Risk factors associated with missed colorectal flat adenoma: A multicenter retrospective tandem colonoscopy study

Table 1 Demographic and clinical characteristics of patients with different types of colorectal adenomas n (%)

Patients	Total(n = 2093)	Flat adenoma(n = 177)	Flat and protruding adenoma (n = 514)	Protruding adenoma(n = 1402)	P value
Sex
Male	1369	91 (51.4)	329 (64.0)	949 (67.7)	< 0.001
Female	724	86 (48.6)	185 (34.0)	453 (32.3)	< 0.001
Age (mean ± SD, yr)		55.91 ± 12.68	59.30 ± 12.47	54.78 ± 13.24	< 0.001
Alarm symptoms	1621	134 (75.7)	388 (75.5)	1099 (78.4)	0.341
Diverticulosis	123	10 (5.6)	27 (5.3)	86 (6.1)	0.761
Family history of CRC	131	11 (6.2)	32 (6.2)	88 (6.3)	0.999
History of adenomas	475	40 (22.6)	139 (27.0)	296 (21.1)	0.023
History of abdominal surgery	149	3 (1.7)	35 (6.8)	111 (7.9)	0.010
Cases with adenomas ≥ 3 at first colonoscopy	458	8 (4.5)	222 (43.2)	228 (16.3)	< 0.001

Family history of colorectal cancer (CRC) was defined as the development of CRC in one first-degree relative < 50 years or at least two first-degree relatives 50-70 years; Diverticulosis is defined as the presence of ≥ 2 diverticula. Data are expressed as number (%) unless otherwise indicated.

Table 2 Clinicopathologic characteristics of different types of colorectal adenomas n (%)

Characteristic	Total (n = 4632)	Flat (n = 916)	Protruding (n = 3716)	χ2test	P value
Location				61.902	< 0.001
Rectum	1003	184 (20.1)	819 (22.0)
Left colon	2054	322 (35.2)	1732 (46.6)
Right colon	1575	410 (44.8)	1165 (31.4)
Size				95.954	< 0.001
< 6 mm	1223	353 (38.5)	870 (23.4)
6-9 mm	2159	391 (42.7)	1768 (47.6)
≥ 10 mm	1250	172 (18.8)	1078 (29.0)
Pathological classification				13.775	0.001
Tubular	3910	745 (81.3)	3165 (85.2)
Tubulovillous and villous	666	151 (16.5)	515 (13.9)
Serrated	56	20 (2.2)	36 (1.0)
Dysplasia				7.534	0.006
Low	4370	847 (92.5)	3523 (94.8)
High	262	69 (7.5)	193 (5.2)
Advanced adenoma				19.606	< 0.001
No	3322	711 (77.6)	2611 (70.3)
Yes	1310	205 (22.4)	1105 (29.7)

Table 3 “Per-adenoma” miss rates and the risk factors in detection of flat adenomas during colonoscopy n (%)

Risk factor	Total(n = 916)	Diagnosed(n = 510)	Missed(n = 406)	Univariate analysis		Multivariate analysis
				χ2test	P value	OR (95%CI)	P value
Patient-related
Age				9.021	0.003
< 60 (yr)	493	297 (60.2)	196 (39.8)			1
≥ 60 (yr)	423	213 (50.4)	210 (49.6)			2.062 (1.390-3.061)	< 0.001
Sex				1.586	0.208
Male	559	302 (54.0)	257 (46.0)
Female	357	208 (58.3)	149 (41.7)
Anesthesia				0.197	0.657
Yes	239	136 (56.9)	103 (43.1)
No	677	374 (55.2)	303 (44.8)
History of adenomas
Yes	243	129 (53.1)	114 (46.9)	0.899	0.343
No	673	381 (56.6)	292 (43.4)
Previous surgery				0.105	0.746
Yes	45	24 (53.3)	21 (46.7)
No	871	486 (55.8)	385 (44.2)
Diverticulosis				0.013	0.909
Yes	51	28 (54.9)	23 (45.1)
No	865	482 (55.7)	383 (44.3)
Numbers at first colonoscopy				0.163	0.686
< 3	580	320 (55.2)	260 (44.8)
≥ 3	336	190 (56.5)	146 (43.5)
Concomitance with protruding adenoma(s) at first colonoscopy				127.154	< 0.001
No	280	234 (83.6)	46 (16.4)			1
Yes	636	276 (43.4)	360 (56.6)			7.759 (4.420-13.618)	< 0.001
Bowel preparation				45.773	< 0.001
Good	757	460 (60.8)	297 (39.2)			1
Poor	159	50 (31.4)	109 (68.6)			4.389 (2.314-8.352)	< 0.001
Adenoma-related
Size				122.706	< 0.001
≥ 10 mm	172	159 (92.4)	13 (7.6)			1
6-9 mm	391	202 (51.7)	189 (48.3)			9.239 (4.306-19.824)	< 0.001
< 6 mm	353	149 (42.2)	204 (57.8)			19.613 (8.984-42.822)	< 0.001
Location				74.571	< 0.001
Rectum	184	152 (82.6)	32 (17.4)	6.81	0.0091	1
Left colon	322	175 (54.3)	147 (45.7)			2.866 (1.623-5.062)	< 0.001
Right colon	410	183 (44.6)	227 (55.4)			3.259 (1.819-5.838)	< 0.001
Advanced adenoma				113.850	< 0.001
Yes	205	181 (88.3)	24 (11.7)
No	711	329 (46.3)	382 (53.7)
Pathologic classification				74.745	< 0.001
Tubular	745	366 (49.1)	379 (50.9)
Tubulovillous and villous	151	132 (87.4)	19 (12.6)
Serrated	20	12 (60.0)	8 (40.0)
Procedure-related
Proficiency				28.18	< 0.001
> 1000 cases	585	363 (62.1)	222 (37.9)			1
500-1000 cases	234	109 (46.6)	125 (53.4)			2.219 (1.397-3.525)	0.001
< 500 cases	97	38 (39.2)	59 (60.8)			3.003 (1.568-5.754)	0.001
Specialty				6.86	0.009
Gastroenterologist	739	427 (57.8)	312 (42.2)
Non-gastroenterologist	177	83 (46.9)	94 (53.1)
Operative mode				4.862	0.027
One-person technique	721	415 (57.6)	306 (42.4)
Two-person technique	195	95 (48.7)	100 (51.3)
Withdrawal time				6.069	0.014
≥ 6 min	254	158 (62.2)	96 (37.8)			1
< 6 min	662	352 (53.2)	310 (46.8)			1.958 (1.276-3.006)	0.020

¹The comparison between the left and right colon.

Table 4 “Per-adenoma” miss rates and risk factors in detection of advanced flat adenomas during colonoscopy n (%)

Factor	Total (n = 205)	Diagnosed (n = 181)	Missed (n = 24)	χ2test	P value
Size				17.796	< 0.001
< 10 mm	33	22 (66.7)	11 (33.3)
≥ 10 mm	172	159 (92.4)	13 (7.6)
Location				11.838	0.003
Rectum	68	67 (98.5)	1 (1.5)	1.127	0.2881
Left colon	36	32 (88.9)	4 (11.1)
Right colon	101	82 (81.2)	19 (18.8)
Pathologic classification				0.025	0.874
Tubular	57	50 (87.7)	7 (12.3)
Tubulovillous and villous	148	131 (88.5)	17 (11.5)
Age (yr)				1.157	0.282
< 60	98	89 (90.8)	9 (9.2)
≥ 60	107	92 (86.0)	15 (1.4)
Bowel preparation				13.815	< 0.001
Good	162	150 (92.6)	12 (7.4)
Poor	43	31 (72.1)	12 (27.9)
Proficiency				1.078	0.583
> 1000 cases	135	120 (88.9)	15 (11.1)
500-1000 cases	55	49 (89.1)	6 (10.9)
< 500 cases	15	12 (80.0)	3 (20.0)
Specialty				6.167	0.013
Gastroenterologist	156	146 (93.6)	10 (6.4)
Non- gastroenterologist	49	35 (71.4)	14 (28.6)
Operative mode				2.272	0.132
One-person technique	161	145 (90.1)	16 (9.9)
Two-person technique	44	36 (81.8)	8 (18.2)
Withdrawal time
≥ 6 min	145	129 (89.0)	16 (11.0)	0.217	0.641
< 6 min	60	52 (86.7)	8 (13.3)

¹Comparison between the left and right colon.