INTRODUCTION
Colorectal cancer (CRC) is a major health problem worldwide, being the third most common cancer and the second leading cause of cancer death (1 2 3–6 7,8 9,10
Recently, several studies have reported that Endocuff, full-spectrum endoscopy, water-aided colonoscopy, and repeat examination including retroflection or second forward view can effectively increase the ADR in the proximal or whole colon (11–15 second forward view and standard examination of the proximal colon on ADR remain limited. To date, only a randomized controlled trial (RCT) and a clinical study are available (14,15 16
METHODS
Study design
This prospective, single-center, RCT was conducted by the Third People's Hospital of Jingdezhen, Jiangxi Province, from June 2021 to June 2022. The study protocol was approved by the ethics committees of the participating hospitals. Informed consent was obtained from all the study participants. All authors had full access to the data in the study and had final responsibility for the decision to submit for publication. The trial was registered in the Chinese Clinical Trial Registration (chictr.org.cn
Study population
Consecutive patients aged 18–80 years undergoing colonoscopy for screening, surveillance, or diagnostic purposes were recruited. The categories were defined as follows: (i) screening: asymptomatic patients undergoing first-time colonoscopy; (ii) surveillance: patients who had undergone a previous colonoscopy (irrespective of the presence or absence of polyps) in the context of CRC screening or postpolypectomy surveillance; and (iii) diagnostic: patients undergoing colonoscopy for any symptomatic indication (abdominal pain, blood per rectum, constipation, chronic diarrhea, etc). Symptomatic patients with both surveillance and diagnostic indications were considered to have the surveillance indications if they met the surveillance criteria. Patients were excluded if they failed cecal intubation, previous colorectal resection, inadequate bowel preparation quality (Boston Bowel Preparation Scale [BBPS] scores <2 in any segment of the colon) (17
Colonoscopy procedures and randomization
High-definition colonoscopes (CF-HQ290I, CF-H290I, PCF-Q260AZI; Olympus, Tokyo, Japan) were used for all procedures. Colonoscopies were performed by 1 of 3 endoscopists (E1, E2, and E3). Image enhancement (narrow-band imaging and indigo carmine staining) does not allow routine use for polyp detection. Other additional techniques (e.g., water-aided colonoscopy, antispasmodics, retroflection, or position change) were not used during a colonoscopy.
All patients received split-dose bowel preparation with 3 L of polyethylene glycol electrolyte solution (Jiangxi Hygecon Pharmaceutical, Jiangxi, China). Most colonoscopies (90.8%) were performed with the patient under general anesthesia with propofol. The colonoscope was inserted in a standard manner. After successful insertion in the cecum, the colonoscope was slowly withdrawn to the splenic flexure and the mucosa was carefully observed. The polyps that were found were removed for histopathologic examination. When the colonoscope completed the first forward view examination of the proximal colon (defined as proximal to the splenic flexure), patients were randomly assigned to either the intervention or the control group. The randomization sequence was computer-generated and concealed in sequentially numbered sealed opaque envelopes, and at this moment, the envelope was opened. For patients in the intervention group, the colonoscope was advanced to the cecum again, additional polyps were removed from the proximal colon during the second withdrawal, and the remainder of the colon was examined in a standard manner. For patients in the control group, the colonoscope was withdrawn directly from the splenic flexure to the rectum, and polyps that were found were removed. Multiple diminutive hyperplastic polyps (≤5 mm) in the sigmoid colon and rectum were not subjected to removal, and only 1 representative polyp biopsy was analyzed. We recorded all adverse events at the time of the colonoscopy and for 1 week thereafter.
The cecal intubation time and withdrawal time were recorded by an assistant with a stopwatch. The time for polypectomy and biopsy was excluded from the withdrawal time.
Polyp data
The polyp size was estimated by comparison with open biopsy forceps or snares of known dimensions. The colon was categorized as the right-sided colon, transverse colon, or left-sided colon (17 18 19
Outcome measures
The primary outcome measure was per-patient proximal colon ADR, defined as the proportion of patients with at least 1 adenoma found in the proximal colon. The secondary outcome measures included per-patient whole-colon ADR and polyp detection rate (PDR), withdrawal time, and BBPS scores. Adenomas counted toward the ADR were only conventional adenomas. Missed adenomas/polyps were defined as those detected on a second examination of the proximal colon.
Sample size calculation
Recent study found that the proximal colon ADR in the 6-minute withdrawal time group was 11.9% (20 21,22 14
Statistical analysis
Statistical analyses were performed using SPSS version 25.0 (SPSS, Chicago, IL). All data were analyzed according to the intention-to-treat (ITT) analysis, and the per-protocol (PP) analysis was performed for the outcomes. Continuous variables were reported as the mean ± SD for data with a normal distribution, or the median with interquartile range for data with a skewed distribution and compared using the Student t test or the Mann–Whitney U test, respectively. Categorical variables were expressed as percentages and compared using the χ2 test or Fisher exact test. A P value of <0.05 was considered statistically significant. Logistic regression analysis was used to identify predictive factors for detecting ≥1 adenoma on the second withdrawal from the proximal colon.
RESULTS
Study population and baseline characteristics
A total of 924 patients were assessed for study eligibility between June 2021 and June 2022. Eighty-four patients were excluded. Finally, 840 patients were enrolled for ITT analysis, of whom 5 and 4 were excluded from the PP analysis in the 2 groups because of polyp retrieval failure (Figure 1 ). The baseline characteristics of all included patients are summarized in Table 1 . No statistically significant differences were found between the 2 groups.
Figure 1.: Flow diagram of the study presented according to the CONSORT statement.
Table 1. -
Patient baseline characteristics according to the intention-to-treat analysis
Intervention group (n = 420)
Control group (n = 420)
P value
Age, yr, mean ± SD
51.1 ± 11.9
50.8 ± 12.4
0.773
Sex, male, n (%)
211 (50.2)
220 (52.4)
0.534
BMI, kg/m2 , mean ± SD
23.2 ± 3.1
23.4 ± 3.3
0.308
Smoking, n (%)
105 (25.0)
106 (25.2)
0.937
Diabetes, n (%)
40 (9.5)
51 (12.1)
0.222
Hypertension, n (%)
81 (19.3)
92 (21.9)
0.348
Colonoscopy findings
The colonoscopy findings are presented in Table 2 . The indications for colonoscopy examination and the median BBPS scores in the segment of the colon did not differ between the 2 groups. The median withdrawal time of the first proximal colon examination was also not significantly different between the 2 groups (4.3 [4.0–4.7] vs 4.3 [4.0–4.8] minutes, P = 0.469). The median withdrawal time of the second proximal colon examination was 3.1 (2.7–3.4) minutes. The median total proximal colon withdrawal time (7.4 [6.8–8.0] vs 4.3 [4.0–4.8] minutes, P < 0.001) and the median whole-colon withdrawal time (10.2 [9.4–11] vs 7.3 [6.6–8.1] minutes, P < 0.001) were longer in the intervention group. The median time of the second insertion into the cecum was 0.4 (0.3–0.5) minutes. When the first and second cecal intubation times were also included, the total colonoscopy time was significantly longer in the intervention group than in the control group (13.5 [12.4–14.7] vs 10.2 [9.0–11.5] minutes, P < 0.001). The type of sedation of all the patients was intravenous anesthesia. The average amount of propofol used was 237.1 ± 61.6 (range 140–580) mg in the intervention group (n = 389) and 228.7 ± 61.5 (range 120–550) mg in the control group (n = 374) (P = 0.059). Regarding the adverse events, 1 patient in the intervention group had postpolypectomy bleeding requiring endoscopic hemostasis, and this was considered irrelevant to the second examination.
Table 2. -
Colonoscopy details comparison in the intention-to-treat analysis
Intervention group (n = 420)
Control group (n = 420)
P value
Indication of colonoscopy, n (%)
0.443
Screening
166 (39.5)
150(35.7)
Surveillance
115 (27.4)
129 (30.7)
Diagnostic
139 (33.1)
141 (33.6)
Quality of bowel preparation by BBPS, median (IQR)
Right-sided colon
2 (2–3)
2 (2–3)
0.527
Transverse colon
3 (2–3)
3 (2–3)
0.163
Left-sided colon
3 (3–3)
3 (3–3)
0.333
Proximal colon
5 (4–6)
5 (4–6)
0.716
Whole colon
8 (7–9)
8 (7–9)
0.656
Cecal intubation time, min, median (IQR)
2.7 (2.1–3.7)
2.7 (2.1–3.7)
0.737
Withdrawal time, min, median (IQR)
First proximal colon examination
4.3 (4.0–4.7)
4.3 (4.0–4.8)
0.469
Second proximal colon examination
3.1 (2.7–3.4)
—
—
Total proximal colon examination
7.4 (6.8–8.0)
4.3 (4.0–4.8)
<0.001
Left-sided colon examination
2.7 (2.2–3.2)
2.9 (2.5–3.5)
<0.001
Whole-colon examination
10.2 (9.4–11)
7.3 (6.6–8.1)
<0.001
Adverse event, n (%)
1
a
0
0.500
No. of colonoscopy, n (%)
0.843
E1
338 (80.5)
335 (79.8)
E2
43 (10.2)
48 (11.4)
E3
39 (9.3)
37 (8.8)
BBPS, Boston Bowel Preparation Scale; E, endoscopist; IQR, interquartile range.
a One patient with postpolypectomy bleeding requiring endoscopic hemostasis.
Adenoma and polyp detection rates
The ITT analysis showed that the proximal colon ADR in the intervention group was significantly higher than that in the control group (35.7% vs 25.2%, P = 0.001), and the whole-colon ADR was also higher in the intervention group (44.0% vs 34.0%, P = 0.003) (Table 3 ). In addition, there was an increase in the proximal colon PDR (55.0% vs 41.2%, P < 0.001) and whole-colon PDR (67.6% vs 60.2%, P = 0.026) in the intervention group. The higher ADR and PDR were also confirmed by the PP analysis (see Supplementary Table 1, Supplementary Digital Content 1, https://links.lww.com/CTG/A899 https://links.lww.com/CTG/A899 P = 0.001). The mean number of additional adenomas on the second examination was 0.19 (80 of 420).
Table 3. -
Detection of adenoma and polyp according to the intention-to-treat analysis
Intervention group (n = 420)
Control group (n = 420)
P value
Patients with ≥1 adenoma, n (%)
First proximal colon examination
107 (25.5)
106 (25.2)
0.937
Second proximal colon examination
70 (16.7)
—
—
Total proximal colon examination (proximal colon ADR)
150 (35.7)
106 (25.2)
0.001
Left-sided colon examination (left-sided colon ADR)
79 (18.8)
74 (17.6)
0.655
Whole-colon examination (whole-colon ADR)
185 (44.0)
143 (34.0)
0.003
No. of adenomas
First proximal colon examination
156
152
0.907
Second proximal colon examination
80
—
Total proximal colon examination
236
152
0.001
Whole-colon examination
346
248
0.003
The adenoma miss rate of the proximal colon (%)
33.9 (80/236)
Patients with ≥1 polyp, n (%)
First proximal colon examination
182 (43.3)
173 (41.2)
0.530
Second proximal colon examination
120 (28.6)
—
Total proximal colon examination (proximal colon PDR)
231 (55.0)
173 (41.2)
<0.001
Whole-colon examination (whole-colon PDR)
284 (67.6)
253 (60.2)
0.026
No. of polyps
First proximal colon examination
328
319
0.665
Second proximal colon examination
167
—
Total proximal colon examination
495
319
<0.001
Whole-colon examination
755
583
0.002
The polyp miss rate of the proximal colon (%)
33.7 (167/495)
ADR, adenoma detection rate; PDR, polyp detection rate.
Characteristics of adenomas detected on the second examination of the proximal colon
The second examination of the proximal colon found 80 additional adenomas in 70 patients (16.7%) (Table 4 ). The adenoma miss rate of the proximal colon was 33.9% (80 of 236) (Table 3 ). The mean size of adenomas found in the proximal colon on the first examination was 4.9 ± 2.3 mm (range 2–18 mm) in the intervention group and 4.7 ± 2.3 mm (range 2–16 mm) in the control group (P = 0.427). In the intervention group, the mean size of adenomas found in the proximal colon on the second examination was less than that on the first examination (4.2 ± 2.2 mm vs 4.9 ± 2.3 mm, P = 0.012). Among the 80 additional adenomas, most (96.3%) of the adenomas were <10 mm in size, and 100% were slightly elevated or sessile in morphology. A total of 100% were tubular adenomas. Adenoma with high-grade dysplasia was not found (Table 4 ).
Table 4. -
Characteristics of adenomas detected in the proximal colon between the intervention group and control group
Intervention group
Control group (n = 152)
First examination (n = 156)
Second examination (n = 80)
Size, mm, mean ± SD
4.9 ± 2.3
4.2 ± 2.2
4.7 ± 2.3
Polyps by size, mm, n (%)
≤5
102 (65.4)
64 (80.0)
106 (69.7)
6–9
46 (29.5)
13 (16.3)
36 (23.7)
≥10
8 (5.1)
3 (3.7)
10 (6.6)
Morphology, n (%)
Pedunculated (0–Ip)
3 (2.0)
0
2 (1.3)
Sessile (0–Is)
57 (36.5)
20 (25)
57 (37.5)
Slightly elevated (0–IIa)
96 (61.5)
60 (75)
93 (61.2)
Histology, n (%)
Villous adenoma
0
0
0
Tubulovillous adenoma
1 (0.6)
0
7 (4.6)
Tubular adenoma
155 (99.4)
80 (100)
145 (95.4)
Grade of dysplasia, n (%)
Adenoma with low-grade dysplasia
156 (100)
80 (100)
152 (100)
Adenoma with high-grade dysplasia
0
0
0
Alteration in surveillance recommendations after second examination
According to a consensus update by the US Multi-Society Task Force on Colorectal Cancer (19 Table 5 ), and 11 (2.6%) experienced a change from no-risk or low-risk to high-risk adenoma.
Table 5. -
Change in surveillance recommendation after second examination
Alteration in surveillance recommendations after second examination based on the USMSTF
Intervention group (n = 420)
Adenoma was found only on the second examination
32
Third adenoma was found
8
Fifth adenoma was found
1
Adenoma with size ≥10 mm, with tubulovillous or villous histology, or with high-grade dysplasia was found on the second examination
3
a
Patients whose surveillance recommendations changed after second examination, n (%)
41 (9.8)
USMSTF, US Multi-Society Task Force.
a Adenoma was found only on the second examination.
Predictive factors of detecting ≥1 adenoma on the second withdrawal from the proximal colon
On univariate analysis, older age, proximal colon withdrawal time of the first examination and second examination, total proximal colon withdrawal time, and adenoma detected on the first proximal colon examination were associated with adenomas detected on the second examination of the proximal colon. On multivariate logistic regression analysis, older age, adenoma detected on the first proximal colon examination, and longer total proximal colon withdrawal time were independent predictive factors for detecting ≥1 adenoma on the second withdrawal from the proximal colon (Table 6 ).
Table 6. -
Predictive factors of detecting ≥1 adenoma on the second withdrawal from the proximal colon
Univariate analysis
P value
Multivariate analysis
P value
Indication of colonoscopy
Screening
1
—
—
Nonscreening
1.525 (0.882–2.637)
0.129
—
—
Age, yr
≤50
1
1
>50
2.594 (1.471–4.572)
0.001
2.227 (1.247–3.976)
0.007
Sex
Female
1
—
—
Male
1.059 (0.634–1.769)
0.827
—
—
Smoking
No
1
—
—
Yes
1.046 (0.581–1.884)
0.880
—
—
Diabetes
No
1
—
—
Yes
1.282 (0.564–2.915)
0.552
—
—
Hypertension
No
1
—
—
Yes
1.299 (0.699–2.414)
0.407
—
—
BMI
1.030 (0.949–1.118)
0.481
—
—
Proximal colon BBPS
1.324 (0.968–1.810)
0.065
—
—
Withdrawal time, min
First proximal colon examination
1.007 (1.001–1.013)
0.034
—
—
Second proximal colon examination
1.009 (1.003–1.016)
0.007
—
—
Total proximal colon examination
1.007 (1.002–1.011)
0.002
1.006 (1.002–1.010)
0.007
Adenoma detected on the first proximal colon examination
No
1
1
Yes
2.119 (1.232–3.644)
0.006
1.914 (1.094–3.346)
0.023
BBPS, Boston Bowel Preparation Scale; BMI, body mass index; CI, confidence interval; OR, odds ratio.
DISCUSSION
In this RCT, we found that the second examination of the proximal colon can significantly increase the proximal colon ADR (35.7% vs 25.2%, P = 0.001) and the whole-colon ADR (44.0% vs 34.0%%, P = 0.003). In addition, there was an increase in the proximal colon PDR (55.0% vs 41.2%, P < 0.001) and whole-colon PDR (67.6% vs 60.2%, P = 0.026). Recently, several RCTs have been published assessing the impact of a second examination on adenoma detection compared with a single forward view examination (14,23–25 14
The results of our study suggest that the second examination of the proximal colon resulted in a 10.5% increase in the proximal colon ADR compared with the control group and a 10.2% increase in the proximal colon ADR compared with the first proximal colon examination of the intervention group. Notably, the median withdrawal time of the first proximal colon examination was 4.3 minutes in both groups. Based on previous findings, the proximal colon ADR was significantly increased when the proximal colon withdrawal time was ≥4 minutes compared with <4 minutes (26,27 14 15,25
The second examination of the proximal colon found 80 additional adenomas in 70 patients (16.7%). Most (96.3%) of the adenomas were <10 mm in size, and the characteristics were consistent with those described in previous studies (14,15 14,28,29
In this study, there was a 10.0% increase in the whole-colon ADR after the second examination of the proximal colon (44.0% vs 34.0%, P = 0.003). Our study further found that the left-sided colon ADR was not different between the 2 groups (18.8% vs 17.6%, P = 0.655), although the median left-sided colon withdrawal time in the intervention group was 0.2 minutes shorter (2.7 vs 2.9 minutes, P < 0.001). Indeed, the association between withdrawal time and ADR was weaker in the distal colon than in the proximal colon (26 20 30,31
On logistic regression analysis, older age, adenoma detected on the first proximal colon examination, and longer total proximal colon withdrawal time were independent predictive factors for detecting ≥1 adenoma on the second withdrawal from the proximal colon. Our results were different from those described by Guo et al. (14 14 21,22,25,32
Our study has several limitations. First, the study was a single-center design, which may limit generalizability. Therefore, future studies will require a multicenter design to gain more accurate information. Second, we included colonoscopies for any indications, and the calculation of ADR was not restricted to a screening indication. However, recent studies have shown that ADR measurement can include surveillance, diagnostics, and screening colonoscopies (33 1
In conclusion, second examination in the proximal colon significantly increased the proximal colon ADR and the whole-colon ADR. Therefore, this simple and reliable technique should be considered during a routine colonoscopy.
CONFLICTS OF INTEREST
Guarantor of the article: Li Yang, MD.
Specific author contributions: Q.Y.Y. and X.J.Z. designed the study, analyzed the data, and wrote the manuscript. Z.X.W. and F.L. collected the data. X.S. and L.Y. supervised this study. All authors read and approved the final manuscript.
Financial support: This study was supported by grants from the National Natural Science Foundation of China (Grant No. 81860108, PI: X.S.).
Potential competing interests: None to report.Study Highlights
WHAT IS KNOWN
✓ Interval colorectal cancer (CRC) identified before the next surveillance colonoscopy was more likely to be located in the proximal colon.
✓ Previous studies have reported that the adenoma detection rate (ADR) is inversely associated with the risk of interval CRC.
WHAT IS NEW HERE
✓ Second examination of the proximal colon significantly increased the proximal colon ADR and whole-colon ADR in patients undergoing colonoscopy for any indication.
✓ This simple and reliable technique should be considered during a routine colonoscopy.
ACKNOWLEDGMENT
We thank Xu Shu for providing the funding by grants from the National Natural Science Foundation of China for this writing assistance.
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