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Nutrition, Nutritional Status, Micronutrients Deficiency, and Disease Course of Inflammatory Bowel Disease

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2023-9-1 17:56
MDPI
PTLv2
Followers：3Columns：927

1. Introduction

Inflammatory bowel diseases (IBD) are chronic inflammatory diseases, mediated by the immune system, which affect the gastrointestinal tract. The two main manifestations are Crohn’s Disease (CD) and ulcerative colitis (UC). CD may affect any area of the gastrointestinal tract and has a transmural involvement. UC generally occurs only in the rectum and colon and involves the mucosa and submucosa layers [1,2].

The etiology of IBD is not completely defined. Yet, several studies support the hypothesis that their onset is due to a combination and interplay of genetic factors, immune dysregulation and environmental triggers that can modify gut microbiome [3,4,5]. In this scenario, diet is a potential environmental trigger. The global increasing incidence of IBD seems to be associated with Western lifestyle and diet: a high intake of proteins and red meat can result in an increased production of bacterial metabolites, such as an increase of ammonia, indoles, phenols, and sulphides, and a decrease of short-chain fatty acids (SCFAs), which could all be involved in the development of IBD [6,7].

As a consequence, diet modifications have been considered therapeutic tools; for example, in pediatric IBD patients, enteral nutrition has been shown to be effective in inducing clinical remission, independently of the used formula [8,9,10].

Malnutrition, undernutrition and overnutrition seen in such patients are variable during the disease course [11] and due to suboptimal nutritional intake, alterations in nutrient requirements and metabolism, malabsorption, excessive gastrointestinal losses, and medication [12].

At the time of diagnosis, 60% of CD patients and 35% of UC patients are underweight, even if this proportion is lowered in the last years, reflecting the increased incidence of obesity [13,14]: 20–40% of adult patients with IBD are overweight (25 < body mass index (BMI) < 30 kg/m2), and an additional 15–40% are obese (BMI > 30 kg/m2) [15].

Obesity is associated with treatment failure (especially with anti-TNF drugs), risk of hospitalization, and lower endoscopic remission rates [16,17,18,19]; sarcopenia in overweight IBD patients (BMI ≥ 25 kg/m2) is the only significant predictor of the need for surgery (p = 0.002) [20]; nutritional deficits and low micronutrients serum levels can have a negative impact on both induction and maintenance of remission and on the quality of life of these patients [21,22]. Thus, the assessment of nutritional status in IBD patients is a crucial issue and current guidelines suggest that patients with IBD should be regularly screened for nutritional status, micronutrient deficiencies and bone mineral density [21,23].

Currently, there are limited data on the disease course and therapy response in cases of malnutrition in IBD, especially in the context of sarcopenia and undernutrition. Moreover, if micronutrient or vitamin supplementation (e.g., vitamin D supplementation) could be a potential therapeutic option or only an effect of disease activity it is still unclear [24,25].

The aim of this systematic review is trying to clarify the connection between nutrition, malnutrition (including overnutrition and undernutrition), micronutrient deficiency, and both disease course and therapeutic response in IBD patients.

2. Materials and Methods

This systematic review was performed using PubMed/MEDLINE and Scopus. For each of the relevant publications (previous review articles and included studies), reference sections were also screened for other applicable publications.

The research strategy for each clinical question is reported in the . We found 6077 articles; 762 duplicated studies were removed. Out of 412 full texts analyzed, 227 were included in the review .

No filters were used in the search strategy. The data of the last search was May 2023. The complete selection process is reported in the .

Four authors did a systematic literature search. Clinical questions and related outcomes of interest were identified using the PICO framework. Four main clinical settings concerning adult IBD patients were identified.

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Induction of remission
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Maintenance of remission
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Risk of surgery
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Postoperative recurrence (POR) and surgery-related complications

2.1. Selection of Studies and Data Extraction

Four authors (GS, SF, SM, and MM) independently reviewed abstracts and manuscripts for eligibility.

Conflicts were resolved by consensus, referring to the original articles. The selection was made according to the following criteria:

2.2. Inclusion CriteriaPatient Type: Adult Patients (age ≥ 18) with a Confirmed Diagnosis of IBD

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Intervention: Nutritional management; Nutritional evaluation; serum evaluation or supplementation of micronutrients or albumin.
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Outcome: evaluation of clinical relapse or disease activity (evaluated with disease activity score or loss of response to therapy); risk of surgery; POR and surgery-related complications
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Study type: Meta-analysis, Randomized clinical trial (RCT), Non-randomized study of intervention (NRSI), cross-sectional study.

2.3. Exclusion Criteria

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Paediatric patients
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Non-human study
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Lack of data concerning clinical response, risk of surgery, POR, and surgery-related complications.

Four reviewers (GS, SF, SM, and MM) independently reviewed the literature according to the above-predefined strategy and criteria and selected eligible studies; any disagreement was resolved by consensus or by recourse to a fifth author (MV).

Each reviewer extracted the data of interest in a pre-made template: title and reference details (first author, journal, year, country), study population characteristics (number of patients, gender, age, disease type (UC or CD), intervention details and outcome data (induction of remission, maintenance of remission, risk of surgery, POR, and surgery-related complications).

All data were recorded independently by the literature reviewers in separate databases and will be compared at the end of the reviewing process to limit selection bias. The database was also reviewed by another author (MV). Any disagreement was resolved by consensus or by recourse to the senior author.

3. Nutrition and Nutritional Status

If food is implicated in the pathogenesis of IBD is still not clear, but the impact of some nutrients on the behalf of the gastrointestinal tract has been suggested. For example, dietary fibre escape digestion in the small bowel and enter the colon where they are metabolized by gut bacteria which produce SCFAs, energy sources for colonocytes [26]. On the contrary red meat and other high-protein foods, contribute to sulphides formation which damages the mucus in the colon [27,28]. In the IBD population, 70% of patients report food-related symptom exacerbation, while a wide variety of foods are believed to be helpful [29]. This becomes a concern when patients drastically reduce or completely avoid important nutrients such as folic acid, calcium, vitamin B 12, and iron which represent the most frequent nutritional deficiency in IBD patients. This attitude, summed to disease duration, extent and severity, may put them at risk of developing nutritional deficiencies in the long term [30].

3.1. Nutrition and Exclusion Diet

Compared to recommended requirements, adults with IBD have an inadequate intake of energy, fibres, fat-soluble vitamins, folate and calcium [31]. Nutritional support for correcting deficiencies can be provided summarily in the form of parenteral nutrition (PN), enteral nutrition (EN) and specific diets.

3.2. Sarcopenia

Sarcopenia is defined by a loss in muscle mass and lean body mass that leads to functional changes and decreased strength [64].

The European Working Group on Sarcopenia in Older People (EWGSOP) developed 3 criteria for its definition and diagnosis: low muscle mass, low muscle strength, low physical performance (being necessary for the diagnosis the first criterion, plus one or both of the other two criteria) [65].

During disease flares, both the reduced caloric intake and the mucosa inflammation can impair nutrient absorption and determine weight loss [21].

3.3. Obesity

In the last decades, overweight (BMI > 25 kg/m2) and obesity (BMI > 30 kg/m2) increased not only in the general population but also among IBD patients [97]. In a time-trend analysis involving 10,282 CD patients (from 1991 to 2008) and including 40 RCT, the mean BMI increased from 20.8 to 27.0 [98]. Obesity and overweight were reported respectively in 18% and 38% of IBD patients, with a higher percentage of obesity in CD than in UC [99].

Only few studies analyzed the impact of obesity on the course of UC, while more data are available in CD patients. Anyhow, results are often contrasting and non-conclusive [100]. Obesity may be associated with a worse prognosis in CD in terms of perianal complications, disease activity, hospitalization, time to the first surgery and more aggressive medical treatment [101]. This could be probably due to the ability of visceral fat to produce cytokines and thus promote inflammation [102].

3.4. Albuminemia

Chronic inflammation of the mucosa determines both malabsorption and intestinal protein losses, resulting in hypoalbuminemia.

4. Anemia and Micronutrients

The chronic inflammatory status and the impaired absorption of nutrients due to bowel damage leads to a possible deficiency of vitamins and micronutrients that are crucial for the overall well-being [11]. If the low serum levels of these microelements are a cause or an effect of disease activity remains unclear, and if supplementation of these elements could be a potential therapeutic target is not well defined. However, the evidence is sufficiently solid in showing that active disease is linked to low serum micronutrient levels .

The micronutrients and vitamins most involved in IBD are iron, selenium, zinc, copper, manganese, vitamin D, vitamin B12 and folic acid, vitamins A, E, C, K, B1 and B6. Micronutrient and vitamin deficiencies may be linked only to IBD or also to the concomitant presence of other autoimmune diseases such as autoimmune chronic atrophic gastritis (leading to malabsorption of iron and vitamin B12) and celiac disease (responsible for malabsorption of iron and folic acid) [192].

4.1. Anemia

Anemia is a common complication of IBD. According to the World Health Organization (WHO) criteria, anemia is defined as a hemoglobin (HgB) level less than 13 g/dL in men and 12 g/dL in non-pregnant females [193].

The most common causes of anemia in IBD are iron deficiency, folic acid or vitamin B12 deficiency, chronic disease anemia due to inflammation, and combined causes. Certainly, it is crucial to classify the etiology of anemia in IBD to select the correct treatment [194,195].

Pure iron deficiency anemia is defined in the case of ferritin serum levels < 30 μg/L and the normal value of CRP; chronic disease anemia is defined by ferritin serum level > 100 μg/L and high levels of CRP. Combined anemia is defined by ferritin serum level < 100 μg/L and high levels of CRP [196].

Anemia affects the quality of life, cognitive functions, the ability to work, hospitalization, and healthcare costs [197]; if low levels of HgB could affect the disease course of IBD is not well known.

4.2. Iron

Iron deficiency (ID) is one of the worldwide most common disorders, affecting about 50% of IBD patients [195,203,204], with a prevalence ranging from 26.5% to 62.5% and representing the most common micronutrient deficiency of IBD [195,205,206,207].

In IBD patients, the diagnostic criteria for ID depend on the severity of inflammation: in remission, serum ferritin < 30 µg/L and transferrin saturation index (TSAT) < 16% are indicative of ID, while during the acute phase of the disease (CRP > 5 mg/L and/or FC > 150 mg/kg), ID is defined as ferritin < 100 µg/L.

Iron is an essential trace element involved in many cellular processes including oxygen transport, mitochondrial electron transport, gene regulation and DNA synthesis, and its deficit can manifest through a court of very heterogeneous extra-bowel symptoms including chronic fatigue, sleep disorders, agitation, decreased physical and cognitive performance, immune system impairment, significantly affecting the patient’s wellbeing [178].

Female patients and severe disease activity patients are at higher risk, due to menstrual losses in premenopausal women and to bloody diarrhoea. Interestingly, patients with ID without anaemia presented health-related quality of life (HRQoL) questionnaires with lower overall scores [178,208].

4.3. Vitamin B12 and Folic Acid

Vitamin B12 and folate deficiencies are common in patients with IBD. Folate deficiency is due to a combination of factors: poor diet, malabsorption, an increased requirement due to the increased granulocytes and other inflammatory cells, severe inflammation, resection, enteric fistulas and the use of drugs such as sulfasalazine and methotrexate [216,217].

As shown in a recent meta-analysis, the folate level in IBD patients was significantly lower compared to healthy groups; however, a lower concentration of folate was found in UC but not in CD patients [218].

Vitamin B12 deficiency is more common in CD patients compared to UC, with a prevalence of 33% and 16% respectively [219].

In CD patients, prior intestinal surgery is an independent risk factor for low serum concentrations of vitamin B12 [220]. A meta-analysis by Battat et al. identified that an ileal resection longer than 20 cm is the only factor to predispose CD patients to vitamin B12 deficiency [221].

Vitamin B12 is absorbed in the distal ileum, the intestinal tract most commonly involved in CD, and this would explain the higher prevalence of vitamin B12 deficiency in CD compared to UC.

A periodical assessment of blood levels of vitamins and iron is suggested. Guideline recommendations suggest checking haemoglobin and iron status every 6–12 months for patients in remission or with mild disease, and every 3 months in case of active disease. For patients at risk of vitamin B12 or folic acid deficiency (e.g., small bowel disease or resection), serum levels should be measured at least annually, or when macrocytosis is present [193].

4.4. Vitamin D

During the last few years, there has been an increase in interest concerning the immuno-modulating role of vitamin D [25,222]. Firstly, several observational and cross-sectional studies included in three meta-analyses showed that IBD patients presented low serum vitamin D levels compared to healthy people [183,223,224]. A meta-regression analysis shows that latitude does not influence the association between IBD and vitamin D deficiency (p = 0.34) [223].

4.5. Other Vitamins (A, E, K, Group B, and C)

As for other nutritional deficits, vitamin deficiency is common in IBD patients, and its pathogenesis is multifactorial [192].

A meta-analysis including 19 case-control studies, showed a lower serum level of fat-soluble vitamins (A, D, E, K) in IBD patients compared to the control group.

Interestingly, in the meta-regression analysis, significant associations between vitamin A levels in CD patients, and the levels of inflammatory biomarkers (CRP: p = 0.03, and albumin p = 0.0003), were found. The data concerning vitamins E and K were not enough strong to show a correlation with disease activity, however, a clear trend was found [236]. Another study showed a lower level of vitamin K in CD. The vitamin K level (evaluated by measuring serum undercarboxylated osteocalcin) was significantly correlated with the clinical activity index among CD patients [237].

Few studies reported that vitamin C deficiency is relatively common in IBD patients, in particular in patients with reduced intake of vegetables and fruit [238,239].

Little evidence showed a plausible increase in vitamin A levels after adequate treatment for disease activity in UC patients. Plasma vitamin A is significantly lower in active UC patients compared to the control group (p = 0.0005) [240,241]. Another retrospective study including CD patients who underwent surgery showed a significantly higher basal peroxidative state and lower levels of Vitamin A and E compared to controls among the CD patients. Two months after surgery, a significant increase in serum vitamin A levels but not Vitamin E was found [242].

Concerning the other vitamin of group B only a few data are available [192,243]. However, some evidence showed that Vitamin B1 deficiency could be related to chronic fatigue in IBD patients [244].

4.6. Other Trace Elements (Selenium, Zinc, Copper, Manganese)

Zinc and Selenium are involved in the regulation of the immune response, inflammatory processes, and the regulation of oxidative stress [245,246]. Considering this, their low serum concentration may exacerbate inflammation through the dysfunction of the epithelial barrier, an altered mucosal immunity, and an increased production of pro-inflammatory cytokines.

5. Conclusions

In a more and more ambitious approach to IBD with a treat-to-target strategy that considered tighter objectives such as mucosal healing, transmural healing, histological healing, and overall, a deep remission of the disease even the nutritional status must be considered [1,2,3,4] (Figure 1).

Figure 1. Nutrition, nutritional status, micronutrients deficiency and disease course of Inflammatory Bowel Disease [11].

The evidence summarized in this review showed that many nutritional aspects could be potential targets to induce a better control of symptoms, a deeper remission, and overall improve the quality of life of IBD patients .

Certainly, many aspects summarized in this review are still lacking strong evidence. Few data are available concerning the effect of nutritional status on the induction of remission and the impact on the risk of surgery. Obviously, some clinical outcomes need data deriving from RCTs or non-randomized studies of intervention with a long follow-up (such as the risk of surgery, POR, and clinical relapse). Often these data are still lacking. Moreover, considering that the majority of available data derive from observational studies, inclusion criteria, and the analyzed outcome are often heterogeneous.

However, the large number of studies included and analyzed in this review allow us to produce a very extensive overview concerning this issue stating practical clinical aspects and highlighting the current knowledge gap helping to drive future research. An optimal nutritional status and the good management of micronutrient deficiency, ideally with the help of dietitians, may reduce this risk of clinical relapse, risk of surgery and post-operative recurrence. Considering this, all these variables should be considered for the general assessment and monitoring of IBD patients.

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Reproduced from:https://www.mdpi.com/2072-6643/15/17/3824
During the disease course, most Inflammatory Bowel Disease patients present a condition of malnutrition, undernutrition, or even overnutrition. These conditions are mainly due to suboptimal nutritional intake, alterations in nutrient requirements and metabolism, malabsorption, and excessive gastrointestinal losses. A suboptimal nutritional status and low micronutrient serum levels can have a negative impact on both induction and maintenance of remission and on the quality of life of Inflammatory Bowel Disease patients. We performed a systematic review including all the studies evaluating the connection between nutrition, nutrition status (including undernutrition and overnutrition), micronutrient deficiency, and both disease course and therapeutic response in Inflammatory Bowel Disease patients. This systematic review was performed using PubMed/MEDLINE and Scopus. Four main clinical settings concerning the effect of nutrition on disease course in adult Inflammatory Bowel Disease patients were analyzed (induction of remission, maintenance of remission, risk of surgery, post-operative recurrence, and surgery-related complications). Four authors independently reviewed abstracts and manuscripts for eligibility. 6077 articles were found; 762 duplicated studies were removed. Out of 412 full texts analyzed, 227 were included in the review. The evidence summarized in this review showed that many nutritional aspects could be potential targets to induce a better control of symptoms, a deeper remission, and overall improve the quality of life of Inflammatory Bowel Disease patients.
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