Frequency, types, and treatment of anemia in Turkish patients with inflammatory bowel disease

Table 1 Types of anemia according to iron parameters

	Ferritin (ng/mL)	Transferrin saturation (%)	CRP (5 mg/L)
IDA	< 30	< 20	-
CDA	> 100	< 20	> 5
Mixed anemia (IDA + CDA)	> 30 and < 100	< 20

IDA: Iron deficiency anemia; CDA: Chronic disease anemia; CRP: C reactive protein.

Table 2 Demographic data of inflammatory bowel disease patients n (%)

	IBD overall	Crohn’s disease	Ulcerative colitis	P value
n	465	257 (55.3)	208 (44.7)
Age (yr) mean (SD; range)	47.1 (14.3; 18-83)	46.2 (13.4; 17-78)	48 (15.3; 12-83)	0.183
Sex (male/female)	254 (54.6)/211 (45.4)	153 (59.5)/104 (40.5)	101 (48.6)/107 (51.4)	0.019
Disease characteristics
Age at diagnosis (yr)	40.2	39.7	40.7	0.46
Location of the disease
L1		122 (48.2)
L2		48 (19)
L3		83 (32.8)
L4		-
Disease behavior
B1		148 (60.9)
B2		40 (16.5)
B3		55 (22.6)
Disease extension
E1			49 (27.5)
E2			73 (41)
E3			56 (31.5)
Drugs
SZP/5-ASA	360 (77.4)	171 (66.5)	189 (90.6)	< 0.001
Corticosteroids	55 (11.8)	30 (11.7)	25 (12)	0.90
Budenoside	17 (3.7)	15 (5.8)	2 (1)	0.005
AZA / MTX	200 (43)	155 (60.3)	45 (21.6)	< 0.001
IFX/ADA	81 (17.4)	72 (28)	9 (4.3)	< 0.001
Antibiotic	92 (19.8)	68 (26.5)	24 (11.5)	< 0.001
Surgery	70 (15.1)	60 (23.3)	10 (4.8)	< 0.001

IBD: Inflammatory bowel disease; L: Disease location (for Crohn’s disease); L1: Ileal disease; L2: Colonic disease; L3: Ileocolonic disease; L4: Upper gastrointestinal tract disease; B: Disease behavior (for Crohn’s disease); B1: Inflammatory disease; B2: Stricturing disease; B3: Penetrating disease; E: Disease extension (for ulcerative colitis); E1: Ulcerative proctitis; E2: Left-sided ulcerative colitis; E3: Extensive disease; SZP: Sulphasalazinep; 5-ASA: 5-aminosalicyclate; AZA: Azathiopurine; MTX: Methotrexate; IFX: Infliximab; ADA: Adalimumab.

Table 3 Prevalence of anemia and hematological profile at the time of diagnosis in patients with inflammatory bowel disease n (%)

	IBD overall	Crohn’s disease	Ulcerative colitis	P value
Anemia	240 (51.6)	148 (57.6)	92 (44.2)	0.005
Severe anemia	64 (16.4)	47 (21.6)	17 (9.8)	0.002
Hemoglobin (g/dL) mean (SD; range)	12.3 (2.1; 5.3-17.9)	12.1 (2.2; 5.3-16.8)	12.5 (1.9; 7.1-17.9)	0.03
Hematocrit (%) mean (SD; range)	37.41 (6.1; 10-53)	36.8 (6.6; 10-52)	38.16 (5.3; 22-53)	0.02
MCV (fL) mean (SD; range)	84.54 (7.7; 57-112)	84.75 (8.3; 58-112)	84.28 (7; 57-100)	0.46
Iron (μg/dL) mean (SD; range)	43.76 (30.3; 4-160)	43.26 (30.4; 4-126)	44.5 (30; 4-160)	0.73
Ferritin (μg/dL) mean (SD; range)	40.3 (74; 2-754)	48.96 (91; 2-754)	27.26 (37; 2-167)	0.01
TS (%) mean (SD; range)	15.35 (13; 2-100)	15.14 (12.7; 2-100)	15.67 (12; 2-92)	0.9
CRP (mg/L) mean (SD; range)	13 (29; 1-289)	17.1 (32.8; 0-289)	7.9 (7.93; 1-242)	0.001
Albumin mean (SD; range)	4.2 (0.4; 1.9-5.0)	4.1 (0.4; 1.9-4.9)	4.1 (0.4; 2.0-5.0)	0.17

MCV: Mean corpuscular volume; TS: Transferrin saturation; CRP: C reactive protein.

Table 4 Evaluation of disease characteristics according to types of anemia in inflammatory bowel disease n (%)

	Anemia	IDA	CDA	Mixed anemia	B12/Folic acid anemia	Other anemia
Sex
M	105 (41.3)	48 (18.9)	18 (7.1)	8 (3.8)	34 (13.4)	35 (13.8)
F	135 (64)	91 (43.1)	19 (9)	8 (3.1)	31 (14.6)	36 (17.1)
P value	< 0.001	< 0.001	0.44	0.7	0.6	0.32
Disease duration (yr)
A+	6.6	6.7	6.1	5.9	5.9	6.8
A -	7.1	6.9	6.9	6.9	7	6.9
P value	0.55	0.45	0.31		0.14	0.36
Disease type
CD	148 (57.6)	84 (32.7)	31 (12.1)	13 (5.1)	50 (19.4)	39 (15.2)
UC	92 (44.2)	55 (26.4)	6 (2.9)	3 (1.4)	15 (7.2)	32 (15.4)
P value	0.004	0.14	< 0.001	0.03	0.001	0.95
Disease localization
L1	66 (54.1)	34 (27.9)	13 (10.7)	5 (4.1)	25 (20.5)	19 (15.6)
L2	29 (60.4)	17 (35.4)	8 (16.7)	1 (2.1)	3 (6.3)	9 (18.8)
L3	50 (60.2)	31 (37.3)	9 (13.8)	6 (7.2)	22 (26.5)	10 (12)
P value	0.6	0.32	0.51		0.02	0.56
Disease behavior
B1	90 (60.8)	53 (35.8)	18 (12.2)	8 (5.4)	23 (15.6)	25 (16.9)
B2	27 (67.5)	12 (30)	5 (12.5)	1 (2.5)	14 (35)	6 (15)
B3	26 (47.3)	16 (29.1)	8 (14.5)	4 (7.3)	12 (21.8)	6 (10.9)
P value	0.1	0.59	0.9		0.02	0.57
Disease extension
E1	16 (32.7)	6 (12.2)	1 (2)	0	2 (4.1)	9 (18.4)
E2	32 (48.8)	19 (26)	2 (2.7)	2 (2.7)	6 (8.2)	12 (16.4)
E3	35 (62.5)	26 (46.4)	3 (5.4)	1 (1.8)	6 (10.7)	6 (10.7)
P value	0.008	< 0.001				0.51
Corticosteroid use
+	44 (80)	28 (50.9)	10 (18.2)	4 (7.3)	15 (27.3)	10 (18.2)
None	196 (47.8)	111 (27.1)	27 (6.6)	12 (2.9)	50 (12.2)	61 (14.9)
P value	< 0.001	< 0.001	0.003	0.097	0.003	0.52
AZA/MTX use
+	129 (64.5)	73 (36.5)	25 (12.5)	11 (5.5)	45 (22.5)	36 (18)
None	111 (41.9)	66 (24.5)	12 (4.5)	5 (1.9)	20 (7.5)	35 (13.2)
P value	< 0.001	0.007	0.002	0.03	< 0.001	0.15
Anti-TNF use
+	56 (69.1)	38 (46.9)	13 (16)	7 (8.6)	21 (26)	11 (13.6)
None	184 (47.9)	101 (26.3)	24 (6.3)	9 (2.3)	44 (11.5)	60 (15.6)
P value	0.001	< 0.001	0.003	0.01	0.002	0.64
Surgery
+	44 (62.9)	23 (32.9)	11 (15.7)	5 (7.19)	15 (21.4)	14 (20)
None	196 (49.6)	116 (29.4)	26 (6.6)	11 (2.8)	50 (12.6)	57 (14.4)
P value	0.041	0.55	0.009	0.07	0.55	0.23
CRP (mg/L)
< 5	109 (41.3)	70 (26.5)	7 (2.7)	3 (1.1)	31 (11.8)	29 (11)
> 5	120 (65.6)	63 (34.4)	29 (15.8)	12 (6.6)	30 (16.4)	39 (21.3)
P value	0.001	0.07	0.001	0.002	0.37	0.003

M: Male; F: Female; A+: Anemia present; A-: Anemia absent; IBD: Inflammatory bowel disease; L: Disease location (for Crohn’s disease); L1: Ileal disease; L2: Colonic disease; L3: Ileocolonic disease; L4: Upper gastrointestinal tract disease; B: Disease behavior (for Crohn’s disease); B1: Inflammatory disease; B2: Stricturing disease; B3: Penetrating disease; E: Disease extension (for ulcerative colitis); E1: Ulcerative proctitis; E2: Left-sided ulcerative colitis; E3: Extensive disease; SZP: Sulphasalazine; 5-ASA: 5-aminosalicyclate; AZA: Azathiopurine; MTX: Methotrexate; IFX: Infliximab; ADA: Adalimumab.

Table 5 Factors associated with anemia by logistic regression in patients with Crohn’s disease and ulcerative colitis at the diagnosis

	Odds ratio	95%CI	P value
All IBD patients
Sex (female)	3.19	2.07-4.91	< 0.001
Corticosteroids	3.21	1.52-6.80	0.002
AZA/MTX	2.28	1.48-3.49	< 0.001
Anti-TNF (INF/ADA)	2.32	1.30-4.11	0.004
Elevated CRP	2.75	1.78-4.24	< 0.001
Crohn’s disease
Sex (female)	4.10	2.19-7.68	< 0.001
Corticosteroids	4.06	1.27-12.96	0.018
AZA/MTX	2.30	1.26-4.20	0.006
Anti-TNF (INF/ADA)	2.34	1.20-4.53	0.012
Elevated CRP	3.05	1.67-5.58	< 0.001
Ulcerative colitis
Sex (female)	3.12	1.58-6.18	0.001
Corticosteroids	3.62	1.22-10.67	0.02
Elevated CRP	2.03	0.96-4.26	0.062
Disease extension	3.79	1.51-9.55	0.005

IBD: Inflammatory bowel disease; E: Disease extension (for ulcerative colitis); E1: Ulcerative proctitis; E2: Left-sided ulcerative colitis; E3: Extensive disease; AZA: Azathiopurine; MTX: Methotrexate; IFX: Infliximab; ADA: Adalimumab.