Prospective evaluation of bowel function and quality of life after colon cancer surgery – is it time for routine screening for late sequelae?

Figures & data

Table 2. Change in bowel function from 3 m to 12 m after surgery, for patients undergoing a right-sided or a left-sided colon resection (n = 662).

	Right-sided colon resection (n = 410)				Left-sided colon resection (n = 252)
	Comparison of 3 m versus 12 m				Comparison of 3 m versus 12 m
Bowel function scores and items
	3 m	12 m	Difference (95% CI)	p	3 m	12 m	Difference (95%CI)	p
Bowel function scores and single items
Bristol Stool Chart, n (%)
1–2 (hard)	24 (6.2)	21 (5.4)	−0.8 (−4.2; 2.6)	0.63	25 (10.3)	24 (9.8)	−0.4 (−5.7; 4.9)	0.87
3–5 (normal)	291 (75.0)	289 (74.5)	−0.5 (−5.7; 4.7)	0.84	199 (81.6)	207 (84.8)	3.3 (−2.9; 9.5)	0.27
6–7 (loose)	73 (18.8)	78 (20.1)	1.3 (−3.3; 5.9)	0.56	20 (8.2)	13 (5.3)	−2.9 (−6.6; 0.8)	0.09
PAC-SYM, median (IQR)
Abdominal	0.5 (0.0–1.0)	0.25 (0.0–1.0)	0.00 (−0.05; 0.05)*	0.91	0.5 (0.0–0.8)	0.5 (0.0–0.8)	−0.01 (−0.08; 0.06)*	0.63
Rectal	0.0 (0.0–0.5)	0.0 (0.0–0.7)	0.07 (0.02; 0.13)*	0.005	0.0 (0.0–0.3)	0.0 (0.0–0.3)	−0.01 (−0.08; 0.05)*	0.64
Stool	0.4 (0.2–0.8)	0.4 (0.2–1.0)	0.02 (−0.03; 0.08)*	0.30	0.8 (0.4–1.2)	0.8 (0.4–1.4)	0.02 (−0.05; 0.10)*	0.93
Total	0.4 (0.2–0.8)	0.4 (0.2–0.8)	0.02 (−0.02; 0.06)*	0.37	0.5 (0.3–0.8)	0.5 (0.3–0.9)	0.00 (−0.05; 0.05)*	0.91
LARS Score items
Flatus incontinence, n (%)
Never	155 (38.6)	133 (33.1)	−5.5 (−10.5; −0.4)	0.026	63 (25.6)	60 (24.4)	−1.2 (−7.1; 4.7)	0.66
<1 per week	120 (29.9)	151 (37.6)	7.7 (2.0; 13.4)	0.008	67 (27.2)	90 (36.6)	9.4 (1.5; 17.2)	0.015
>/= 1 per week	127 (31.6)	118 (29.4)	−2.2 (−6.7; 2.2)	0.30	116 (47.2)	96 (39.0)	−8.1 (−15.4; −0.9)	0.022
Incontinence liquid stool, n (%)
Never	250 (62.3)	220 (54.9)	−7.5 (−13.5; −1.9)	0.007	155 (63.0)	169 (68.7)	5.7 (−0.1; 12.2)	0.07
<1 per week	112 (27.9)	146 (36.4)	8.5 (2.9; 14.1)	0.002	63 (25.6)	70 (28.5)	2.9 (−4.1; 9.8)	0.39
>/= 1 per week	39 (9.7)	35 (8.7)	−1.0 (−4.5; 2.5)	0.55	28 (11.4)	7 (2.9)	−8.5 (−12.9; −4.1)	<0.001
Bowel movement frequency, n (%)
>/= 4 daily	33 (8.2)	36 (9.0)	0.8 (−2.3; 3.9)	0.61	34 (13.7)	28 (11.3)	−2.4 (−6.8; 2.0)	0.24
1–3 daily	307 (76.6)	305 (76.1)	−0.5 (−5.2; 4.2)	0.83	176 (71.0)	182 (73.4)	2.4 (−4.0; 8.8)	0.43
<1 daily	61 (15.2)	60 (15.0)	−0.3 (−4.3; 3.8)	0.90	38 (15.3)	38 (15.3)	0 (−5.3; 5.3)	1.00
Fragmented defaecation, n (%)
Never	179 (44.9)	164 (41.1)	−3.8 (−8.6; 1.1)	0.11	94 (38.2)	94 (38.2)	0 (−6.9; 6.9)	1.00
<1 per week	111 (27.8)	121 (30.3)	2.5 (−3.4; 8.4)	0.38	85 (34.6)	93 (37.8)	3.25 (−4.5; 11.0)	0.39
>/= 1 per week	109 (27.3)	114 (28.6)	1.3 (−3.9; 6.4)	0.62	67 (27.2)	59 (24.0)	−3.25 (−9.9; 3.4)	0.31
Urgency, n (%)
Never,	142 (35.2)	122 (30.2)	−5.0 (−10.1; 0.2)	0.048	92 (37.1)	119 (48.0)	10.9 (4.4; 17.4)	<0.001
<1 per week	144 (35.6)	149 (36.9)	1.2 (−4.8; 7.3)	0.68	73 (29.4)	74 (29.8)	0.4 (−6.8; 7.6)	0.91
>/= 1 per week	118 (29.2)	133 (32.9)	3.7 (−1.4; 8.9)	0.14	83 (33.5)	55 (22.2)	−11.3 (−18.1; −4.5)	< 0.001
St. Mark’s Faecal Incontinence Score, median (IQR)
Total score	4 (1–7)	4 (0.5–7)	−0.10 (−0.47; 0.27)*	0.77	4 (1.5; 7.5)	3 (0.5; 7.0)	−0.61 (−1.10; −0.13)*	0.008
Night-time defaecation^a, n (%)
Never	332 (83.0)	331 (82.8)	−0.3 (−4.3; 3.8)	0.90	176 (71.5)	193 (78.5)	6.9 (0.5; 13.4)	0.027
<1 week	44 (11.0)	45 (11.3)	0.3 (−3.7; 4.2)	0.89	38 (15.5)	34 (13.8)	_1.6 (−7.7; 4.4)	0.57
>/= 1 week	24 (6.0)	24 (6.0)	0.00 (−2.7; 2.7)	1.00	32 (13.0)	19 (7.7)	−5.3 (−9.6; −1.0)	0.009
Use of medication and fibre supplements
Constipating agents, n (%) (St. Mark’s Faecal Incontinence Score item)
Yes	23 (5.9)	22 (5.6)	−0.3 (−3.0; 2.5)	0.84	10 (4.1)	11 (4.5)	0.40 (−3.5; 4.3)	0.82
Laxatives^a, n (%)
Yes	65 (16.5)	54 (13.7)	−2.8 (−6.2; 0.6)	0.09	47 (19.4)	50 (20.7)	−1.2 (−4.1; 6.6)	0.62
Fibre supplements^a, n (%)
Yes	98 (24.8)	101 (25.6)	0.8 (−3.6; 5.1)	0.71	72 (29.4)	66 (26.9)	−2.5 (−8.3; 3.4)	0.38
Self-rated bowel function and quality of life
Self-rated bowel function^a, n (%)
Very good/good	278 (68.6)	258 (63.7)	−4.9 (−10.1; 0.2)	0.047	152 (61.3)	155 (62.5)	1.2 (−5.6; 8.0)	0.71
Acceptable	101 (24.9)	120 (29.6)	4.7 (−0.8; 10.2)	0.08	76 (30.7)	77 (31.1)	0.4 (−6.9; 7.7)	0.91
Bad/very bad	26 (6.4)	27 (6.7)	0.3 (−2.7; 3.2)	0.86	20 (8.1)	16 (6.5)	−1.6 (−5.5; 2.3)	0.37
Impact of bowel function on quality of life^a, n (%)
Some/a lot^b	70 (17.3)	65 (16.1)	−1.2 (−5.5; 3.0)	0.54	48 (19.3)	47 (18.9)	−0.4 (−6.2; 5.4)	0.88
EQ5D-5L, median (IQR)
Index value	0.95 (0.88; 1.00)	0.95 (0.88; 1.00)	0.00 (−0.01; 0.01)*	0.80	0.95 (0.91; 1.00)	0.96 (0.90; 1.00)	0.01 (−0.02; 0.01)*	0.70

3 m/12m: 3/12 months after surgery;

PAC-SYM: Patient Assessment of Constipation Symptoms;

LARS Score: Low Anterior Resection Syndrome Score;

EQ5D-5L: EuroQol 5 Dimensions – 5 Levels.

Patients with stomas at 3 m and/or 12 m were not included (n = 46).

aad hoc items.

^bversus ‘not at all/a little’. *Difference between means (95% CI) (see Method section).

Red: Worsening from 3 m to 12 m, p < 0.05.

Green: Improvement from 3 m to 12 m, p < 0.05.

Table 3. Bowel symptoms in right- and left-sided colon resections 12 months after surgery (n = 677).

	Right-sided colon	Left-sided colon	Difference (95% CI)	p
Bowel function scores and single items
Bristol stool chart, n (%)
1–2 (hard)	24 (6.0)	26 (10.2)	−4.2 (−8.6; 0.1)	0.046
3–5 (normal)	298 (74.0)	216 (84.7)	−10.8 (−16.9; −4.6)	0.001
6–7 (loose)	81 (20.1)	13 (5.1)	15.0 (10.3; 19.8)	<0.001
PAC SYM, median (IQR)
Abdominal	0.25 (0.00–1.00)	0.50 (0.00–0.75)	−0.25 (−0.34; −0.16)	<0.001*
Rectal	0.00 (0.00–0.67)	0.00 (0.00–0.67)	0.00 (−0.12; 0.12)	1.00
Stool	0.40 (0.20–1.00)	0.80 (0.40–1.40)	−0.40 (−0.50; −0.30)	<0.001*
Total	0.42 (0.16–0.83)	0.50 (0.25–0.92)	−0.08 (−0.17; 0.01)	0.07
LARS Score items
Flatus incontinence, n (%)
Never	134 (32.9)	62 (24.0)	8.9 (2.0,15.8)	0.01
<1 per week	154 (37.8)	96 (37.2)	0.6 (−6.9; 8.2)	0.87
>/= 1 per week	119 (29.2)	100 (38.8)	−9.5 (−16.9; −2.1)	0.01
Incontinence liquid stool, n (%)
Never	224 (55.0)	178 (68.7)	−13.7 (−21.1; −6.3)	<0.001
<1 per week	148 (36.4)	73 (28.2)	8.2 (1.0; 15.4)	0.03
>/= 1 perweek	35 (8.6)	8 (3.1)	5.5 (2.1; 9.0)	0.005
Bowel movement frequency, n (%)
>/= 4	36 (8.8)	32 (12.4)	−3.6 (−8.5; 1.3)	0.13
1–3	310 (75.8)	188 (72.9)	2.9 (−3.9; 9.8)	0.40
<1	63 (15.4)	38 (14.7)	0.7 (−4.9; 6.2)	0.81
Fragmented defaecation, n (%)
Never	165 (40.6)	101 (38.9)	1.8 (−5.8; 9.4)	0.64
<1 per week	126 (31.0)	97 (37.3)	−6.3 (−13.7; 1.1)	0.09
>/= 1 per week	115 (28.3)	62 (23.9)	4.5 (−2.3; 11.3)	0.20
Urgency, n (%)
Never	122 (29.8)	122 (46.9)	−17.2 (−24.7; −9.7)	<0.001
<1 per week	152 (37.1)	79 (30.4)	6.7 (−0.6; 14.0)	0.08
>/= 1 per week	136 (33.2)	59 (22.7)	10.5 (3.7; 17.3)	0.004
St. Mark’s Incontinence Score, median (IQR)
Total score	4.00 (0.50–7.00)	3.5 (0.5–7.00)	0.5 (−0.20; 1.20)	0.16
Night-time defaecation^a, n (%)
Never	340 (82.9)	200 (76.9)	6.0 (−0.3; 12.3)	0.06
<1 week	45 (11.0)	36 (13.9)	−2.9 (−8.1; 2.3)	0.27
>/= 1 week	25 (6.1)	24 (9.2)	−3.1 (−7.4; 1.1)	0.13
Use of medication and fibre supplements
Constipating agents, n (%) (St. Mark’s Faecal Incontinence Score item)
Yes	22 (5.5)	13 (5.0)	0.4 (−3.0; 3.9)	0.81
Laxatives^a, n (%)
Yes	57 (14.1)	51 (20.0)	−5.9 (−11.9; 0.1)	0.05
Fibre supplements^a, n (%)
Yes	104 (25.5)	70 (27.1)	−1.6 (−8.5; 5.2)	0.64
Self-rated bowel function and quality of life
Self-rated bowel function^a, n (%)
Very good/good	263 (63.7)	163 (62.7)	1.1 (−6.4; 8.6)	0.76
Acceptable	122 (29.6)	81 (31.2)	−1.5 (−8.7; 5.6)	0.67
Bad/very bad	27 (6.6)	16 (6.2)	0.4 (−3.4; 4.2)	0.84
Impact of bowel function on quality of life^a, n (%)
Some/a lot^b	68 (16.5)	48 (18.5)	−2.2; (−8.2; 3.7)	0.46
EQ5D-5L, median (IQR)
EQ5D index value	0.95 (0.88; 1.00)	0.96 (0.90; 1.00)	−0.01 (−0.03; 0.02)	0.59

Patients with a stoma at 12 months were not included (n = 31).

PAC-SYM: Patient Assessment of Constipation Symptoms; LARS Score: Low Anterior Resection Syndrome Score; EQ5D-5L: EuroQol 5 Dimensions – 5 Levels instrument.

^aad hoc items.

^bversus ‘not at all/a little’. *Clinically irrelevant difference.

Yellow: Worse symptoms in right-sided – than in left-sided resected patients, p < 0.05.

Blue: Worse symptoms in left-sided – than in right-sided resected patients, p < 0.05.

Figure 1. Flow chart of the in-/excluded patients.

Table 1. Patient characteristics (n = 708).

	Right-sided colon resection	Left-sided colon resection
	n = 423 (59.7 %)	n = 285 (40.3 %)
Male gender, n (%)	210 (49.7)	165 (57.9)
Age at surgery, mean (SD)	71.97 (9.88)	68.06 (11.19)
Type of surgery, n (%)
Right-sided hemicolectomy	344 (81.5)	–
Extended right-sided hemicolectomy	79 (18.7)	–
Left-sided hemicolectomy	–	77 (27.0)
Sigmoid resection	–	208 (73.0)
Body Mass Index, mean (SD)	26.65 (4.90)	27.01 (4.89)
WHO Performance Status, n (%)
0	283 (68.5)	209 (74.6)
1	104 (25.2)	57 (20.4)
2–4	26 (6.3)	14 (5.0)
Charlson Comorbidity Score, n (%)
0	161 (39.0)	124 (43.8)
1–2	190 (45.9)	120 (42.4)
>2	63 (15.2)	39 (13.8)
pUICC stage, n (%)
0–2	273 (66.6)	179 (63.9)
3	120 (29.3)	79 (28.2)
4	17 (4.15)	22 (7.9)
Surgical access, n (%)
Laparotomy (incl. converted)	82 (19.4)	30 (10.6)
Laparoscopy	340 (80.6)	254 (89.4)
Post-operative chemotherapy, n (%)	96 (22.7)	87 (30.5)
Stoma at 3 months and/or 12 months after surgery, n (%)	13 (3.1)	33 (11.6)
Grade b/c anastomotic leak^a, n (%)	6 (1.4)	6 (2.1)

WHO: World Health Organisation, pUICC : pathological Union for International Cancer Control.

^aSymptomatic leakage requiring active therapeutic treatment.

Table 4. Associations between demographic/clinical variables and QoL (N = 701).

	Affected QoL*	Adjusted OR (95 %CI)^b	p
Age </= 64 years (n = 173)	27.2 %	2.58 (1.63; 4.10)	<0.001
Age > 64 years (n = 528)	15.3 %	Ref
Female (n = 331)	21.8%	1.54 (0.99; 2.31)	0.06
Male (n = 370)	15.1%	Ref
BMI < 25 (n = 270)	19.3%	1.11 (0.74; 1.70)	0.63
BMI >/= 25 (n = 421)	17.6 %	Ref
Left-sided (n = 282)	20.6 %	1.27 (0.84; 1.96))	0.27
Right-sided (n = 419)	16.7 %	Ref
Laparotomy (n = 110)	20.9 %	1.33 (0.76; 2.34)	0.32
Laparoscopy (n = 589)	17.8 %	Ref
No post-operative chemo (n = 518)	19.9 %	1.47 (0.76; 2.87)	0.25
Post-operative chemo (n = 183)	13.7 %	Ref
pUICC 0–2 (n = 449)	19.8 %	3.28 (0.88; 12.17)	0.08
pUICC 3 (n = 196)	15.8 %	2.79 (0.77; 10.12)	0.12
pUICC 4 (n = 38)	7.9 %	Ref
WHO performance 0–1 (n = 648)	18.1 %	Ref	0.49
WHO performance 2–4 (n = 40)	25.0 %	1.36 (0.56; 3.30)
Charlson comorbidity score 0–1 (n = 385)	16.4 %	Ref	0.09
Charlson comorbidity score > 1 (n = 311)	20.9 %	1.44 (0.95; 2.18)
No stoma at 12 m (n = 670)	17.2 %	Ref	<0.001
Stoma at 12 m (n = 31)	41.9 %	4.32 (1.9 (9.83)

^aPatients responding ‘somewhat’ or ‘very much’ to the question ‘Overall, how much does your bowel function affect your QoL?’ at 12 m.

^bn = 663.

p-values <0.05 are shown in bold font.

Table A1. PROMs included in the survey.

Tool	Description	Interpretation/notes
The Bristol Stool Form Scale (25,26)	A tool combining graphical illustrations with text to classify stool consistency into seven types.	Types 1 and 2 are considered abnormally hard stools; types 3, 4 and 5 are considered normal; whereas types 6 and 7 are considered abnormally loose/liquid stools
The Patient Assessment of Constipation Symptoms (PAC-SYM) (27)	Consists of 12 items assigned to three subscales and a total score: Abdominal Symptoms (four items; abdominal discomfort, pain, bloating and cramps), Rectal Symptoms (three items; painful bowel movements, rectal burning and rectal bleeding/tearing) and Stool Symptoms (five items; incomplete bowel movements, hard stools, small portions, straining and false alarm), and Total Score (all 12 items). Each item is measured on a five-point Likert-like scale scored from 0 (absent) to 4 (very severe).	Lower scores equal a lower symptom severity. The minimal important difference (MID) for PAC-SYM has previously been established to be 0.6 points (28)
The Low Anterior Resection Syndrome Score (LARS score) (29)	Consists of five items, which have proven to be strongly correlated with bowel-related impact on QoL in RC patients. The response options for items covering incontinence for flatus and liquid stool, fragmented defaecation and faecal urgency are ‘Never, < 1/week, </= 1 per week’, whereas the response options for daily frequency of bowel movements are ‘>/= 4, 1–3, <1’.	A summary score, based on a weighted scoring system, facilitates categorisation into three groups: no, minor, major LARS. However, the scoring system was developed specifically for and validated in cohorts of RC patients only. Therefore, the summarised score was not analysed in the present study.
The St. Marks Faecal Incontinence Score/Vaizey Score (30)	Measures faecal incontinence severity by means of four items (Solid/liquid/gas incontinence and lifestyle alteration) scored on a five-point Likert-like scale based on the frequency of the symptom (‘Never’/0 points, ‘Always’/4 points); and, in addition, the use of pads (‘Yes’/2 points), usage of anti-diarrhoeal medication (‘Yes’/2 points) and urgency symptoms (Yes/4 points). The total score ranges from 0 to 24.	Lower scores equal a lower symptom severity.
		The original score was initially developed to be completed by a clinician. The score used in this study is an adapted version which can be completed by the patients. It has not yet been formally validated.
EuroQoL 5 Dimensions − 5 levels (EQ5D-5L) (31)	A generic QoL questionnaire consisting of five items measuring mobility, self-care, usual activities, pain/discomfort and anxiety/depression. The EQ5D-5L establishes five categories for each item (from no problems to extreme problems).	Higher scores equal better QoL. The minimally important difference of the EQ-5D utility score has been reported to be 0.08 among cancer patients (32,33)
Ad hoc items	Single items regarding night-time defaecation (‘Never, < 1/week, </= 1 per week’) and use of laxative agents and fibre supplements (Yes/No).
	Two questions regarding self-rated bowel function and impact on QoL:
	‘How would you evaluate your bowel function over the past four weeks?’ (Very good, good, acceptable, poor, very poor)
	‘Overall, how much does your bowel function affect your quality of life?’ (Not at all, a little, somewhat, very much).

Data availability statement

The data that support the findings of this study are available from the corresponding author, TJ, upon reasonable request.