Background

Ulcerative colitis (UC) is a common type of inflammatory bowel disease (IBD) with increasing prevalence over time1. It is characterized by periods of active disease and remission. In the active phase, the patients experience different symptoms including bloody diarrhea with rectal urgency and tenesmus2. The disease courses and therapies affect the health-related quality of life in UC patients and the disease activity is the most significant factor3,4. Therefore, the primary goals of treatments in these patients are to induce and maintain longstanding clinical and endoscopic remission, reduce the incidence of complications, and improve quality of life5. Based on the disease severity and extent, different induction and maintenance therapies are recommended6. However, most of the UC patients had poor tolerance to the prescribed medications and experienced different side effects that influenced their quality of life7. In addition, broad medical care leads to a significant economic burden in UC treatment8. So, it is important to determine new approaches in the investigation, treatment, and prevention of UC.

For this purpose, different studies have assessed the association between various nutrients, foods, and dietary indices and IBD risk, progression, and management9,10,11,12,13,14,15,16,17. The studies that investigated the effect of diet on the disease course indicated that a plant-based diet, Mediterranean diet, and anti-inflammatory diets were effective in relapse prevention in patients with UC18,19,20. These diets had antioxidant and anti-inflammatory effects that may affect the disease course in patients with IBD. So, it is postulated that other dietary indices with antioxidant and anti-inflammatory effects such as dietary approaches to stop hypertension (DASH) and Mediterranean-DASH Intervention for Neurodegenerative Delay (MIND) also affect the course of disease in patients with IBD. Identical to Mediterranean and DASH diets, the MIND diet highlights the consumption of natural plant-based foods and limits the intake of animal and high saturated fat foods. This pattern is unique in recommending the consumption of berries and green leafy vegetables21. These food items are good sources of different phenolic compounds, fibers, and antioxidant vitamins and minerals22,23,24,25,26. Previous studies showed the promising effect of these components on inflammatory factors12,13,27,28,29. Moreover, consuming these foods together in a diet can have additive and synergistic effects30.

According to the growing evidence on the role of diet in the development and exacerbation of UC, it is important to explore the relationship between adherence to different dietary patterns and disease severity in these patients. Owing to the potential antioxidant and anti-inflammatory effects of the MIND diet score, it is hypothesized that adherence to this dietary pattern may associated with lower odds of severe UC. So, in this cross-sectional study, the association between MIND diet score and disease severity in patients with UC was investigated.

Materials and methods

The present cross-sectional study was conducted in the IBD clinic of Imam Reza Hospital, the central clinic of IBD management in East Azerbaijan, Iran. One hundred fifty-eight patients with UC were enrolled from July 2022 to March 2023.

The sample size for the present study was calculated by Power Analysis & Sample Size (PASS) software using the logistic regression category, and a two-sided type I error of 5% (α = 0.05) and 80% power (PASS 2021, NCSS, LLC. Kaysville, Utah, USA, ncss.com/software/pass). In the previous study31, the association between dietary intake of food groups and relapse in UC was reported and this data was used for calculation.

The inclusion criteria for participation in the present study were age 20–60 years old and being diagnosed at least six months before contribution. The exclusion criteria were having other gastrointestinal problems, tumors, autoimmune diseases, or other disorders that necessitate following special diets.

The present study fulfills the Declaration of Helsinki and was approved by the ethics committee of Tabriz University of Medical Sciences (Ethics code: IR.TBZMED.REC.1403.1021).

General characteristics, diseases related information, and anthropometric assessments

Demographic information, including age (continuous), sex (male/female), and smoking status (current smoker) was obtained using a demographic questionnaire by in-person interview.

The disease-related information including disease duration (continuous), the extension of disease (proctitis, left-side colitis, proctosigmoiditis, and pancolitis), and drug regimen (mesalazine, Azathioprine, prednisolone) was completed by an expert gastroenterologist. Moreover, the disease severity was determined by a skilled gastroenterologist and endoscopist using the Mayo score. This score consists of four subscales including rectum hemorrhage, defection rate, physician’s global assessment, and endoscopic assessment. Each subscale was scored from 0 to 3. The scores were summed up, with a possible score range of 0–12 for total Mayo score. In the present study, we considered a total Mayo score < 6 as an inactive or mild disease severity, and a score ≥ 6 as a moderate or severe UC stage.

The anthropometric measurements including weight and height were measured by an expert dietitian and according to standard protocols and instruments (SECA weight scale), and the body mass index (BMI) was calculated by dividing the weight (kg) by the square of height (meters).

Dietary assessments

A valid 168-item Food Frequency Questionnaire (FFQ)32 was applied to gather the dietary intake of different food items in the past year and completed by a skilled nutritionist. The amount and frequency of each food item were recorded in grams and daily food intakes were analyzed using the Nutritionist IV software (N Squared Computing, California, USA).

The MIND diet score was calculated based on Morris et al.21 and considering the consumption of nine brain-healthy food items (green leafy vegetables, other vegetables, berries, nuts, whole grains, fish, beans, poultry, olive oil), and five brain-unhealthy food items (butter and margarine, cheese, red meat and processed meats, fast-fried foods, pastries and sweets). Considering that the mentioned FFQ did not have data regarding wine consumption, and due to the illegal nature of alcohol consumption in Iran that may encourage people to hide their alcohol consumption33, this item was not considered for calculation. Then, based on the method used in the previous study34, the participants were categorized based on their tertiles intake of the MIND diet score components. For brain-healthy food items, the individuals in the first, second, and third tertiles were specified 0, 0.5, and 1 scores, respectively. The reverse scores were given for tertiles of brain-unhealthy foods. The consumption of olive oil was scored as one if the individual recognized it as the main oil often used at home and as 0 otherwise. Finally, the total MIND diet score was computed by summing each food item’s scores, ranging from 0 to 14.

Statistical analysis

We used IBM SPSS statistics-26 software for data analysis. The continuous variables were reported as mean and standard deviations. The nominal and categorical data were reported as frequency and percent. The patients were stratified into three groups according to their tertiles of MIND diet scores. Then the differences in numerical data across tertiles were conducted using the one-way ANOVA. The nominal and categorical data were compared using the chi-square across quartiles. The crude and adjusted ORs for the associations between the MIND diet score and UC severity were conducted using logistic regression. Considering that previous studies indicated that demographic35, lifestyle36, dietary37,38, and disease-related parameters may affect the symptoms and disease activity in patients with IBD, the results of regression were adjusted to energy intake, BMI, nutritional supplement use, age, sex, smoking, treatments, and disease duration.

Results

In the present cross-sectional study, 158 patients with a mean age of 42.52 ± 12.61 years old participated. The flow diagram of patient inclusion is presented in Fig. 1. As shown in Table 1, there were no significant differences in demographic characteristics of participants across different tertiles of the MIND diet except for prednisolone use, and following a special diet that was significantly different across different tertiles of the MIND diet score (p < 0.05).

Fig. 1
figure 1

Flow chart of patients’ inclusion.

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Table 1 Demographic characteristics of participants across different tertiles of MIND score.
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The consumption of food components of the MIND diet across tertiles of the MIND diet is shown in Table 2. According to the results of one-way ANOVA, the subjects in the higher tertiles consumed significantly more green leafy vegetables (P < 0.001), other vegetables (P < 0.001), berries (P = 0.02), nuts (P = 0.02), and olive oils (P = 0.0), but consumed less fast fries’ foods (P = 0.03) than those in the lower tertiles.

Table 2 Dietary intakes of MIND diet components among participants across tertiles of the MIND diet score.
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Table 3 presents the association between disease severity and MIND diet score in patients with ulcerative colitis. In the unadjusted model, the patients who were in the second tertile (OR: 0.45, 95% CI: 0.21, 0.97), and the third tertile (OR: 0.33, 95% CI: 0.14, 0. 47) of the MIND diet score compared with patients who were in the first tertile, had significantly lower total mayo scores. Moreover, after adjusting for diet-related, and demographic characteristics, compared with the patients in the first tertile of the MIND diet score, the patients in the third tertile had significantly lower odds of disease severity (OR: 0.39, 95% CI: 0.16, 0.97).

Table 3 The association between disease severity and MIND score tertile in patients with ulcerative colitis.
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Discussion

This cross-sectional study investigated the association between disease severity and adherence to the MIND diet score in patients with ulcerative colitis. The results indicated that the patients in the higher tertile of the MIND diet score had 61% lower odds of having severe UC than those in the first tertile. Previously, in a cohort study, higher adherence to the MIND diet was associated with a lower risk of IBD39. However, no significant association was observed between MIND diet adherence and other gastrointestinal disease such as IBS40.

To the best of the author’s knowledge, no study has been published regarding the association of the MIND diet and disease severity in patients with UC. However, some studies reported an association between adherence to other healthy dietary patterns and disease severity in these patients18,19,20. For instance, the positive effect of a plant-based diet, and the Mediterranean diet on UC severity have been stated18,19,41,42. Although like the plant-based diet (PBD) and Mediterranean diet (MD), the MIND diet recommends the consumption of plant foods and limits the consumption of animal-based dietary products, it is unique in recommending the consumption of berries, whole grains, and green leafy vegetables43. Therefore, in addition to the positive effects of PBD, and MD on IBD, the MIND diet may have additional effects.

Berries are most commonly rich in phenolic compounds and antioxidants22. In addition to berries, whole grains are composed of bran and germ, which have unique health-promoting bioactive components such as phenolic acids and flavonoids23,24,25. Green leafy vegetables also are good sources of phytochemicals such as carotenoids, and lutein26. Previous studies indicated that polyphenols apply anti-inflammatory and antioxidant effects through the modulation of cellular signaling pathways and transcription factors important in IBD progression27. Moreover, dietary polyphenols decrease intestinal inflammation by modifying gut microbiota composition and regulating macrophage activation44,45,46,47. Considering that berries, green leafy vegetables, and whole grains compose different types of phytochemicals, consuming these foods together in a diet, can have additive and synergistic effects of phytochemicals30. In addition to polyphenols, these food items are high in dietary fiber. An interventional study showed that a diet with high fiber content may have a similar potency in maintaining remission in patients with UC as mesalazine therapy48. In addition, another interventional study showed the positive effect of germinated barely food stuff on inflammatory factors in patients with UC12,13. The review study results also conclude that dietary fiber may positively affect the course of UC remission49. In addition to polyphenols and fiber, these food items are good sources of antioxidant vitamins and minerals. The positive effect of antioxidant vitamins and minerals on inflammatory factors and disease severity in patients with UC has been reported28,29.

The present study has some limitations that should be considered in the interpretation of the results. first, this study has a cross-sectional design that limits the assessment of the causal effects of the MIND diet on the UC course. Second, the dietary intake was assessed by FFQ that is Less accurate for absolute intake estimation. However, we used a valid 168-item FFQ with an in-person interview to increase its accuracy. Third, considering the stigmatized and illegal nature of alcohol consumption in Iran, most patients did not report their real alcohol consumption specially in direct interviews. So, we did not consider the wine consumption score in the total MIND diet score. Fifth, in the present study, the data were collected from only one center, which may limit its generalizability. However, the center where the data were collected is the referral center for all IBD patients in northwest Iran. sixth, although we considered different covariates in regression analysis to report accurately the association between MIND diet score and disease severity, some unidentified and unmeasured covariates such as genetic factors50, serum vitamin D level51,52, and physical activity53, could not be controlled.

Conclusion

In conclusion, the results of the present study showed that high adherence to the MIND diet score was significantly associated with lower odds of severe UC. So, from the clinical point of view, this dietary pattern could be recommended to patients with active UC to decrease the disease severity. Moreover, it could be recommended to patients in remission to prevent flares-up. However, from the research point of view, considering the study limitations, more prospective and interventional studies adjusting to additional covariates are needed to provide a complete overview of the association between MIND diet score and UC severity.