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Address correspondence to: Miranda C. E. Lomer, PhD, RD, Department of Nutritional Sciences, King’s College London, 4.104 Franklin-Wilkins Bldg, 150 Stamford St, London SE1 9NH, United Kingdom.
Malnutrition is common in patients with Crohn’s disease and negatively influences immunity and quality of life. The optimal tools for nutrition assessment in patients with Crohn’s disease are not clearly defined and lead to variations in practice. With this review, we aimed to appraise the existing evidence for nutrition assessment of patients with Crohn’s disease compared with healthy controls and provide a comprehensive guide with relevant measures applicable to clinical practice. A literature search using Medline, Embase, and Scopus from inception to October 1, 2018, was conducted. Forty-one articles that assessed body composition, muscle strength, micronutrient status and/or dietary intake in adults with Crohn’s disease compared with an age- and sex-matched healthy individuals were included. There were heterogeneous findings on nutritional status in patients with Crohn’s disease compared with healthy controls. Only one article reported a clinically significant difference for body mass index; however, significant deficits in fat mass, fat-free mass, and muscle strength were observed in patients with Crohn’s disease compared with healthy controls, with more pronounced differences with increasing disease activity and length of diagnosis. Most research reported significantly lower serum micronutrients in patients with Crohn’s disease compared with healthy controls. Half of studies measuring micronutrient intake reported lower intakes in patients with Crohn’s disease compared with healthy controls. Fruit and vegetable intake was also lower in patients with Crohn’s disease. Difficulties characterizing the type and prevalence of malnutrition exist due to the heterogeneous nature of Crohn’s disease and warrants continued investigation. As a result of this review, we advocate that a nutrition assessment should include more parameters than weight and body mass index.
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Research Question: What is the existing evidence to inform a comprehensive nutrition assessment of patients with Crohn’s disease?
Key Findings: There were heterogeneous findings on nutritional status in Crohn’s disease. Significant deficits in fat mass, fat-free mass, and muscle strength were observed. Lower serum micronutrient levels, micronutrient intakes, and fruit and vegetable intakes were reported in patients with Crohn’s disease compared with healthy controls. The findings from this narrative review have informed the development of a practical clinical guide for comprehensive nutrition assessment of patients with Crohn’s disease.
Malnutrition is a significant issue in patients with Crohn’s disease with an estimated prevalence between 20% and 85%, depending on the criteria used.
It is associated with increased susceptibility to infections, gastrointestinal barrier dysfunction, postoperative complications, and reduced quality of life.
Risk factors for intra-abdominal septic complications after a first ileocecal resection for Crohn's disease: A multivariate analysis in 161 consecutive patients.
Reasons for malnutrition in patients with Crohn’s disease are multifactorial. More than 80% of people with Crohn’s disease experience problems with food
Micronutrient deficiencies in patients with Crohn’s disease are a further health care burden. Inflammation and suboptimal vitamin D levels are associated with impaired bone mineral density, making osteoporosis common in patients with Crohn’s disease.
The risk of malnutrition persists during the remission phase of the disease; whilst 86% of patients with active disease avoid certain foods during flare-ups, 77% of patients continue to avoid certain foods during remission to prevent disease relapse.
In clinical practice, nutrition assessment in patients with Crohn’s disease remains challenging and most frequently is measured using weight and body mass index (BMI).
Weight and BMI are inadequate measures of malnutrition in Crohn’s disease as systemic inflammation alters body composition, meaning BMI may mask deficits in lean mass due to increased fat mass.
However, there are no guidelines on what components should be included in a comprehensive nutrition assessment for patients with Crohn’s disease.
Accurate quantification of nutritional status in Crohn’s disease is essential to enable diet and nutrition therapy to be targeted to address specific deficits. However, in a study on nutrition assessment in patients with Crohn’s disease, body composition was measured in only 3%, handgrip strength in only 4%, and dietary micronutrient intake in 16% of patients, suggesting that current assessments are limited.
This narrative review comprehensively appraised the existing evidence for nutrition assessment of patients with Crohn’s disease in comparison to a healthy population. It aims to provide a comprehensive guide with relevant measures applicable to clinical practice.
Methods
Search Strategy and Study Selection
The population, intervention, comparison, outcomes, and type of study framework
was used to inform the criteria needed to answer the research question, What evidence exists on the nutritional status of patients with Crohn’s disease and how can this evidence inform nutrition assessment in clinical practice? The search strategy included studies of patients with Crohn’s disease aged 18 to 64 years using validated assessment methods available in clinical practice to establish nutritional status compared with a healthy age- and sex-matched control group (HC) sampled from the same population as those with Crohn’s disease. Studies that reported nutritional status outcomes, including body composition, muscle strength and function, micronutrient status, and/or dietary intake were included in the case that they were in the English language and primary research or systematic reviews.
Limiting the search in this way allowed the literature review to establish a typical nutritional status in healthy people without Crohn’s disease and facilitated the comparative quantification of nutritional status in Crohn’s disease. Whilst anthropometric reference ranges for the healthy population have been developed, these vary depending on assessment methods used.
Recruiting a HC group ensured comparisons were made using identical methods to those used with patients with Crohn’s disease. Three databases were searched (Medline, Embase, and Scopus) on October 1, 2018. Multiple search terms were combined with the Boolean functions and and or to focus the search.
The medical library subject heading terms or keywords included were [Crohn’s disease OR inflammatory bowel disease] AND [nutrition* assessment, body composition, body fat, fat mass, anthropometry, lean body weight, malnutrition, protein energy malnutrition, muscle strength, hand grip, grip strength, trace element, nutrition* status, nutrition* deficiency, vitamin deficiency, mineral deficiency, dietary intake, diet OR micronutrient]. Filters (English, human, and adults aged 18 to 64 years) were applied to target the search results.
Following removal of duplicates, the titles, and where applicable abstracts, were screened for relevance. Abstracts of relevant titles were reviewed and in the case that an HC group was described the full text was examined against the inclusion and exclusion criteria.
Data Extraction and Synthesis
Eligible studies for data synthesis were critically appraised using the Critically Appraising Papers process in Hickson
to assess quality of individual studies. Data were summarized in a data extraction spreadsheet according to anthropometric, biochemical, and dietary assessment techniques (per the Nutrition Care Process structure
). The Nutrition Care Process was developed by the Academy of Nutrition and Dietetics and is used by members of the dietetics profession to ensure systematic, evidence-based nutrition care.
Outcome data were only extracted when they were available and clinically relevant. Anthropometric outcomes included assessment of body composition using direct anthropometry, bioelectrical impedance analysis (BIA), dual energy x-ray absorptiometry (DEXA), computed tomography (CT) or magnetic resonance imaging (MRI), and muscle strength or function measurements. Biochemical outcomes included plasma or serum markers of nutritional status such as folic acid, vitamin B-12, vitamin C, vitamin D, zinc, copper, and selenium. Iron status and albumin were not collected because these are acute phase reactants and results are difficult to compare with an HC population. Dietary intake outcomes included macronutrient and micronutrient intake, food group intake, or exclusions of specific food groups. Where possible the anthropometric, biochemical, and dietary assessment methods and results were compared and critiqued across studies.
Discussion
To our knowledge, this is the first review appraising the evidence for methods of nutrition assessment in patients with Crohn’s disease relevant to clinical practice. There were 41 eligible papers (Figure 1), including 2,370 patients with Crohn’s disease and 4,450 HC. All studies were cross-sectional in design. The Crohn’s disease cohorts included patients with active disease and/or disease in remission. Most studies included men and women with the exception of two studies that reported body composition data of only men
Nevertheless, compared with HC, there were significant differences in body composition and dietary intake as well as deficits in muscle strength and serum micronutrients. The findings follow the Nutrition Care Process (anthropometric, biochemical, and dietary assessment structure) and include recommendations for clinical practice (Figure 2).
Figure 1Preferred Reporting Items for Systematic Reviews and Meta-Analyses flow diagram for studies included in the narrative review on nutrition assessment in patients with Crohn’s disease.
Figure 2Components of a comprehensive nutrition assessment tool for patients with Crohn’s disease. Components are based on evidence from studies included in the narrative review.
Figure 2Components of a comprehensive nutrition assessment tool for patients with Crohn’s disease. Components are based on evidence from studies included in the narrative review.
However, studies rarely assessed clinically significant differences in BMI, because BMI tended to be reported as a mean rather than as the proportion of patients who had a clinically underweight BMI (<18.5).
These findings suggest that lean mass depletion in patients with Crohn’s disease occurs over time. One study recruited patients with active Crohn’s disease and showed that BMI was significantly lower in the active disease group as was FFM, and FM was nonsignificantly different when compared with HC.
DEXA scans have ethical and practical limitations. Small amounts of radiation are absorbed by bone and tissue and increasing exposure to radiation is linked to an increased cancer risk.
However, it lacks external validity to non-Indian populations because recent data demonstrate significant ethnic disparities in body composition, especially in South Asians.
Thus, there are body composition deficits in patients with active Crohn’s disease, highlighting the importance of considering disease activity in the clinical assessment section of the Nutrition Care Process.
CT and MRI
Three studies used medical imaging techniques to further explore body composition.
The researchers found intra-abdominal fat was significantly higher in patients with Crohn’s disease vs HC. Furthermore, using MRI, visceral adipose tissue was significantly higher in patients with Crohn’s disease in remission compared with HC.
Quadricep muscle cross-sectional area was 14% lower in patients with Crohn’s disease compared with HC; however, this was not statistically significant.
Muscle Strength and Function
Eight studies assessed muscle strength and function.
whereas at least 5 years after diagnosis, the literature suggests a reduction in muscle strength and increased muscle fatigue in active disease or disease in remission.
There are no reports of change in muscle strength over time in patients with Crohn’s disease compared with HC. It is unknown whether reduced muscle strength during active disease is a temporary reduction in strength associated with a disease flare and if, or how quickly, muscle strength improves once the disease is in remission. One study found no difference in handgrip strength but reduced muscle endurance between patients with Crohn’s disease in remission for at least 3 months compared with HC.
Longitudinal research on muscle strength during periods of active disease and disease remission would provide further understanding on the effects of acute and chronic inflammation on muscle strength and function. Muscle wasting and weakness results in fatigue and reduced quality of life,
The authors cite strong correlations between their direct anthropometry results and BIA/DEXA as a justification for presenting only the results of the latter. However, critics may argue this preferential inclusion of BIA/DEXA results at the expense of omitting anthropometric data represents reporting bias.
FM percentage and muscle mass did not differ significantly between patients with Crohn’s disease and HC. This finding that the body composition of Crohn’s disease patients is not inferior to HC is surprising; especially considering 47% of the group had active disease (Crohn's disease activity index [CDAI] >150). In another study, lower tricep skinfold thickness was reported in men with Crohn’s disease compared with HC men, whilst there was no difference between women, suggesting there may be sex differences.
confirming that using BMI alone provide limited data for an optimal nutrition assessment. Only 14 studies examined FFM and FM, half of which suggest that FFM is decreased in Crohn’s disease
However, the routine use of BIA in clinical practice may be time intensive and financially challenging; thus, mid-arm anthropometry and handgrip strength (HGS) are measures that can be readily and cheaply assimilated into clinical practice
report deficiency prevalence for micronutrients other than vitamin D. In clinical practice, patients are not treated for low micronutrient levels unless they are deficient,
Table 3Vitamin D concentration and prevalence of deficiency in patients with Crohn’s disease (CD) compared with an age- and sex-matched healthy control group (HC)
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
a To convert nmol/L vitamin D to ng/mL, multiply nmol/L by 0.4006. To convert ng/mL vitamin D to nmol/L, multiply ng/mL by 2.496. Vitamin D of 70 nmol/L=28.042 ng/mL.
b No statistical test reported comparing CD and HC.
There were no studies comparing micronutrient differences between active and remission Crohn’s disease, although the validity of measuring micronutrients in active disease is questionable. In clinical practice, and in the included studies, micronutrients are quantified in the plasma fraction of blood. However, inflammatory responses in patients with active Crohn’s disease have been found to decrease plasma micronutrient concentrations by decreasing albumin, independent of their actual body stores.
Impact of exclusive enteral nutrition on body composition and circulating micronutrients in plasma and erythrocytes of children with active Crohn's disease.
Micronutrients on circulating erythrocytes provide a more accurate marker of micronutrient stores, particularly for zinc, copper, selenium, riboflavin and vitamin B-6, but this analysis is not available in routine clinical practice. Indeed, the transport protein for copper increases in the acute phase response, which may explain one study’s finding of significantly higher serum levels of copper in patients with Crohn’s disease compared with HC.
In summary, the majority of studies reported lower mean levels of circulating micronutrients in patients with Crohn’s disease compared with HC, including folic acid, vitamin B-12, vitamin C, vitamin D, zinc, and selenium.
Whilst the review findings do not support the routine measurement of vitamin B-6 and thiamine in all Crohn’s disease patients, consideration must be given to their jejunal absorption site. For patients with small bowel disease or previous resection, it is common practice to measure micronutrients absorbed at the jejunum every 3 to 6 months.
See Figure 2 for key micronutrients that should be measured in Crohn’s disease in clinical practice, and their accuracy in reflecting body stores during the acute phase response.
Dietary Assessment Outcomes
Eleven studies assessed dietary intake and the main findings are summarized in Table 4.
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