Endoscopy-based management decreases the risk of postoperative recurrences in Crohn’s disease

Table 1 Baseline characteristics of the 161 included Crohn’s disease patients at the time of surgery n (%)

Mean age at the time of surgery (yr)	36.4 ± 13.4	Adalimumab	22 (13.7)
Mean age at diagnosis (yr)	28.7 ± 13.1	Anti-TNF naive at the time of surgery	37 (23.0)
Median disease duration (yr) (IQR)	5.8 (2.0–11.7)	Type of surgery
Female gender	93 (57.8)	Ileocecal resection	76 (47.2)
Mean weight (kg)	60.2 ± 14.8	Ileal resection	21 (13.1)
Mean body mass index (kg/m²)	21.5 ± 4.9	Ileo-colectomy	14 (8.7)
Active smoker	53 (32.9)	Partial colectomy	31 (19.2)
Familial history of IBD	20 (12.4)	Subtotal colectomy	8 (5.0)
Previous appendectomy	67 (41.6)	Total colectomy	9 (5.6)
Previous intestinal resection	50 (31.1)	Abdomino-perianal amputation	2 (1.2)
Montreal classification		Site of anastomosis
Age at diagnosis		Ileo-colic	91 (66.4)
A1	15 (9.3)	Ileo-rectal	9 (6.6)
A2	116 (72.1)	Ileo-ileal	21 (15.3)
A3	28 (17.4)	Colo-colonic	31 (22.6)
Crohn’s disease location		Colo-rectal	7 (5.1)
L1	64 (39.8)	Stomia
L2	21 (13.0)	None	113 (70.2)
L3	75 (46.6)	Transitory	39 (24.2)
L4	18 (11.2)	Definitive	9 (5.6)
Crohn’s disease behaviour		Surgical technic of anastomosis
B1	12 (7.4)	Stapled	46 (43.8)
B2	75 (46.6)	Handsewn	59 (56.2)
B3	74 (46.0)	Type of anastomosis
Perianal lesions	69 (42.8)	Side-to-end	18 (18.0)
Anal ulceration, fissure	15 (9.3)	Side-to-side	54 (54.0)
Fistula/abscess	54 (33.5)	End-to-end	28 (28.0)
Medication at the time of surgery		Mean length of ileal resection (cm)	18.1 ± 17.1
5-ASA	24 (14.9)	Mean length of colonic resection (cm)	14.3 ± 17.7
Steroids	38 (23.6)	Mean length of digestive resection (cm)	31.6 ± 18.8
Budesonide	9 (5.6)	Perioperative complications	25 (16.8)
Thiopurines	36 (22.4)	Free margin resection	21 (17.1)
Methotrexate	5 (3.1)	Granuloma	47 (40.5)
Infliximab	15 (9.3)	Median CRP level, mg/L (IQR)	17.0 (3.8-61.0)

IQR: Interquartile; CRP: C-reactive protein; TNF: Tumor necrosis factor; IBD: Inflammatory bowel disease.

Table 2 Univariate analysis of risk factors for endoscopic postoperative recurrence in Crohn’s disease

	Median time to endoscopic POR (mo)	HR [95%CI]	P value
Age		1.00 [0.99-1.00]	0.2
Age
< 35 yr	41.4	Reference
≥ 35 yr	24.0	1.26 [0.86-1.84]	0.23
Age at diagnosis
≤ 16 yr	38.1	Reference
16-40 yr	34.6	0.88 [0.47-1.67]	0.71
≥ 40 yr	17.6	1.41 [0.60-2.63]	0.53
Tobacco use
Non-smoker	38.1	Reference
Active smoker	27.9	1.28 [0.77-1.70]	0.49
Previous intestinal resection
No	43.5	Reference
Yes	20.5	1.22 [0.98-2.15]	0.06
Total resection length > 50 cm
No	20.5	Reference
Yes	30.2	0.98 [0.56-1.73]	0.7
Disease behavior (Montreal classification)
B1	-	Reference
B2	43.5	1.30 [0.46-3.75]	0.62
B3	22.6	1.34 [0.47-3.80]	0.58
Fistulizing Crohn’s disease (B3)
No	29.3	Reference
Yes	22.6	1.06 [0.73-1.53]	0.75
Perianal lesions
No	34.6	Reference
Yes	19.2	1.18 [0.82-1.71]	0.37
Type of perianal lesions
Non-fistulizing lesions	33.4	Reference
Fistula, abscess	20.5	1.10 [0.75-1.60]	0.23
Disease duration		1.00 [0.99-1.01]	0.77
Ileal resection > 50 cm
No	25.9	Reference
Yes	114.5	0.58 [0.21-1.60]	0.29
Prior exposure to anti-TNF therapy before surgery
No	41.5	Reference
Yes	8.0	3.91 [1.80-5.90]	< 0.001
Thiopurines therapy in prevention of endoscopic postoperative recurrence
No	43.5	Reference
Yes	43.7	1.07 [0.69-1.65]	0.75
Anti-TNF therapy in prevention of endoscopic postoperative recurrence
No	41.4	Reference
Yes	20.5	1.28 [0.78-2.13]	0.55
Period of surgery
1986-1999		Reference
2000-2015		1.00 [0.54-1.84]	0.99

CRP: C-reactive protein; TNF: Tumor necrosis factor.

Table 3 Univariate analysis of risk factors for clinical postoperative recurrence in Crohn’s disease

	Median time to clinical POR (mo)	HR [95%CI]	P value
Age		1.00 [0.99-1.01]	0.4
Age
< 35 yr	45.2	Reference
≥ 35 yr	30.2	1.25 [0.84-1.85]	0.27
Age at diagnosis
≤ 16 yr	38.1	Reference
16-40 yr	48.0	0.81 [0.43-1.54]	0.52
≥ 40 yr	30.2	1.03 [0.48-2.23]	0.93
Tobacco use
Non-smoker	45.2	Reference
Active smoker	43.7	1.00 [0.66-1.53]	0.98
Previous intestinal resection
No	51.0	Reference
Yes	26.6	1.62 [1.07-2.44]	0.02
Total resection length > 50 cm
No	38.1	Reference
Yes	33.4	1.20 [0.66-2.16]	0.55
Disease behavior (Montreal classification)
B1	84.5	Reference
B2	54.5	1.39 [0.48-4.00]	0.53
B3	28.9	1.61 [0.56-4.56]	0.37
Fistulizing Crohn’s disease (B3)
No	58.2	Reference
Yes	28.9	1.21 [0.81-1.78]	0.34
Perianal lesions
No	54.5	Reference
Yes	26.9	1.26 [0.85-1.86]	0.24
Type of perianal lesions
Non-fistulizing lesions	54.5	Reference
Fistula, abscess	20.5	1.46 [1.01-2.16]	0.05
Disease duration		1.00 [0.99-1.01]	0.31
Ileal resection > 50 cm
No	33.4	Reference
Yes	59.5	0.72 [0.26-2.02]	0.54
Prior exposure to anti-TNF therapy before surgery
No	48.0	Reference
Yes	24.0	2.64 [1.24-4.33]	0.007
Thiopurines therapy in prevention of clinical postoperative recurrence
No	44.8	Reference
Yes	43.7	1.14 [0.74-1.76]	0.53
Anti-TNF therapy in prevention of clinical postoperative recurrence
No	48.6	Reference
Yes	29.3	1.39 [0.88-2.20]	0.16
Period of surgery
1986-1999		Reference
2000-2015		1.71 [1.12-2.63]	0.013

CRP: C-reactive protein; TNF: Tumor necrosis factor.

Table 4 Univariate analysis of risk factors for surgical postoperative recurrence in Crohn’s disease

	Median time to surgical POR (mo)	HR [95%CI]	P value
Age		1.00 [0.99-1.01]	0.29
Age
< 35 yr	218.3	Reference
≥ 35 yr	131.6	1.32 [0.77-2.26]	0.30
Age at diagnosis
≤ 16 yr		Reference
16-40 yr	144.0	1.37 [0.42-4.42]	0.60
≥ 40 yr	108.6	1.73 [0.45-6.54]	0.42
Tobacco use
Non-smoker	136.2	Reference
Active smoker	173.4	0.84 [0.46-1.52]	0.56
Previous intestinal resection
No	173.4	Reference
Yes	108.6	1.74 [1.01-3.00]	0.04
Total resection length > 50 cm
No	136.2	Reference
Yes	120.0	1.50 [0.67-3.34]	0.32
Disease behavior (Montreal classification)
B1		Reference
B2	162.1	3.93 [0.52-29.33]	0.18
B3	128.8	5.71 [0.77-42.23]	0.09
Fistulizing Crohn’s disease (B3)
No	165.4	Reference
Yes	128.8	1.78 [1.04-3.05]	0.03
Perianal lesions
No	136.2	Reference
Yes	151.1	0.99 [0.58-1.69]	0.97
Type of perianal lesions
Non-fistulizing lesions	156.9	Reference
Fistula, abscess	144.0	1.14 [0.66-1.97]	0.63
Disease duration		1.00 [0.99-1.01]	0.67
Ileal resection > 50 cm
No	136.2	Reference
Yes	120.0	1.23 [0.29-5.16]	0.78
Prior exposure to anti-TNF therapy before surgery
No	151.1	Reference
Yes	.	1.62 [0.92-7.08]	0.07
Thiopurines therapy in prevention of surgical postoperative recurrence
No	144.0	Reference
Yes	151.1	0.91 [0.50-1.65]	0.75
Anti-TNF therapy in prevention of surgical postoperative recurrence
No	156.9	Reference
Yes	136.2	2.09 [1.14-3.81]	0.02
Period of surgery
1986-1999		Reference
2000-2015		1.85 [1.22-2.80]	0.004

CRP: C-reactive protein; TNF: Tumor necrosis factor.

Table 5 Step-up strategies in patients experiencing endoscopic postoperative recurrence in the endoscopic management-based group

Number of patient	Treatment before endoscopic evaluation	Rutgeerts’ score	Treatment after endoscopic evaluation
1	None	i2	AZA
2	AZA	i3	IFX
3	AZA	i4	IFX
4	AZA	i2	AZA
5	AZA	i2	AZA (increased dose)
6	5-ASA	i4	IFX
7	ADA eow	i3	ADA ew
8	None	i4	ADA
9	5-ASA	i4	IFX + MTX
10	AZA	i4	IFX
11	AZA	i2	AZA (increased dose)
12	IFX + MTX	i3	IFX (increased dose) + MTX
13	ADA eow	i4	ADA ew
14	None	i2	AZA
15	None	i3	ADA
16	None	i2	AZA
17	None	i2	AZA
18	ADA eow	i3	ADA ew

AZA: Azathioprine; MTX: Methotrexate; IFX: Infliximab; ADA: Adalimumab; eow: Every other week; ew: Every week.