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. 2021 Jun 22;12(6):2288–2300. doi: 10.1093/advances/nmab069

Index-Based Dietary Patterns and Inflammatory Bowel Disease: A Systematic Review of Observational Studies

Zhenyi Tian 1, Xiaojun Zhuang 2, Min Zhao 3, Shuyu Zhuo 4, Xiaozhi Li 5, Ruiqi Ma 6, Na Li 7, Caiguang Liu 8, Yijun Zhu 9, Ce Tang 10, Rui Feng 11,✉, Minhu Chen 12,✉
PMCID: PMC8634451  PMID: 34157069

ABSTRACT

Diet is one of the most critical factors for inflammatory bowel disease (IBD). A whole dietary pattern should be considered when doing nutrient-based research to preserve the potential for synergism between nutrients. Dietary indices are important tools to evaluate diet quality, and we investigated the associations of it with IBD. Fourteen studies on the relation between index-based dietary patterns and IBD were included. 6 studies showed the relation between index-based dietary patterns and IBD risk, 7 studies explored the dietary indices and progression of IBD, and 1 study investigated the relationship between index and all-cause mortality in IBD patients. These results implied that a high score on the Mediterranean diet was negatively associated with risk and progression of IBD. However, a diet with high inflammatory potential could increase risk and aggravate disease activity in IBD. Dietary scores have the potential to evaluate the association between overall diet quality and risk and progression of IBD. Future randomized controlled trials are required to confirm the effect of the change in dietary score.

This review was registered at www.crd.york.ac.uk/prospero/ as CRD42020220926.

Keywords: inflammatory bowel disease, dietary patterns, dietary index, Mediterranean diet, diet inflammatory index

Statement of Significance: To date, this is the first systematic review to narrate the relation between index-based dietary patterns and the risk and disease activity of patients with inflammatory bowel disease (IBD). It implied that dietary scores have the potential to evaluate the association between overall diet quality and the risk and progression of IBD.

Introduction

Inflammatory bowel disease (IBD) mainly includes Crohn disease (CD) and ulcerative colitis (UC), and its incidence and prevalence are increasing worldwide, especially in developing countries (1). Increasing incidence and the pathogenesis of IBD are closely associated with several environmental factors. As one of the most crucial etiologic factors, diet plays a vital role in the pathogenesis of IBD via an interaction between gut microbiota, host barrier function, and immunity (2). Numerous prospective cohort studies have attempted to highlight the relations between individual food groups or nutrition components and IBD, but they obtained relatively few plausible causal connections owing to dietary complexity (3). Overall, diet is a complex concept consisting of quantity, variety, or combination of different foods and beverages in a diet and the frequency with which they are habitually consumed. Furthermore, the effects of the dietary constituents may be affected by each other. Hence, the relation between a whole dietary pattern, rather than of a single food or nutrient, and IBD should be examined for findings to capture the complexities of diet and the potential for synergism between dietary components. Dietary indices assessing the quality of the whole dietary pattern and allowing more precise diet management are useful tools in preventing and managing certain chronic diseases (4). Therefore, it is necessary to estimate the quality of the whole dietary pattern using dietary indices and evaluate the relation with IBD.

Numerous studies have explored the role of dietary patterns in IBD. A recent review showed that several dietary patterns, including a specific carbohydrate diet, a diet low in fermentable oligosaccharides, disaccharides, monosaccharides, and polyols (low FODMAP diet), a gluten-free diet, an anti-inflammatory diet, and a Mediterranean diet (MED), were beneficial for IBD symptom improvement and mucosal healing (5). The typical dietary patterns that can be derived using principal component analysis, reduced rank regression, and index-based methods mainly include a priori and a posteriori dietary patterns (6, 7). The a priori approach is hypothesis-driven and used to quantify dietary quality according to dietary guidelines or certain types of diets; whereas, the a posteriori approach that defines dietary patterns empirically is based on statistical exploratory methods, such as factor analysis or principal components analysis (4, 6).

With an increasing number of studies exploring the relation between diet and IBD, the relation between IBD and index-based dietary patterns, including the different versions of the Mediterranean diet score (MDS), Healthy Eating Index (HEI), and dietary inflammatory index (DII), is being emphasized. The DII, which can reflect the inflammatory effect of a diet, is likely to play a stimulative role in the initiation and progression of IBD (8–10). The dietary pattern with high MDS might not only reduce the risk of IBD and play an important role in modifying intestinal inflammation (11–13) but also reduce all-cause mortality in patients with CD or UC (14). Thus, studies on the connection between index-based dietary patterns and IBD are necessary to elucidate the role of dietary patterns in IBD.

To date, to our knowledge, there is no systematic review or meta-analysis on the association between index-based dietary patterns and the risk, quality of life, and disease activity of patients with IBD. Consequently, this systematic review aimed to narrate studies investigating the relation between index-based dietary patterns and the risk and progression of IBD.

Methods

Search process

The protocol was registered on the International Prospective Register of Systematic Reviews (PROSPERO) as CRD42020220926. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist was used as a guideline during the review process. A comprehensive search was performed on public databases, including PubMed, Web of Science, Cochrane Library, Scopus, and Embase (last search: 30 October, 2020), with no date or language restrictions. The combination of Medical Subject Headings terms and free-text words were “Inflammatory Bowel disease,” “IBD,” “Crohn's disease,” “CD,” “Ulcerative colitis,” “UC,” “diet,” “dietary pattern,” “diet score,” “healthy eating index,” “HEI,” “alternate healthy eating index,” “a-HEI,” “healthy eating index 2010,” “HEI-2010,” “healthy eating index 2015,” “HEI-2015,” “dietary inflammatory index,” “DII,” “empirical dietary inflammatory pattern (EDIP/EDII),” “Mediterranean diet score,” “MDS,” “MED,” “alternate Mediterranean diet score,” “aMDS,” “adapted Mediterranean diet,” “aMED,” “modified Mediterranean diet,” “mMED,” and “mMDS.”

Eligibility criteria and study selection

1) Articles were selected if the study they reported involved a priori dietary pattern indices, including the HEI, DII, EDIP/EDII, or MDS, rather than a posteriori dietary pattern indices; 2) prospective and retrospective cohort, case-control, and cross-sectional studies were included, whereas all reviews and meta-analyses were excluded from this systematic review, and abstracts from conference proceedings without the full article were also excluded; 3) articles were selected if the study explored the relation between dietary patterns using a dietary index; and 4) the study must involve humans, whereas cellular and animal experiments were excluded.

Data extraction and quality assessment

Two researchers completed the literature search and data extraction. Data related to the patients’ general information, sample size (number of participants), dietary assessments, dietary index, and indicators of disease activity were extracted to assess disease status in the patients, analyze findings (the relation of dietary indices with IBD, ORs, HRs, 95% CIs, correlation coefficients, and P values), and determine confounding variables related to IBD (e.g., age, sex, education, smoking, disease activity, drug use, physical activity).

The Newcastle-Ottawa Scale was used to assess the quality and risk of bias of the included studies. The quality of the articles was evaluated in 3 aspects, including selection, comparability, and outcome. Scores ranged from 0 to 9, and studies with a score ≥6 were considered as high-quality studies.

Results

Study characteristics and quality assessment

The initial search yielded 5645 articles. After excluding systematic reviews and meta-analyses, 17 articles were obtained. These articles underwent full-text review, and 3 studies were eliminated. Finally, 14 original articles were selected for this systematic review. The detailed retrieval process is shown in a flowchart (Figure 1). The selected studies included 1 study which evaluated the relation between HEI-2015 scores and IBD (15); 5 studies that reported the link between the DII, EDIP/EDII, and IBD (8–10, 16, 17); and 8 studies that assessed the association between IBD and different versions of the MDS (11–14, 18–21). The article quality and detailed evaluation are shown in Table 1, and all studies were considered high-quality studies.

FIGURE 1.

FIGURE 1

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Preferred Reporting Items for Systematic Reviews and Meta-Analyses flow diagram summarizing the studies identified during the selection process. DII, dietary inflammatory index; EDIP, empirical dietary inflammatory pattern; HEI, Healthy Eating Index; MDS, Mediterranean diet score.

TABLE 1.

Newcastle-Ottawa Scale of 14 studies in the systematic review

Selection Exposure
Case–control study Definition of cases Representativeness of cases Selection of controls Definition of controls Comparability Assessment of outcome Method of ascertainment Nonresponse rate Total score
Rahmani et al. (15) 1 1 0 1 2 1 1 0 7
Shivappa et al. (9) 1 1 0 1 2 1 1 0 7
Strisciuglio et al. (20) 1 1 1 1 1 1 1 0 7
Mirmiran et al. (16) 1 1 0 0 2 1 1 0 6
Lamers et al. (10) 1 1 0 0 2 1 1 0 6
Papada et al. (12) 1 1 0 0 2 1 1 0 6
Godny et al. (13) 1 1 0 0 2 1 1 0 6
Elmaliklis et al. (18) 1 1 0 1 1 1 1 0 6
Strisciuglio et al. (19) 1 1 1 1 1 1 1 0 7
Selection Outcome
Cohort study Exposed cohort Nonexposed cohort Ascertainment of exposure Outcome of interest Comparability Assessment of outcome Length of follow-up Adequacy of follow-up Total score
Lo et al. (14) 0 1 0 1 2 1 1 1 7
Racine et al. (21) 1 1 0 1 2 1 1 1 8
Khalili et al. (11) 1 1 0 1 2 1 1 1 8
Lo et al. (8) 0 1 0 1 2 1 1 1 7
Vagianos et al. (17) 1 0 1 0 1 1 1 1 6
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The review included 7 case-control studies, 5 cohort studies, and 2 cross-sectional studies, and dietary indices were evaluated in 3868 accurately classified IBD patients (1502 CD patients and 2366 UC patients) and 142 patients with unclassified IBD, irritable bowel syndrome, or gastroesophageal reflux disease. Further, the studies involved different dietary indices, and different food items were included in each index. FFQs were applied to collect the food consumption of participants in 10 of 14 studies. There were some differences in food items among the FFQs, and the time of recollection was not consistent among participants.

Index-based dietary patterns and the risk of IBD

Six studies highlighted the relation between index-based dietary patterns and the risk of IBD (Table 2). Only 1 study examined whether a dietary pattern based on the HEI-2015 was related to the risk of IBD and showed that compared with UC patients in the lowest quartile of the HEI-2015, patients in the highest quartile had a 66% lower OR for UC (OR: 0.34; 95% CI: 0.12, 0.96; P = 0.04) (15). Two studies investigated the relation between the inflammatory potential of diet and the risk of IBD, but the results of the 2 studies were inconsistent. Shivappa et al. (9) found that subjects who consumed a diet with a higher DII score were at increased risk of UC compared with participants who consumed a diet with a lower DII score (OR: 2.58; 95% CI: 1.03, 6.48; P-trend = 0.04). However, a recent and more extensive cohort study exploring the relation between the inflammatory potential of diet and IBD showed that, compared with the lowest quartile, patients in the highest quartile of the cumulative average EDIP score had a 51% higher risk of CD (HR: 1.51; 95% CI: 1.10, 2.07; P-trend = 0.01), but no association with change in EDIP score was found for the risk of UC (all P > 0.05) (8). Although the results of these 2 studies were inconsistent, they suggested that the risk of IBD was possibly linked to the inflammatory potential of diet. The other 3 studies investigated the association between MDS and the risk of IBD, and 1 of the 3 studies involved children and adolescents. Racine et al. (21) indicated that no association was observed between aMED score and either UC (P = 0.41) or CD (P = 0.67). However, the results of another study elaborated that, compared with participants in the lowest category of the mMED score, the multivariable-adjusted HR of CD was 0.42 (95% CI: 0.22, 0.80) for participants with an mMED score of 6–8, and the HR of UC was 1.08 (95% CI: 0.74, 1.58), which suggested that higher mMED score was associated with a lower risk of CD (P-trend = 0.03), but not UC (P-trend = 0.61) (11). Whereas, a study that discussed the effect of environmental factors in pediatric patients with IBD by Strisciuglio et al. (20) showed that low MDS was significantly associated with UC (OR: 2.3; 95% CI: 1.2, 4.5; P = 0.01).

TABLE 2.

Characteristics of studies investigating the MDS, HEI, or DII, and IBD risk1

Authors, country Study Sample size Dietary assessment Dietary index Findings Covariates included in model
Rahmani et al. (15), Iran A case–control study 58 UC cases (adult) and 123 healthy controls (20–80 y); patients with recently diagnosed (<6 mo) UC FFQ (168 items); average monthly intake HEI-2015 scores Participants who were in the highest quartile of the HEI-2015 had a 66% lower OR of UC than the lowest quartile (OR: 0.34; 95% CI: 0.12, 0.96; P = 0.04) Age, gender, weight, consumption of antibiotics, NSAID consumption, smoking, education, Helicobacter pylori status, and oral contraceptive drug (for women)
Shivappa et al. (9), Iran A case–control study 62 UC cases (adult) and 124 controls hospitalized for acute nonneoplastic diseases (20–80 y); patients newly diagnosed (<6 mo) with UC FFQ (168 items); 1 y prior DII scores (27 food parameters were used) Subjects in the highest quartile were at 158% higher odds of having UC than subjects in the lowest quartile (OR: 2.58; 95% CI: 1.03, 6.48; P = 0.04) Age, energy, sex, education, BMI, family history of IBD, appendectomy, smoking, H. pylori infection, NSAID use
Lo et al. (14), USA The Nurses’ Health Study, Nurses’ Health Study II, Health Professionals Follow-up Study Data from 208,834 people (328 CD and 428 UC) in the Nurses’ Health Study (1984–2014), Nurses’ Health Study II (1991–2015), and Health Professionals Follow-up Study (1986–2012) FFQ; updated every 2–4 y EDIP score (18 food groups were used) Compared with participants in the lowest quartile of cumulative average EDIP score, those in the highest quartile had 51% higher risk of CD (HR: 1.51; 95% CI: 1.10, 2.07; P = 0.01); compared with participants with persistently low EDIP scores at both time points, those who changed to a proinflammatory diet 8 y after baseline had a 2-fold increase in the risk of incident CD (HR: 2.05; 95% CI: 1.10, 3.79). No association with change in EDIP score was found for the risk of UC (all P > 0.05) Race, smoking, BMI, physical activity, regular NSAID use, oral contraceptive pill, and hormonal replacement therapy
Racine et al. (21), Europe European Prospective Investigation into Cancer study 366,351 healthy participants (20–80 y old); a total of 256 participants developed incident UC and 117 incident CD Country-specific validated FFQs (200 food items); the past 12 mo aMED score (9 components were used) There were no associations between quintiles of the aMED score and either UC (P = 0.41) or CD (P = 0.67) Daily energy intake, BMI, smoking status
Strisciuglio et al. (20), Italy A case–control study 264 IBD cases and 203 controls; ages between 1 and 18 y A dietician performed a separate validated questionnaire KIDMED (≤3: low adherence; 4–7: medium adherence; ≥8: high adherence) A low adherence to Mediterranean diet was significantly associated with UC (OR: 2.3; 95% CI: 1.2, 4.5; P = 0.01) No
Khalili et al. (11), Sweden The Cohort of Swedish Men and Swedish Mammography Cohort 83,147 participants (adult); 164 incident cases of CD and 395 incident cases of UC FFQ (96 items); the previous year mMED score Higher mMED score was associated with a lower risk of CD (P = 0.03) but not UC (P = 0.61). Compared with participants in the lowest category of mMED score, there was a statistically significant lower risk of CD (HR: 0.42; 95% CI: 0.22, 0.80; P = 0.03) but not UC (HR: 1.08; 95% CI: 0.74, 1.58; P = 0.61) Cohort (sex), age, education, BMI, smoking, and total caloric intake
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OR and HR estimates for studies were calculated for IBD risk, comparing the highest diet score group with the lowest diet score group in the respective study. aMED, adapted Mediterranean diet; CD, Crohn disease; DII, dietary inflammatory index; EDIP, empirical dietary inflammatory pattern; HEI, Healthy Eating Index; H. pylori, Helicobacter pylori; IBD, inflammatory bowel disease; KIDMED, Mediterranean Diet Quality Index in children and adolescents; mMED, modified Mediterranean diet; NSAID, nonsteroidal anti-inflammatory drug; UC, ulcerative colitis.

Index-based dietary patterns and IBD progression

Seven studies discussed the connection between index-based dietary patterns and disease activity in IBD patients through analyzing the links between diet indices and various disease activity indices. Three studies demonstrated the relation between MDS and IBD progression, as shown in Table 3 . MDS was inversely associated with the OR for elevated fecal calprotectin (OR: 0.74; 95% CI: 0.56, 0.99; P < 0.05) in UC patients after pouch surgery, and patients with high MDS were less likely to develop pouchitis (26% compared with 45.4%, P = 0.17) (13). There was a significant negative correlation of MDS with the Harvey Bradshaw Index (r = −0.400, P < 0.001) and C-reactive protein concentrations (r = −0.268, P = 0.027), as well as a positive relation with the Inflammatory Bowel Disease Questionnaire (r = 0.291, P = 0.008), and the correlations between them remained statistically significant after adjusting for some factors in the regression models (12). Strisciuglio et al. (19) also observed that IBD patients with low fecal calprotectin concentrations showed a significantly higher mean Mediterranean Diet Quality Index in children and adolescents (KIDMED score) (5.82 ± 2.35 compared with 4.85 ± 2.16; P = 0.027), but no significant difference was detected in other parameters of inflammation. A case–control study that investigated the effect of functional foods in IBD and several other gastrointestinal diseases reported that an increase in MDS might be protective against gastrointestinal disease development (OR: 0.70; 95% CI: 0.56, 0.88) (18). Furthermore, the disease status of IBD might also be correlated with the inflammation index of diet. In a recent study, CD disease activity scores were positively associated with the DII (β = 11.86; P = 0.008), but no association with UC was reported (10). Mirmiran et al. (16) suggested that the DII and EDIP were not associated with disease severity. However, the result of another research showed that an increased EDII was associated with greater odds of fecal calprotectin (OR: 3.1; 95% CI: 1.02, 9.93; P = 0.04) and a rise in the IBD Symptom Index of 6.7 (95% CI: 1.0, 12.4; P = 0.022), but no relation was found between changes in DII and changes in fecal calprotectin or the IBD Symptom Index (17).

TABLE 3.

Characteristics of studies investigating the MED or DII and the progression of IBD1

Authors, country Study Sample size Dietary assessment Dietary index Activity Index Findings Covariates included in model
Lamers et al. (10), Netherlands A cross-sectional study 329 participants (168 CD, 161 UC); patients aged 18 y or older FFQ (179 items); the previous month DII (28 parameters were used) sCDAI and P-SCCAI CD disease activity score was positively associated with DII (β = 12.96; P = 0.002). After adjustment for some factors, this association remained (β = 11.86; P = 0.008). No significant association was found between UC disease activity scores and the DII (P = 0.307) Age, age at diagnosis, gender, BMI, and education level
Mirmiran et al. (16), Iran A cross-sectional study 143 IBD patients (32 CD and 111 UC, newly diagnosed patients with IBD <6 mo); patients aged ≥18 y FFQ (168 items); the previous year DII (38 food parameters were used) and EDIP (15 food groups were used) CDAI and Mayo score No significant association was observed between DII and disease activity. The risk of having an active disease was higher with higher EDIP scores, but did not reach statistical significance Total energy intake, type of disease, and drug consumption
Vagianos et al. (17), Canada The Manitoba Living with IBD Study 135 participants (89 CD, 46 UC); patients aged ≥18 y FFQ (149 items); 1-y follow-up DII (33 components were used) and EDII (17 components were used) IBDSI and FC Each unit increase in the change in EDII (baseline to follow-up) was associated with greater odds of FC (OR: 3.1; 95% CI: 1.02, 9.93; P = 0.04) and with a rise in IBDSI of 6.7 (95% CI: 1.0, 12.4; P = 0.022; theoretical IBDSI) No
Strisciuglio et al. (19), Italy A cross-sectional study 125 IBD cases, 125 healthy controls (aged <18 y) Food diary record; 3 d KIDMED was based on a test of 16 questions with scores ranging from 0 to 12 PCDAI/PUCAI and FC IBD patients with low values of FC showed a significantly higher KIDMED mean score (5.82 ± 2.35 compared with 4.85 ± 2.16; P = 0.027). There were no significant differences in terms of KIDMED score and other parameters of inflammation No
Papada et al. (12), Greece Observational study 86 adult patients with CD were enrolled (41 active, 45 inactive) An experienced dietitian recorded the 24-h dietary recall intake and assessed the macronutrient and micronutrient composition of the diet with software; the past 6 mo MDS ΗΒΙ and IBDQ There was a significant negative correlation of MDS with HBI (r = −0.400, P < 0.001) and CRP concentrations (r = −0.268, P = 0.027), whereas MDS correlated positively with the IBDQ (r = 0.291, P = 0.008). HBI showed a Age, sex, BMI, smoking, disease duration, disease location, and anti-inflammatory medication
highly significant negative association with MDS (P = 0.005), and IBDQ showed a positive association with MDS (P = 0.03) in regression models
Godny et al. (13), Israel Prospective observational study 153 patients with UC who underwent pouch surgery (≥18 y) FFQ (106 food items) MDS PDAI and FC MDS was associated with lower odds for elevated FC (OR: 0.74; 95% CI: 0.56, 0.99; P < 0.05) in patients with UC after pouch surgery; patients who had high MDS had lower rates of pouchitis than patients with low MDS (26% vs. 45.4%, P = 0.17); improved adherence to the MED by a 1-point increase in MDS was associated with 26% decreased odds for elevated FC Age, gender, origin (Ashkenazi/non-Ashkenazi/mixed/other), pouch age, pouch behavior, disease activity, BMI, smoking status
Elmaliklis et al. (18), Greece A case–control study 289 participants: 142 cases (IBD, IBS, and GERD); 147 healthy controls FFQ; 2–3 y before the disease diagnosis or the enrolment MDS No The increase of MED adherence was a protective factor for appearance of gastrointestinal diseases (OR: 0.70; 95% CI: 0.56, 0.88) No
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All ORs represent the OR of the highest quantile compared with the referent, and the lowest quantile was considered as the referent. β and r represent the coefficients of association. CD, Crohn disease; CDAI, Crohn's disease activity index; CRP, C-reactive protein; DII, dietary inflammatory index; EDII/EDIP, empirical dietary inflammatory pattern; FC, fecal calprotectin; GERD, gastroesophageal reflux disease; ΗΒΙ, Harvey Bradshaw Index; IBD, inflammatory bowel disease; IBDQ, Inflammatory Bowel Disease Questionnaire; IBDSI, IBD Symptom Index; IBS, irritable bowel syndrome; KIDMED, Mediterranean Diet Quality Index in children and adolescents; MDS, Mediterranean diet score; MED, Mediterranean diet; PCDAI, pediatric Crohn's disease activity index; PDAI, pouchitis disease activity index; P-SCCAI, patient simple clinical colitis activity index; PUCAI, pediatric ulcerative colitis activity index; sCDAI, short Crohn's disease activity index; UC, ulcerative colitis.

TABLE 4.

Mediterranean diet score was associated with reduced all-cause mortality in patients with CD or UC1

Authors, country Study Sample size Dietary assessment Dietary index Findings Covariates included in model
Lo et al. (14), USA The Nurses’ Health Study, Nurses’ Health Study II, Health Professionals Follow-up Study Data from the Nurses’ Health Study (1986–2014), Nurses’ Health Study II (1991–2015), and Health Professionals Follow-up Study (1986–2014), 83 deaths in 363 patients with CD during 4741 person-years and 80 deaths in 465 patients with UC during 6061 person-years FFQ; updated every 4 y aMED score (9 components were used) An aMED score ≥4 was associated with lower mortality than a score <4 (HR: 0.69; 95% CI: 0.49, 0.98) in IBD patients. CD patients with an aMED score ≥4 had lower mortality risk than those with a score <4 (HR: 0.50; 95% CI: 0.29, 0.87) Race, postdiagnostic smoking status, BMI, physical activity
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1aMED, adapted Mediterranean diet; CD, Crohn disease; IBD, inflammatory bowel disease; UC, ulcerative colitis.

Index-based dietary patterns and all-cause mortality in IBD

Only 1 study assessed the relation between a dietary index and all-cause mortality in IBD patients (Table 4). The study that was conducted by Lo et al. (14) evaluated diet quality with the aMDS. The authors observed that cancer and cardiovascular disease were the leading causes of death in patients with IBD and also indicated that an aMDS ≥4 was associated with lower mortality than a score <4 (HR: 0.69; 95% CI: 0.49, 0.98; P = 0.04) (14).

Discussion

We searched for studies that assessed the relation between different types of index-based diet patterns and IBD, intending to determine the association between the occurrence and progression of IBD and diet indices, such as the MDS, HEI, and DII. From the literature search, we found that the first study on a dietary index and IBD was published in 2016. More literature about it was reported in the years following, which indicated that researchers gradually became more interested in the topic. Nonetheless, studies on the relation between them remained relatively few, and different dietary indices or other versions of the indicator scoring system were adopted in these studies; hence, we could not perform a meta-analysis to intuitively explain the relation between index-based dietary patterns and the risk and progression of IBD. Eight studies referred to different versions of the MDS, and the results suggested that high adherence to an MED might have a preventive effect on IBD. Five studies that explored the relation between the inflammatory potential of diet estimated via the DII or EDIP/EDII and IBD implied that a proinflammatory dietary pattern might elevate the risk of IBD and aggravate the patient's condition. Because there was only 1 study on the connection between IBD and the HEI, the relation between IBD and this index could not be well described. Although there is inadequate evidence to support the finding that index-based dietary patterns were associated with the risk of IBD, these studies’ findings could still provide clues for further studies on the relation between dietary patterns and IBD.

In the early 1960s, the dietary habits of residents in most parts of Greece and southern Italy were defined as the MED pattern (22). This diet pattern was characterized by high consumption of fruits, nuts, vegetables, legumes, nonrefined cereals, fish, and olive oil; moderate consumption of dairy and wine; and low consumption of red meat and processed foods (22). The MED pattern was the broadest-described pattern in the literature, and the first scoring system used to assess its quality was designed by Trichopoulou et al. in 1995 (23, 24). Subsequently, the scoring version was altered repeatedly to evaluate the dietary patterns in various regions (25–29). It was widely believed that high adherence to an MED was closely associated with significantly improved health. For instance, the MED could improve insulin sensitivity and persistent thrombosis and reduce blood lipid and inflammatory marker concentrations (23). Reductions in the incidence of cancer, cardiovascular disease, metabolic disease, Parkinson disease, and Alzheimer disease were also related to greater adherence to an MED (23, 30). Furthermore, the results of various studies indicated that a lower risk of all‐cause mortality was associated with a higher MDS (23). However, there were considerably fewer studies on the relation between MDS and mortality in IBD patients because mortality directly from IBD was rare; cardiovascular diseases and cancer were common causes of death in IBD as in the general population (31), and Lo et al. (14) also observed that they were the leading causes of all-cause mortality in IBD patients. So, an MED pattern with high scores was likely to reduce the incidence and mortality of IBD patients who had cardiovascular diseases and cancer and thereby decrease the overall mortality of IBD.

Although the MED pattern has been widely explored in other diseases, the relation between index-based MED patterns and IBD risk has not been extensively explored. Seven studies investigated the relation between the risk of IBD and MDS, and the earliest study was reported in 2016. The result that improvements in some indicators evaluating the disease activity of IBD were associated with high MDS suggested that the MED pattern with high scores might have a crucial protective impact on onset and progression of IBD, but the conclusion remains to be further verified because of a small number of studies, the inclusion of different versions of the MDS, and the participant recall bias in the studies. A recent study that evaluated the impact of short-term MED on the clinical course of IBD indicated that reduction of disease activity indices and improved quality of life in both CD and UC patients were associated with MED, but the patients’ adherence to MED had not been quantified using any specific MDS method (32). It was also found that improved quality of life of IBD patients and lower C-reactive protein concentrations were related to adherence to the MED in another study (33).

Several underlying mechanisms were possibly related to the MED for the prevention and treatment of IBD. Food components in the MED contain many anti-inflammatory and antioxidant substances, such as micronutrients, minerals, vitamins, omega (ω)-3 fatty acids, and polyphenols (34). Greater adherence to the MED was associated with lower blood concentrations of inflammatory markers, such as C-reactive protein, IL-6, e-selectin, and TNF-α (35–37). Several kinds of polyphenols are involved in the synthesis of prostaglandins via inhibition of enzyme activity and the lipopolysaccharide-mediated upregulation of proinflammatory signaling molecules (34). Some other components, such as ω-3 fatty acids, are capable of regulating the function of immune system cells, which modulate the role of T cells directly or indirectly, as well as affecting proinflammatory mediators and cytokine concentrations (38). High intake of dietary fiber is a feature of the MED, leading to the increased production of SCFAs in the intestinal tract, which has a strong action on immune cell chemotaxis and activity and the release of produced reactive oxygen species and cytokines (38). Besides, the MED plays an essential role in maintaining the balance of gut microbiota. It was established that alteration of the gut microbiota and metabolism was related to the initiation and progression of IBD. High adherence to an MED pattern had a remarkable impact on the gut microbiota and the associated metabolome (39). The higher presence of Faecalibacterium prausnitzii and certain clostridial species and lower counts of Escherichia coli were associated with great adherence to the MED (40). F. prausnitzii, a beneficial microbial species of the Firmicutes phylum which secretes anti-inflammatory metabolites, was decreased in patients with CD, and E. coli was increased and considered a pathobiont in CD (41, 42). These 2 genera have been comprehensively reported as closely related to the occurrence and progression of IBD. In addition, increased concentrations of bacterial metabolites (such as butyrate and propionate) in the feces of IBD patients were associated with adherence to the MED (40). Microbial-derived metabolites, such as bile acids, SCFAs, and tryptophan metabolites, were reportedly involved in the pathogenesis of IBD (43).

Growing evidence has suggested that dietary inflammatory potential plays a vital role in the development of IBD. Regarding the inflammatory potential, the diet was divided into proinflammatory or anti-inflammatory components, and 2 methods including the DII and EDII/EDIP were used to calculate the inflammatory potential of a dietary pattern. Both approaches were different in design and conception, but they were both useful in evaluating the inflammatory potential of whole diets. The DII was developed based on the literature and population-based. Forty-five nutrients deemed to have pro- or anti-inflammatory activity were used to calculate the DII (44). However, the assessment of the EDIP was by the weighted sum of 18 food groups instead of nutrients (44). Higher scores calculated by the DII or EDII/EDIP indicated a stronger proinflammatory potential of the diet, and lower scores showed a weak proinflammatory potential (45). The relation between a proinflammatory diet and some chronic inflammatory diseases has been a concern for researchers in recent years. A narrative review conducted by Phillips et al. (46) demonstrated that a more proinflammatory diet in adults was associated with an increased risk of certain cancers, cardiovascular disease and its associated mortality, adverse mental health, and musculoskeletal disorders. In addition, several studies also found an association between disability in older adults and the DII (47–49). The majority of research has suggested that a special relation exists between index-based proinflammatory diets and colorectal cancer, but only a few studies paid attention to the connection between IBD and proinflammatory dietary patterns evaluated by the DII or EDIP/EDII (50). Two studies showed that dietary patterns with higher DII scores were associated with an increased risk of UC or CD (8, 10). However, studies on the relation between the inflammatory potential of diet and the disease activity of IBD were controversial. Lamers et al. (10) demonstrated that higher DII scores were associated with greater severity of disease in IBD patients, but Mirmiran et al. (16) indicated that the disease activity of IBD patients was not related to the inflammatory potential of diet, whether assessed using the DII or EDIP. Vagianos et al. (17) calculated the inflammatory diet potential of a diet at baseline and 1 y of follow-up using the DII and EDII in IBD patients, and they noted that a proinflammatory diet could aggravate inflammation and/or disease symptoms in IBD patients. Although there was insufficient evidence to clarify the relation between the proinflammatory potential of the diet and the risk and disease activity of IBD, it seemed plausible to believe that the index-based proinflammatory diets were related to IBD. It was reported that a high intake of fats and sugar, which were proinflammatory components, was involved in the development of colitis due to the overgrowth of E. coli (50), and the overall score of the inflammatory potential of the diet would also rise with increased intake of these components. Besides, several studies reported that the Western dietary pattern, which contains greater amounts of proinflammatory nutrients and fewer anti-inflammatory nutrients, was involved in the occurrence and progression of IBD (50, 51). Even though the Western diet was not an a priori pattern, it also indicated that a diet pattern with proinflammatory potential was to an extent associated with the risk of IBD. The mechanism of proinflammatory diet in IBD might be that some components of the diet play a direct or indirect role in the occurrence and progression of IBD via 3 physiological processes, including gut microbiota, the immune system, and the intestinal barrier (52). Therefore, the idea that the inflammatory potential of the diet was probably associated with the occurrence and development of IBD should be confirmed by further large, well-designed cohort studies. The underlying mechanism related to proinflammatory diet and nutrients should also be studied in the future.

The HEI was developed by the USDA to monitor changes in dietary intake over time to effectively measure consumers’ overall quality of diet (53). The HEI-2015 is the latest version of the HEI, and the construct validity, reliability, and criterion validity of the HEI-2015 have been evaluated (54). The HEI consists of 13 components, of which the maximum score of 6 items is 5 points, and the maximum score of the remaining items is 10 points (55). Consequently, the minimum score of the HEI-2015 is 0 points, and the maximum score is 100 points; moreover, the higher the score, the higher the quality of the diet (55). The HEI-2015 has been widely used in assessing dietary quality and in several clinical trials to investigate the relation between dietary quality and chronic diseases, such as cancer and cardiovascular disease. However, to our knowledge, only 1 study has evaluated the association between the HEI and the risk of UC. No study has examined whether the HEI is associated with the disease activity of IBD. Even though the research results suggested that UC was related to the HEI-2015, further studies are necessary to verify this result and explore the relation between the HEI and the risk of CD and IBD progression.

Of the 14 studies, 10 included in this review accounted for appropriate confounders via either statistical adjustment or study design. The majority of studies controlled for age, gender, race, BMI, and smoking status. Few studies also controlled for education, total energy intake, type of disease, drug consumption, Helicobacter pylori status, physical activity, etc. The results of several studies were more statistically significant after controlling for confounders. However, these confounders, such as age, BMI, smoking status, antibiotic use, education level, modern lifestyle, pollution, and physical activity, have been implicated as potential environmental risk factors of individual, familial, community-based, country-based, and regionally based origin and could all contribute to the pathogenesis of IBD (56). Disease activity was also closely related to drug use. Therefore, controlling appropriate confounders is required to explore the relation between diet and IBD accurately when studies are designed.

There were several limitations in this review. We searched public databases extensively with no date or language restrictions and assessed the quality of the included articles in detail. Only the articles of high quality could be included, and dietary data were systematically recorded and calculated. The majority of research also controlled for some confounding factors. Nevertheless, publication bias was still inevitable, and there was relatively high publication bias for the following reasons. 1) Only 14 original articles were selected, and the recruited studied populations were from the United States, Europe, Canada, Israel, and Iran. Considering dietary diversity and heterogeneity in different populations, bias may be unavoidable when there is a lack of data from other populations. 2) Different questionnaires were applied in the included studies, and there were differences in the design of the questionnaires, which may lead to bias when assessing the magnitude or direction of results. The participants’ recall time was also not entirely consistent between the studies, and the data acquisition was based on the self-report of participants who might have only recorded the foods they ate most frequently, introducing recall bias. 3) Substantial heterogeneity would exist because the score range was divided into different intervals in different studies during the statistical analysis. The studies’ heterogeneity also increased because different versions of the scores were used to evaluate 1 dietary pattern. 4) Dietary studies have to rely on a large sample size. Nonsignificant associations between index-based dietary indices and IBD may be common and possibly not be published. 5) False positive or negative results might be possible, because dietary consumption and nutritional status may be altered when people start to feel unwell. Furthermore, there are relatively few studies on the relation between index-based diet patterns and IBD, and variability in the study designs and the population makes it difficult to generalize with more determinacy the results from the present review.

Conclusions

This review indicated that lower overall diet quality, whether assessed by the HEI, MDS, or dietary inflammatory index, was associated with the risk and progression of IBD. Therefore, precise assessment of the quality of diet using dietary indices is extremely necessary in the prevention and management of IBD. Therefore, future research should focus on elucidating the link between index-based dietary patterns and IBD in diverse populations and regions, as well as verify the generalizability of diet indices to better quantify the quality of dietary patterns. In addition, the microbiome and metabolomics should be combined to further explore the mechanism of dietary patterns on the risk of IBD in studies assessing diet quality based on a dietary index.

ACKNOWLEDGEMENTS

The authors’ responsibilities were as follows—ZT and XZ: conceptualized the study and drafted the manuscript; MZ, NL, CL, XL, and RM: collected the data and conducted the data abstraction; CT and SZ: designed the study, and edited the manuscript, with significant revisions contributed by YZ, RF, and MC; and all authors: read and approved the final manuscript.

Notes

Supported by National Natural Science Foundation of China grants 81870384 and 81630018 (to MC) and The Leona M & Harry B Helmsley Charitable Trust grant 2019PG-CD018 (to MC).

Author disclosures: The authors report no conflicts of interest.

ZT and XZ contributed equally to this work.

Abbreviations used: aMDS, alternate Mediterranean diet score; aMED, adapted Mediterranean diet; CD, Crohn disease; DII, dietary inflammatory index; EDIP/EDII, empirical dietary inflammatory pattern; HEI, Healthy Eating Index; IBD, inflammatory bowel disease; MDS, Mediterranean diet score; MED, Mediterranean diet; mMED, modified Mediterranean diet; UC, ulcerative colitis.

Contributor Information

Zhenyi Tian, Department of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Xiaojun Zhuang, Department of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Min Zhao, Department of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Shuyu Zhuo, Department of Nutrition, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Xiaozhi Li, Department of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Ruiqi Ma, Department of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Na Li, Department of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Caiguang Liu, Department of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Yijun Zhu, Institute of Precision Medicine, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Ce Tang, Institute of Precision Medicine, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Rui Feng, Department of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

Minhu Chen, Department of Gastroenterology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.

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