Systematic review of nutrition screening and assessment in inflammatory bowel disease

Table 1 Demographics of patients with inflammatory bowel disease included in the studies

Study ID	Total (n) (M:F)	CD:UC:ID (n)	Age (yr)	BMI (kg/m2)	Steroid n (%)	Immunomo-dulator n (%)	Biologics n (%)	Previous resection n (%)
Adams et al[33]	90 (38:52)	76:14	Median: 35 (26-50)	Median: 22.5	30 (33)	40 (44)	15 (17)	40 (44)
Bamba et al[9]	72 (52:19)	43:29	UC Median: 39 (28-55)	Median: 19.5	-	-	-	25 (35)
			CD Median: 29 (25-37)
Csontos et al[30]	173 (92:81)	126:47	Mean: 34.8 ± 12.3	Mean: 23.6	-	-	-	-
Cushing et al[34]	89 (53:29)	0:89	Mean: 43 (9 – 86)	Non-sarcopenic: 26 ± 8	-	33 (37)	26 (29)	-
				Sarcopenic: 23 ± 6
Fujikawa et al[29]	69 (45:24)	0:69:0	Mean: 39.8 ± 14.4	Mean: 20.40 ± 3.65	-	-	-	-
Haskey et al[35]	110 (47:63)	75:35	Mean: 39 ± 15	Mean BMI: 26.4 ± 5.8	5 (4.5)	17 (15.5)	17 (15.5)	-
Holt et al[36]	44 (20:24)	44:0	Mean: 37.8 ± 14.2	Mean: 23.5	20 (45)	26 (59)	10 (24)	44 (100)
Jansen et al[8]	55 (19:36)	55:0	Mean: 40 ± 11	Mean: 24.9	10 (18)	31 (56)	21 (38)	-
O’Brien et al[31]	77 (46:31)	52:21:4	Median: 42 (20-80)	Median: 24 (16-37)	42 (55)	-	-	-
Pedersen et al[12]	178 (86:92)	127:51	Mean: 42.71 (18-86)	-	86 (48)	63 (35)	42 (24)	178 (100)
Sumi et al[27]	16 (12:4)	16:0	Responders median: 34 (18-68)	Responders median: 21.7	5 (31)	8 (50)	-	9 (56)
			Non-responders median: 31 (23-46)	Non-responders Median: 16.8
Takaoka et al[13]	40 (30:10)	40:0	Median: 32.4 (25.3-37.8)	Median:19.2	12 (30)	15 (38)	30 (75)	13 (33)
Thiberge et al[32]	149 (68:81)	149:0	Mean: 41.0 ± 17.5	Mean: 22.7 ± 6.1	108	85	86	85
Zhang T et al[10]	114 (75:39)	114:0	Mean: 32 ± 11.47	Median: 13.66	-	-	-	114 (100)
Zhang T et al[11]	204 (NR)	105:99	NR (min 18; max 65)	Median: 18.41	99 (49)	53 (26)	25 (12)	14 (7)
Zhang W et al[28]	138 (86:52)	138:0	Median: 29 (16-60)	Median: 17.9	13 (9)	50 (36)	-	37 (27)

NR: Not reported; CD: Crohn’s disease; UC: Ulcerative colitis.

Table 2 Components and interpretation of nutrition screening tools

NST	NRS-2002[9]	MUST[9]	NRI[27]	MIRT[8]	SaskIBD-NR[35]
NST components
	Initial screening	BMI	Serum albumin	BMI	Symptoms (nausea/vomiting/diarrhea/poor appetite > 2 wk)
	BMI	Weight loss (last 3-6 mo)	Present weight/usual weight	Weight loss (last 3 mo)	Weight loss (last month)
	Weight loss (last 6 mo)	Acute disease effect3		CRP	Anorexia
	Dietary intake (last week)				Food restriction
	ICU patient
	Final Screening1
	Weight loss
	Food intake
	Disease severity2
NST score indicating risk of malnutrition
	0 = Low	0 = Low	> 97.5 = No Risk	Score range = 0-8	0-2 = Low risk
	1 = Mild	1 = Medium	83.5-97.5 = Moderate	0 = Lowest	3-4 = Medium risk
	2 = Moderate	≥ 2 = High	< 83.5 = High	8 = Highest	≥ 5 = High risk
	≥ 3 = High

¹To be conducted if there is a “YES” to any one of initial screening questions;

²Categorized into mild/moderate/severe based on descriptors in Nutrition Risk Screening 2002 Tool;

³Patient is acutely ill AND there has been/likely to be no nutrition intake > 5 d. BMI: Body mass index; CRP: C-reactive protein; ICU: Intensive care unit. NST: Nutrition screening tools; NRS-2002: Nutrition Risk Screening 2002; MUST: Malnutrition universal screening tool; NRI: Nutritional Risk Index; MIRT: Malnutrition Inflammation Risk Tool; SaskIBD-NR: Saskatchewan Inflammatory Bowel Disease Nutrition Risk.

Table 3 Components and interpretation of nutrition assessment tools

Nutrition Assessment Tools
SGA[8,9,13]	Comprehensive RD/GI Assessment[35]	BIA[28,30]	CT Scan[9-12,29,31-34,36]
NAT Components
Nutrient Intake	BMI	SMP	mHUAC
Weight loss	GI symptoms, oral intake	FFMI	L3 SMI
Symptoms affecting oral intake	IBD location, severity, concurrent conditions		L4 TPA
Functional capacity	Surgical history, medications		ASMI
Metabolic requirement	Laboratory parameters (Albumin/Vit D/Iron/Vit B12)		SMA
Physical examination	SCAI, HBS
NAT interpretation
A = Well nourished	At risk	Sarcopenia:	Sarcopenia:
B = Mild/moderately malnourished	Not at risk	FFMI:	mHUAC: Lowest sex quartile at level of L3 vertebrae
C = Severely malnourished		Men: ≤ 17 kg/m2	L3 SMI: Lowest sex quartile, variable between studies (Male: < 42-55 cm2/m2; Female: < 35.6-41 cm2/m2)
		Women: ≤ 15 kg/m2	L4 TPA: Lowest sex quartile (Male < 56.7 cm2/m2, Female: < 35.6 cm2/m2)
		SMP: Continuous variable	ASMI/SMA: Continuous variable

BMI: Body mass index; SCAI: Simple Colitis Activity Index; HBS: Harvey Bradshaw Score; SGA: Subjective Global Assessment; SMP: Skeletal Muscle Percentage; FFMI: Fat Free Mass Index; mHUAC: Mean Hounsfield Unit Area Calculation; ASMI: Appendicular Skeletal Muscle Index; L3 SMI: L3 Vertebrae Skeletal Muscle Index; SMA: Skeletal Muscle Area; IBD: Inflammatory bowel disease; CT: Computed tomography; RD: Registered dietitian; GI: Gastroenterologist.

Table 4 Proportion of nutrition abnormalities via nutrition screening tools

NST	Proportion of low risk patient’s n (%)	Proportion of mild-moderate risk patient’s n (%)	Proportion of high-risk patient’s n (%)	Study ID
MUST	12 (16.7)	27 (37.5)	49 (68.1)	Bamba et al[9]
	118 (68.2)	18 (10.4)	37 (21.4)	Csontos et al[30]
	93 (84.5)	12 (10.9)	5 (4.5)	Haskey et al[35]
	10 (25.0)	6 (15)	24 (60)	Takaoka et al[13]
NRI	5 (31.3)	11 (68.8)		Sumi et al[27]
NRS-2002	0 (0)	24 (33.3)	48 (66.7)	Bamba et al[9]
	13 (32.5)		27 (67.5)	Takaoka et al[13]
SaskIBD-NRT	89 (80.9)	12 (10.9)	9 (8.2)	Haskey et al[35]

NST: Nutrition screening tools; NRS-2002: Nutrition Risk Screening 2002; MUST: Malnutrition universal screening tool; NRI: Nutritional Risk Index; SaskIBD-NRT: Saskatchewan Inflammatory Bowel Disease Nutrition Risk Tool.

Table 5 Proportion of nutrition abnormalities via nutrition assessment tools

NAT measure
	Proportion of non-sarcopenic patients n (%)	Proportion of sarcopenic patients n (%)		Study ID
Sarcopenia	49 (54.4)	41 (45.6)		Adams et al[33]
	42 (58.3)	30 (41.7)		Bamba et al[9]
	125 (72.3)	48 (27.7)		Csontos et al[30]
	25 (30.5)	57 (69.5)		Cushing et al[34]
	51 (73.9)	18 (26.1)		Fujikawa et al[29]
	47 (67.1)	30 (38.9)		O’Brien et al[31]
	134 (75.3)	44 (24.7)		Pedersen et al[12]
	99 (66.4)	50 (33.6)		Thiberge et al[32]
	115 (56.4)	89 (43.6)		Zhang et al[11]
	44 (35.1)	70 (61.4)		Zhang et al[10]
Comprehensive RD/GI Assessment	Proportion of patients not at risk n (%)	Proportion of patients at risk of malnutrition n (%)		Study ID
	87 (79.1)	23 (20.9)		Haskey et al[35]
SGA	Proportion of SGA A	Proportion of SGA B	Proportion of SGA C	Study ID
	8 (11.1)	37 (51.4)	27 (37.5%)	Bamba et al[9]
	8 (20.0)	17 (42.5)	15 (37.5%)	Takaoka et al[13]
	48 (87.3)	7 (12.7)		Jansen et al[8]

NAT: Nutrition assessment tools; RD/GI: Registered dietitian/Gastroenterologist.

Table 6 Nutrition screening tools correlating with nutrition assessment tools

NST	Comparative NAT measure	Statistical Variable	Value	Study ID
MUST	FFMI	Cohen’s Kappa (low/normal FFMI vs low MUST)	κ = 0.53 (95%CI: 0.39-0.67)	Csontos et al[30]
	SMI	Logistic Regression (MUST 0,1 vs ≥ 2)	OR: 0.934, P = 0.014a	Bamba et al[9]
	RD/GI Assessment	Cohen’s Kappa	κ = 0.15	Haskey et al[35]
MIRT	SGA	Spearman’s Rank Correlation	ρ = 0.394, P = 0.005a	Jansen et al[8]
NRS-2002	SMI	Logistic Regression (NRS-2002 1, 2 vs ≥ 3)	OR: 0.928, P = 0.008a	Bamba et al[9]
SaskIBD-NR	RD/GI Assessment	Cohen’s Kappa	κ = 0.73	Haskey et al[35]

^aIndicates significant P value < 0.05. FFMI: Fat Free Mas Index; SMI: Skeletal Muscle Index; SGA: Subjective Global Assessment; OR: Odds ratio; NST: Nutrition screening tools; NRS-2002: Nutrition Risk Screening 2002; MUST: Malnutrition universal screening tool; SaskIBD-NR: Saskatchewan Inflammatory Bowel Disease Nutrition Risk Tool; MIRT: Malnutrition Inflammation Risk Tool; RD/GI: Registered dietitian/Gastroenterologist.

Table 7 Significant nutrition screening tool correlations with clinical outcomes

NST	Comparative outcome measure	Statistical variable	Value	Study ID
MIRT	Hospitalization	Spearman’s rank correlation	ρ = 0.398, P = 0.003a	Jansen et al[8]
	Disease flare		ρ = 0.299, P = 0.030a
	Disease complications1		ρ = 0.333, P = 0.015a
	Need for surgery		ρ = 0.371, P = 0.006a
NRI	Response to infliximab	Fischer’s exact test	P = 0.037a	Sumi et al[27]
NRS-2002	Length of stay (< 28 vs ≥ 28 d)	Chi-square test	P = 0.032a	Takaoka et al[13]

^aIndicates significant P value < 0.05);

¹Newly occurred stenosis, fistula or abscess. NST: Nutrition screening tools; NRS-2002: Nutrition risk screening 2002; NRI: Nutritional risk index; MIRT: Malnutrition inflammation risk tool.

Table 8 Significant nutrition assessment tool correlations with clinical outcomes

NAT	Comparative outcome measure	Statistical analysis	Result	Study ID
SGA	Length of stay in hospital	Chi-square test	P = 0.008	Takaoka et al[13]
Sarcopenia	Change in IBD disease activity at 6 mo (HBI)	Paired t-test (baseline vs 6 mo)	Sarcopenic: 0.4 (P = 0.80)	Adams et al[33]
			Non-sarcopenic: -2.3 (P = 0.004)
	Need for operation (operation free survival curve)	Kaplan-Meier Analysis	P = 0.003	Bamba et al[9]
			P = 0.003	Zhang et al[11]
	Need for operation	Cox-regression (multivariate)	HR 0.318 (0.126-0.802), P = 0.015	Bamba et al[9]
	Need for any rescue therapy (medical/surgical)	Fischers exact test	P = 0.02	Cushing et al[34]
		Multivariate logistic regression	OR 3.98 (95%CI 1.12-14.1), P = 0.033
	Post-operative complications (Major)1		OR 9.24 (95%CI 1.10-77.50). P = 0.04	Zhang et al[10]
	UC disease activity (Mayo Score ≥ 6)		OR 8.49 (95%CI 1.80-40.10), P = 0.007	Zhang et al[11]
	Post-operative surgical site infection		OR 4.91 (95%CI 1.09-23.50), P = 0.03	Fujikawa et al[29]
	Need for red blood cell transfusion		OR 1.31, P = 0.014	Pedersen et al[12]
	ICU admission		OR 1.32, P = 0.016
	Post-operative sepsis		OR 1.325, P = 0.009
	Deep vein thrombosis		OR 1.265, P = 0.0173
	Clavien-Dindo grade 4 complication		OR 1.329, P = 0.0052
ASMI	Fecal calprotectin	Spearman’s Rank Correlation	ρ = -0.564, P = 0.005	Holt et al[36]
L3 SMI	UC disease activity (Mayo Score)		ρ = -0.523, P ≤ 0.01	Zhang et al[11]
SMA			ρ = -0.445, P ≤ 0.01
SMP	Post-operative complications (Overall)2	Multivariate logistic regression analysis	OR: 0.487 (95%CI 0.307-0.772) P = 0.002a	Zhang et al[28]
	Post-op complications (Major)1		OR: 0.588 (95%CI 0.422-0.820) P = 0.002a

^aIndicates significant P value < 0.05);

¹Clavien-Dindo Score ≥ 3;

²Clavien-Dindo Score 1-5. HR: Hazard ratio; OR: Odds ratio; CI: Confidence interval; HBI: Harvey-bradshaw index; mHUAC: Mean hounsfield unit area calculation; ASMI: Appendicular skeletal muscle index; SMI: Skeletal muscle index; SMA: Skeletal muscle area; SMP: Skeletal muscle percentage; SGA: Subjective global assessment.