Eur J Gastroenterol Hepatol 1995; 7:47–51.
85.Shoda R, Matsueda K, Yamato S, Umeda N. 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's disease in Japan. Am J Clin Nutr 1996; 63:741–745.
86.Belluzzi A, Brignola C, Campieri M, Pera A, Boschi S, Migliolo M. Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med 1996; 334:1557–1560.
87.Gee MI, Grace MGA, Wensel RH, Sherbaniuk RW, Thompson ABR. Nutritional status of gastroenterology outpatients: comparison of inflammatory bowel disease with functional disorders. J Am Dietetic Assoc 1985; 85:1591–1599.
88.Brandes JW, Stenner A, Martini GA. Dietary habits of patients with ulcerative colitis. Zeitschrift fur Gastroenterologie 1979; 12:834–842.
89.Archer LNJ, Harvey RF. Breakfast and Crohn's disease – II. Br Med J 1978; ii:540.
90.McKoewn GE, Sing Yeung KA, Bright-See E. Assessment of past diet in epidemiologic studies. Am J Epidemiol 1986; 124:94–103.
91.Stein RB, Lichtensein GR, Rombeau JL. Nutrition and inflammatory bowel disease. Curr Opin Clin Nutr Metab Care 1999; 2:367–371.

Cited By:

This article has been cited 1 time(s).

Clinical Nurse Specialist
Seeking Control Through the Determination of Diet: A Qualitative Investigation of Women With Irritable Bowel Syndrome and Inflammatory Bowel Disease
JAMIESON, AE; FLETCHER, PC; SCHNEIDER, MA
Clinical Nurse Specialist, 21(3): 152-160.
10.1097/01.NUR.0000270015.97457.9c
PDF (306) | CrossRef
Back to Top | Article Outline
Keywords:

inflammatory bowel disease; nutrition; aetiology

© 2003 Lippincott Williams & Wilkins, Inc.